Skip to main content
Top
Published in: Seminars in Immunopathology 6/2018

01-11-2018 | Review

Macrophage-microbe interaction: lessons learned from the pathogen Mycobacterium tuberculosis

Authors: Somdeb BoseDasgupta, Jean Pieters

Published in: Seminars in Immunopathology | Issue 6/2018

Login to get access

Abstract

Macrophages, being the cornerstone of the immune system, have adapted the ancient nutrient acquisition mechanism of phagocytosis to engulf various infectious organisms thereby helping to orchestrate an appropriate host response. Phagocytosis refers to the process of internalization and degradation of particulate material, damaged and senescent cells and microorganisms by specialized cells, after which the vesicle containing the ingested particle, the phagosome, matures into acidic phagolysosomes upon fusion with hydrolytic enzyme-containing lysosomes. The destructive power of the macrophage is further exacerbated through the induction of macrophage activation upon a variety of inflammatory stimuli. Despite being the end-point for many phagocytosed microbes, the macrophage can also serve as an intracellular survival niche for a number of intracellular microorganisms. One microbe that is particularly successful at surviving within macrophages is the pathogen Mycobacterium tuberculosis, which can efficiently manipulate the macrophage at several levels, including modulation of the phagocytic pathway as well as interfering with a number of immune activation pathways that normally would lead to eradication of the internalized bacilli. M. tuberculosis excels at circumventing destruction within macrophages, thus establishing itself successfully for prolonged times within the macrophage. In this contribution, we describe a number of general features of macrophages in the context of their function to clear an infection, and highlight the strategies employed by M. tuberculosis to counter macrophage attack. Interestingly, research on the evasion tactics employed by M. tuberculosis within macrophages not only helps to design strategies to curb tuberculosis, but also allows a better understanding of host cell biology.
Literature
1.
go back to reference Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17(1):593–623PubMedCrossRef Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17(1):593–623PubMedCrossRef
3.
go back to reference Snelgrove RJ, Goulding J, Didierlaurent AM, Lyonga D, Vekaria S, Edwards L, Gwyer E, Sedgwick JD, Barclay AN, Hussell T (2008) A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat Immunol 9(9):1074–1083PubMedCrossRef Snelgrove RJ, Goulding J, Didierlaurent AM, Lyonga D, Vekaria S, Edwards L, Gwyer E, Sedgwick JD, Barclay AN, Hussell T (2008) A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat Immunol 9(9):1074–1083PubMedCrossRef
4.
go back to reference Wert SE, Yoshida M, LeVine AM, Ikegami M, Jones T, Ross GF, Fisher JH, Korfhagen TR, Whitsett JA (2000) Increased metalloproteinase activity, oxidant production, and emphysema in surfactant protein D gene-inactivated mice. Proc Natl Acad Sci U S A 97(11):5972–5977PubMedPubMedCentralCrossRef Wert SE, Yoshida M, LeVine AM, Ikegami M, Jones T, Ross GF, Fisher JH, Korfhagen TR, Whitsett JA (2000) Increased metalloproteinase activity, oxidant production, and emphysema in surfactant protein D gene-inactivated mice. Proc Natl Acad Sci U S A 97(11):5972–5977PubMedPubMedCentralCrossRef
5.
go back to reference Dixon LJ, Barnes M, Tang H, Pritchard MT, Nagy LE (2013) Kupffer cells in the liver, comprehensive physiology, Wiley Dixon LJ, Barnes M, Tang H, Pritchard MT, Nagy LE (2013) Kupffer cells in the liver, comprehensive physiology, Wiley
6.
go back to reference Klei TRL, Meinderts SM, van den Berg TK, van Bruggen R (2017) From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Front Immunol 8:73PubMedPubMedCentralCrossRef Klei TRL, Meinderts SM, van den Berg TK, van Bruggen R (2017) From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Front Immunol 8:73PubMedPubMedCentralCrossRef
7.
go back to reference Ruggiero MG, Ferretti L, Glomski C, Pica A (2013) Erythrophagocytosis in circulating blood of loggerhead turtles Caretta caretta: the pitting of Heinz bodies. J Exp Zool A Ecol Genet Physiol 321(3):144–150PubMedCrossRef Ruggiero MG, Ferretti L, Glomski C, Pica A (2013) Erythrophagocytosis in circulating blood of loggerhead turtles Caretta caretta: the pitting of Heinz bodies. J Exp Zool A Ecol Genet Physiol 321(3):144–150PubMedCrossRef
8.
go back to reference de Back DZ, Kostova EB, van Kraaij M, van den Berg TK, van Bruggen R (2014) Of macrophages and red blood cells; a complex love story. Front Physiol 5:9PubMedPubMedCentral de Back DZ, Kostova EB, van Kraaij M, van den Berg TK, van Bruggen R (2014) Of macrophages and red blood cells; a complex love story. Front Physiol 5:9PubMedPubMedCentral
9.
go back to reference Manwani D, Bieker JJ (2008) Chapter 2 the erythroblastic island. Red cell development. Elsevier, pp 23–53 Manwani D, Bieker JJ (2008) Chapter 2 the erythroblastic island. Red cell development. Elsevier, pp 23–53
11.
go back to reference Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M (2012) Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 229(2):176–185PubMedCrossRef Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M (2012) Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 229(2):176–185PubMedCrossRef
12.
go back to reference Rabinovitch M (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5(3):85–87PubMedCrossRef Rabinovitch M (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5(3):85–87PubMedCrossRef
13.
go back to reference Dersch P (2002) Molecular and cellular mechanisms of bacterial entry into host cells, contributions to microbiology. KARGER, pp 183–209 Dersch P (2002) Molecular and cellular mechanisms of bacterial entry into host cells, contributions to microbiology. KARGER, pp 183–209
14.
go back to reference Kaufmann SHE, Dorhoi A (2016) Molecular determinants in phagocyte-bacteria interactions. Immunity 44(3):476–491PubMedCrossRef Kaufmann SHE, Dorhoi A (2016) Molecular determinants in phagocyte-bacteria interactions. Immunity 44(3):476–491PubMedCrossRef
15.
go back to reference Sarantis H, Grinstein S (2012) Subversion of phagocytosis for pathogen survival. Cell Host Microbe 12(4):419–431PubMedCrossRef Sarantis H, Grinstein S (2012) Subversion of phagocytosis for pathogen survival. Cell Host Microbe 12(4):419–431PubMedCrossRef
16.
go back to reference Mitchell G, Chen C, Portnoy DA (2016) Strategies used by bacteria to grow in macrophages. Microbiol Spectr 4(3)MCHD-0012-2015 Mitchell G, Chen C, Portnoy DA (2016) Strategies used by bacteria to grow in macrophages. Microbiol Spectr 4(3)MCHD-0012-2015
17.
go back to reference Woolard MD, Frelinger JA (2008) Outsmarting the host: bacteria modulating the immune response. Immunol Res 41(3):188–202PubMedCrossRef Woolard MD, Frelinger JA (2008) Outsmarting the host: bacteria modulating the immune response. Immunol Res 41(3):188–202PubMedCrossRef
18.
go back to reference Andersson K, Carballeira N, Magnusson K-E, Persson C, Stendahl O, Wolf-Watz H, Fällman M (1996) YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol Microbiol 20(5):1057–1069PubMedCrossRef Andersson K, Carballeira N, Magnusson K-E, Persson C, Stendahl O, Wolf-Watz H, Fällman M (1996) YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol Microbiol 20(5):1057–1069PubMedCrossRef
19.
go back to reference McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12(1):117–124PubMedPubMedCentralCrossRef McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12(1):117–124PubMedPubMedCentralCrossRef
20.
go back to reference Kaniga K, Uralil J, Bliska JB, Galán JE (1996) A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurlum. Mol Microbiol 21(3):633–641PubMedCrossRef Kaniga K, Uralil J, Bliska JB, Galán JE (1996) A secreted protein tyrosine phosphatase with modular effector domains in the bacterial pathogen Salmonella typhimurlum. Mol Microbiol 21(3):633–641PubMedCrossRef
21.
go back to reference Fu Y, Galan JE (1999) A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401(6750):293–297PubMedCrossRef Fu Y, Galan JE (1999) A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401(6750):293–297PubMedCrossRef
22.
go back to reference Johnson R, Byrne A, Berger CN, Klemm E, Crepin VF, Dougan G, Frankel G (2017) The type III secretion system effector SptP of Salmonella enterica Serovar Typhi. J Bacteriol 199(4) Johnson R, Byrne A, Berger CN, Klemm E, Crepin VF, Dougan G, Frankel G (2017) The type III secretion system effector SptP of Salmonella enterica Serovar Typhi. J Bacteriol 199(4)
23.
go back to reference Bakowski MA, Braun V, Lam GY, Yeung T, Do Heo W, Meyer T, Finlay BB, Grinstein S, Brumell JH (2010) The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe 7(6):453–462PubMedCrossRef Bakowski MA, Braun V, Lam GY, Yeung T, Do Heo W, Meyer T, Finlay BB, Grinstein S, Brumell JH (2010) The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe 7(6):453–462PubMedCrossRef
24.
go back to reference Konradt C, Frigimelica E, Nothelfer K, Puhar A, Salgado-Pabon W, di Bartolo V, Scott-Algara D, Cristina D, Rodrigues PJ, Sansonetti AP (2011) The Shigella flexneri type three secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 9(4):263–272PubMedCrossRef Konradt C, Frigimelica E, Nothelfer K, Puhar A, Salgado-Pabon W, di Bartolo V, Scott-Algara D, Cristina D, Rodrigues PJ, Sansonetti AP (2011) The Shigella flexneri type three secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 9(4):263–272PubMedCrossRef
25.
go back to reference Hsu F, Mao Y (2015) The structure of phosphoinositide phosphatases: insights into substrate specificity and catalysis. Biochim Biophys Acta Mol Cell Biol Lipids 1851(6):698–710CrossRef Hsu F, Mao Y (2015) The structure of phosphoinositide phosphatases: insights into substrate specificity and catalysis. Biochim Biophys Acta Mol Cell Biol Lipids 1851(6):698–710CrossRef
26.
go back to reference Ibarra JA, Steele-Mortimer O (2009) Salmonella- the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11(11):1579–1586PubMedPubMedCentralCrossRef Ibarra JA, Steele-Mortimer O (2009) Salmonella- the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11(11):1579–1586PubMedPubMedCentralCrossRef
27.
go back to reference Haraga A, West TE, Brittnacher MJ, Skerrett SJ, Miller SI (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated type III secretion system of Burkholderia pseudomallei. Infect Immun 76(11):5402–5411PubMedPubMedCentralCrossRef Haraga A, West TE, Brittnacher MJ, Skerrett SJ, Miller SI (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated type III secretion system of Burkholderia pseudomallei. Infect Immun 76(11):5402–5411PubMedPubMedCentralCrossRef
28.
go back to reference Castro-Gomes T, Cardoso MS, DaRocha WD, Laibida LA, Nascimento AMA, Zuccherato LW, Horta MF, Bemquerer MP, Teixeira SMR (2014) Identification of secreted virulence factors of Chromobacterium violaceum. J Microbiol 52(4):350–353PubMedCrossRef Castro-Gomes T, Cardoso MS, DaRocha WD, Laibida LA, Nascimento AMA, Zuccherato LW, Horta MF, Bemquerer MP, Teixeira SMR (2014) Identification of secreted virulence factors of Chromobacterium violaceum. J Microbiol 52(4):350–353PubMedCrossRef
29.
go back to reference Theriot JA (1995) The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11:213PubMedCrossRef Theriot JA (1995) The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11:213PubMedCrossRef
30.
go back to reference Radoshevich L, Cossart P (2018) Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat Rev Microbiol 16(1):32–46PubMedCrossRef Radoshevich L, Cossart P (2018) Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat Rev Microbiol 16(1):32–46PubMedCrossRef
31.
go back to reference Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, Chretien F, Heitman J, Dromer F, Nielsen K (2010) Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6(6):e1000953PubMedPubMedCentralCrossRef Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, Chretien F, Heitman J, Dromer F, Nielsen K (2010) Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6(6):e1000953PubMedPubMedCentralCrossRef
32.
go back to reference Zaragoza O, Garcia-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodriguez-Tudela JL, Casadevall A (2010) Fungal cell gigantism during mammalian infection. PLoS Pathog 6(6):e1000945PubMedPubMedCentralCrossRef Zaragoza O, Garcia-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodriguez-Tudela JL, Casadevall A (2010) Fungal cell gigantism during mammalian infection. PLoS Pathog 6(6):e1000945PubMedPubMedCentralCrossRef
34.
go back to reference Dorhoi A, Kaufmann SH (2016) Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis. Semin Immunopathol 38(2):153–166PubMedCrossRef Dorhoi A, Kaufmann SH (2016) Pathology and immune reactivity: understanding multidimensionality in pulmonary tuberculosis. Semin Immunopathol 38(2):153–166PubMedCrossRef
35.
go back to reference Stutz MD, Clark MP, Doerflinger M, Pellegrini M (2017) Mycobacterium tuberculosis : rewiring host cell signaling to promote infection. J Leukoc Biol 103(2):259–268PubMedCrossRef Stutz MD, Clark MP, Doerflinger M, Pellegrini M (2017) Mycobacterium tuberculosis : rewiring host cell signaling to promote infection. J Leukoc Biol 103(2):259–268PubMedCrossRef
36.
go back to reference Henderson HJ, Dannenberg AM Jr, Lurie MB (1963) Phagocytosis of tubercle bacilli by rabbit pulmonary alveolar macrophages and its relation to native resistance to tuberculosis. J Immunol (91):553–556 Henderson HJ, Dannenberg AM Jr, Lurie MB (1963) Phagocytosis of tubercle bacilli by rabbit pulmonary alveolar macrophages and its relation to native resistance to tuberculosis. J Immunol (91):553–556
37.
go back to reference Teitelbaum R, Schubert W, Gunther L, Kress Y, Macaluso F, Pollard JW, McMurray DN, Bloom BR (1999) The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis. Immunity 10(6):641–650PubMedCrossRef Teitelbaum R, Schubert W, Gunther L, Kress Y, Macaluso F, Pollard JW, McMurray DN, Bloom BR (1999) The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis. Immunity 10(6):641–650PubMedCrossRef
38.
go back to reference Cambier CJ, O’Leary SM, O’Sullivan MP, Keane J, Ramakrishnan L (2017) Phenolic glycolipid facilitates mycobacterial escape from microbicidal tissue-resident macrophages. Immunity 47(3):552–565PubMedPubMedCentralCrossRef Cambier CJ, O’Leary SM, O’Sullivan MP, Keane J, Ramakrishnan L (2017) Phenolic glycolipid facilitates mycobacterial escape from microbicidal tissue-resident macrophages. Immunity 47(3):552–565PubMedPubMedCentralCrossRef
40.
go back to reference Pieters J (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3(6):399–407PubMedCrossRef Pieters J (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3(6):399–407PubMedCrossRef
41.
go back to reference Talaue MT, Venketaraman V, Hazbon MH, Peteroy-Kelly M, Seth A, Colangeli R, Alland D, Connell ND (2006) Arginine homeostasis in J774.1 macrophages in the context of Mycobacterium bovis BCG infection. J Bacteriol 188(13):4830–4840PubMedPubMedCentralCrossRef Talaue MT, Venketaraman V, Hazbon MH, Peteroy-Kelly M, Seth A, Colangeli R, Alland D, Connell ND (2006) Arginine homeostasis in J774.1 macrophages in the context of Mycobacterium bovis BCG infection. J Bacteriol 188(13):4830–4840PubMedPubMedCentralCrossRef
42.
go back to reference Das P, Lahiri A, Lahiri A, Chakravortty D (2010) Modulation of the arginase pathway in the context of microbial pathogenesis: a metabolic enzyme moonlighting as an immune modulator. PLoS Pathog 6(6):e1000899PubMedPubMedCentralCrossRef Das P, Lahiri A, Lahiri A, Chakravortty D (2010) Modulation of the arginase pathway in the context of microbial pathogenesis: a metabolic enzyme moonlighting as an immune modulator. PLoS Pathog 6(6):e1000899PubMedPubMedCentralCrossRef
43.
go back to reference Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97(16):8841–8848PubMedPubMedCentralCrossRef Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97(16):8841–8848PubMedPubMedCentralCrossRef
44.
go back to reference Reiling N, Blumenthal A, Flad HD, Ernst M, Ehlers S (2001) Mycobacteria-induced TNF- and IL-10 formation by human macrophages is differentially regulated at the level of mitogen-activated protein kinase activity. J Immunol 167(6):3339–3345PubMedCrossRef Reiling N, Blumenthal A, Flad HD, Ernst M, Ehlers S (2001) Mycobacteria-induced TNF- and IL-10 formation by human macrophages is differentially regulated at the level of mitogen-activated protein kinase activity. J Immunol 167(6):3339–3345PubMedCrossRef
46.
go back to reference Peranzoni E, Marigo I, Dolcetti L, Ugel S, Sonda N, Taschin E, Mantelli B, Bronte V, Zanovello P (2007) Role of arginine metabolism in immunity and immunopathology. Immunobiology 212(9–10):795–812PubMed Peranzoni E, Marigo I, Dolcetti L, Ugel S, Sonda N, Taschin E, Mantelli B, Bronte V, Zanovello P (2007) Role of arginine metabolism in immunity and immunopathology. Immunobiology 212(9–10):795–812PubMed
47.
go back to reference McClean CM, Tobin DM (2016) Macrophage form, function, and phenotype in mycobacterial infection: lessons from tuberculosis and other diseases. Pathog Dis 74(7):ftw068PubMedPubMedCentralCrossRef McClean CM, Tobin DM (2016) Macrophage form, function, and phenotype in mycobacterial infection: lessons from tuberculosis and other diseases. Pathog Dis 74(7):ftw068PubMedPubMedCentralCrossRef
48.
go back to reference Fratazzi C, Arbeit RD, Carini C, Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG (1999) Macrophage apoptosis in mycobacterial infections. J Leukoc Biol 66(5):763–764PubMedCrossRef Fratazzi C, Arbeit RD, Carini C, Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG (1999) Macrophage apoptosis in mycobacterial infections. J Leukoc Biol 66(5):763–764PubMedCrossRef
49.
go back to reference van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129(7):1287–1298PubMedCrossRef van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129(7):1287–1298PubMedCrossRef
50.
go back to reference Sundaramurthy V, Korf H, Singla A, Scherr N, Nguyen L, Ferrari G, Landmann R, Huygen K, Pieters J (2017) Survival of Mycobacterium tuberculosis and Mycobacterium bovis BCG in lysosomes in vivo. Microbes Infect 19(11):515–526PubMedCrossRef Sundaramurthy V, Korf H, Singla A, Scherr N, Nguyen L, Ferrari G, Landmann R, Huygen K, Pieters J (2017) Survival of Mycobacterium tuberculosis and Mycobacterium bovis BCG in lysosomes in vivo. Microbes Infect 19(11):515–526PubMedCrossRef
51.
go back to reference Levitte S, Adams KN, Berg RD, Cosma CL, Urdahl KB, Ramakrishnan L (2016) Mycobacterial acid tolerance enables phagolysosomal survival and establishment of tuberculous infection in vivo. Cell Host Microbe 20(2):250–258PubMedPubMedCentralCrossRef Levitte S, Adams KN, Berg RD, Cosma CL, Urdahl KB, Ramakrishnan L (2016) Mycobacterial acid tolerance enables phagolysosomal survival and establishment of tuberculous infection in vivo. Cell Host Microbe 20(2):250–258PubMedPubMedCentralCrossRef
52.
go back to reference Kim M-J, Wainwright HC, Locketz M, Bekker L-G, Walther GB, Dittrich C, Visser A, Wang W, Hsu F-F, Wiehart U, Tsenova L, Kaplan G, Russell DG (2010) Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2(7):258–274PubMedPubMedCentralCrossRef Kim M-J, Wainwright HC, Locketz M, Bekker L-G, Walther GB, Dittrich C, Visser A, Wang W, Hsu F-F, Wiehart U, Tsenova L, Kaplan G, Russell DG (2010) Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2(7):258–274PubMedPubMedCentralCrossRef
53.
go back to reference Ramakrishnan L (2012) Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12(5):352–366PubMedCrossRef Ramakrishnan L (2012) Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 12(5):352–366PubMedCrossRef
54.
go back to reference Russell DG, Cardona P-J, Kim M-J, Allain S, Altare F (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10(9):943–948PubMedPubMedCentralCrossRef Russell DG, Cardona P-J, Kim M-J, Allain S, Altare F (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10(9):943–948PubMedPubMedCentralCrossRef
55.
go back to reference Ferguson JS, Weis JJ, Martin JL, Schlesinger LS (2004) Complement protein C3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human Bronchoalveolar lavage fluid. Infect Immun 72(5):2564–2573PubMedPubMedCentralCrossRef Ferguson JS, Weis JJ, Martin JL, Schlesinger LS (2004) Complement protein C3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human Bronchoalveolar lavage fluid. Infect Immun 72(5):2564–2573PubMedPubMedCentralCrossRef
56.
go back to reference Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, DesJardin LE, Schlesinger LS (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202(7):987–999PubMedPubMedCentralCrossRef Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, DesJardin LE, Schlesinger LS (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202(7):987–999PubMedPubMedCentralCrossRef
57.
go back to reference Pasula R, Downing JF, Wright JR, Kachel DL, Davis TE, Martin WJ (1997) Surfactant protein a (SP-A) mediates attachment of Mycobacterium tuberculosis to murine alveolar macrophages. Am J Respir Cell Mol Biol 17(2):209–217PubMedCrossRef Pasula R, Downing JF, Wright JR, Kachel DL, Davis TE, Martin WJ (1997) Surfactant protein a (SP-A) mediates attachment of Mycobacterium tuberculosis to murine alveolar macrophages. Am J Respir Cell Mol Biol 17(2):209–217PubMedCrossRef
58.
go back to reference Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA (1994) The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci 91(5):1863–1867PubMedCrossRefPubMedCentral Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA (1994) The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc Natl Acad Sci 91(5):1863–1867PubMedCrossRefPubMedCentral
59.
go back to reference Kumar SK, Singh P, Sinha S (2015) Naturally produced opsonizing antibodies restrict the survival of Mycobacterium tuberculosisin human macrophages by augmenting phagosome maturation. Open Biology 5(12):150171PubMedPubMedCentralCrossRef Kumar SK, Singh P, Sinha S (2015) Naturally produced opsonizing antibodies restrict the survival of Mycobacterium tuberculosisin human macrophages by augmenting phagosome maturation. Open Biology 5(12):150171PubMedPubMedCentralCrossRef
60.
61.
go back to reference Lu LL, Chung AW, Rosebrock TR, Ghebremichael M, Yu WH, Grace PS, Schoen MK, Tafesse F, Martin C, Leung V, Mahan AE, Sips M, Kumar MP, Tedesco J, Robinson H, Tkachenko E, Draghi M, Freedberg KJ, Streeck H, Suscovich TJ, Lauffenburger DA, Restrepo BI, Day C, Fortune SM, Alter G (2016) A functional role for antibodies in tuberculosis. Cell 167(2):433–443PubMedPubMedCentralCrossRef Lu LL, Chung AW, Rosebrock TR, Ghebremichael M, Yu WH, Grace PS, Schoen MK, Tafesse F, Martin C, Leung V, Mahan AE, Sips M, Kumar MP, Tedesco J, Robinson H, Tkachenko E, Draghi M, Freedberg KJ, Streeck H, Suscovich TJ, Lauffenburger DA, Restrepo BI, Day C, Fortune SM, Alter G (2016) A functional role for antibodies in tuberculosis. Cell 167(2):433–443PubMedPubMedCentralCrossRef
62.
go back to reference Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13PubMedCrossRef Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13PubMedCrossRef
63.
go back to reference Ferrandon D, Imler J-L, Hoffmann JA (2004) Sensing infection in Drosophila: toll and beyond. Semin Immunol 16(1):43–53PubMedCrossRef Ferrandon D, Imler J-L, Hoffmann JA (2004) Sensing infection in Drosophila: toll and beyond. Semin Immunol 16(1):43–53PubMedCrossRef
65.
66.
go back to reference Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197(1):121–127PubMedPubMedCentralCrossRef Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197(1):121–127PubMedPubMedCentralCrossRef
67.
go back to reference Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, Van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197(1):7–17PubMedPubMedCentralCrossRef Geijtenbeek TB, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CM, Appelmelk B, Van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197(1):7–17PubMedPubMedCentralCrossRef
68.
go back to reference Shams H, Wizel B, Lakey DL, Samten B, Vankayalapati R, Valdivia RH, Kitchens RL, Griffith DE, Barnes PF (2003) The CD14 receptor does not mediate entry of Mycobacterium tuberculosis into human mononuclear phagocytes. FEMS Immunology & Medical Microbiology 36(1–2):63–69CrossRef Shams H, Wizel B, Lakey DL, Samten B, Vankayalapati R, Valdivia RH, Kitchens RL, Griffith DE, Barnes PF (2003) The CD14 receptor does not mediate entry of Mycobacterium tuberculosis into human mononuclear phagocytes. FEMS Immunology & Medical Microbiology 36(1–2):63–69CrossRef
70.
go back to reference Yamashiro LH, Oliveira SC, Báfica A (2014) Innate immune sensing of nucleic acids from mycobacteria. Microbes Infect 16(12):991–997PubMedCrossRef Yamashiro LH, Oliveira SC, Báfica A (2014) Innate immune sensing of nucleic acids from mycobacteria. Microbes Infect 16(12):991–997PubMedCrossRef
71.
go back to reference Yadav M, Schorey JS (2006) The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108(9):3168–3175PubMedPubMedCentralCrossRef Yadav M, Schorey JS (2006) The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108(9):3168–3175PubMedPubMedCentralCrossRef
72.
go back to reference Armstrong JA, Hart PD (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134(3 Pt 1):713–740PubMedPubMedCentralCrossRef Armstrong JA, Hart PD (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134(3 Pt 1):713–740PubMedPubMedCentralCrossRef
73.
go back to reference Russell DG (2001) Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2(8):569–577PubMedCrossRef Russell DG (2001) Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2(8):569–577PubMedCrossRef
74.
go back to reference Nguyen L, Pieters J (2009) Mycobacterial subversion of chemotherapeutic reagents and host defense tactics: challenges in tuberculosis drug development. Annu Rev Pharmacol Toxicol 49:427–453PubMedCrossRef Nguyen L, Pieters J (2009) Mycobacterial subversion of chemotherapeutic reagents and host defense tactics: challenges in tuberculosis drug development. Annu Rev Pharmacol Toxicol 49:427–453PubMedCrossRef
75.
go back to reference Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678–681PubMedCrossRef Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678–681PubMedCrossRef
76.
go back to reference Warner DF, Mizrahi V (2007) The survival kit of Mycobacterium tuberculosis. Nat Med 13(3):282–284PubMedCrossRef Warner DF, Mizrahi V (2007) The survival kit of Mycobacterium tuberculosis. Nat Med 13(3):282–284PubMedCrossRef
77.
go back to reference Ferrari G, Langen H, Naito M, Pieters J (1999) A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97(4):435–447PubMedCrossRef Ferrari G, Langen H, Naito M, Pieters J (1999) A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97(4):435–447PubMedCrossRef
78.
go back to reference Gatfield J, Pieters J (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288(5471):1647–1651PubMedCrossRef Gatfield J, Pieters J (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288(5471):1647–1651PubMedCrossRef
79.
go back to reference Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, Huygen K, Miyazaki T, Albrecht I, Massner J, Pieters J (2007) Survival of mycobacteria in macrophages is mediated by Coronin 1-dependent activation of calcineurin. Cell 130(1):37–50PubMedCrossRef Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, Huygen K, Miyazaki T, Albrecht I, Massner J, Pieters J (2007) Survival of mycobacteria in macrophages is mediated by Coronin 1-dependent activation of calcineurin. Cell 130(1):37–50PubMedCrossRef
80.
go back to reference Pieters J, Müller P, Jayachandran R (2013) On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol 13(7):510–518PubMedCrossRef Pieters J, Müller P, Jayachandran R (2013) On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol 13(7):510–518PubMedCrossRef
81.
go back to reference BoseDasgupta S, Pieters J (2014) Coronin 1 trimerization is essential to protect pathogenic mycobacteria within macrophages from lysosomal delivery. FEBS Lett 588(21):3898–3905PubMedCrossRef BoseDasgupta S, Pieters J (2014) Coronin 1 trimerization is essential to protect pathogenic mycobacteria within macrophages from lysosomal delivery. FEBS Lett 588(21):3898–3905PubMedCrossRef
82.
go back to reference Kumar D, Nath L, Kamal MA, Varshney A, Jain A, Singh S, Rao KVS (2010) Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140(5):731–743PubMedCrossRef Kumar D, Nath L, Kamal MA, Varshney A, Jain A, Singh S, Rao KVS (2010) Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140(5):731–743PubMedCrossRef
83.
go back to reference Mueller P, Massner J, Jayachandran R, Combaluzier B, Albrecht I, Gatfield J, Blum C, Ceredig R, Rodewald H-R, Rolink AG, Pieters J (2008) Regulation of T cell survival through coronin-1–mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol 9(4):424–431PubMedCrossRef Mueller P, Massner J, Jayachandran R, Combaluzier B, Albrecht I, Gatfield J, Blum C, Ceredig R, Rodewald H-R, Rolink AG, Pieters J (2008) Regulation of T cell survival through coronin-1–mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol 9(4):424–431PubMedCrossRef
84.
go back to reference Shiow LR, Roadcap DW, Paris K, Watson SR, Grigorova IL, Lebet T, An J, Xu Y, Jenne CN, Föger N, Sorensen RU, Goodnow CC, Bear JE, Puck JM, Cyster JG (2008) The actin regulator coronin 1A is mutant in a thymic egress–deficient mouse strain and in a patient with severe combined immunodeficiency. Nat Immunol 9(11):1307–1315PubMedPubMedCentralCrossRef Shiow LR, Roadcap DW, Paris K, Watson SR, Grigorova IL, Lebet T, An J, Xu Y, Jenne CN, Föger N, Sorensen RU, Goodnow CC, Bear JE, Puck JM, Cyster JG (2008) The actin regulator coronin 1A is mutant in a thymic egress–deficient mouse strain and in a patient with severe combined immunodeficiency. Nat Immunol 9(11):1307–1315PubMedPubMedCentralCrossRef
85.
go back to reference Haraldsson MK, Louis-Dit-Sully CA, Lawson BR, Sternik G, Santiago-Raber ML, Gascoigne NR, Theofilopoulos AN, Kono DH (2008) The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity 28(1):40–51PubMedPubMedCentralCrossRef Haraldsson MK, Louis-Dit-Sully CA, Lawson BR, Sternik G, Santiago-Raber ML, Gascoigne NR, Theofilopoulos AN, Kono DH (2008) The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity 28(1):40–51PubMedPubMedCentralCrossRef
86.
go back to reference Lang MJ, Mori M, Ruer-Laventie J, Pieters J (2017) A Coronin 1–dependent decision switch in juvenile mice determines the population of the peripheral naive T cell compartment. J Immunol 199(7):2421–2431PubMedCrossRef Lang MJ, Mori M, Ruer-Laventie J, Pieters J (2017) A Coronin 1–dependent decision switch in juvenile mice determines the population of the peripheral naive T cell compartment. J Immunol 199(7):2421–2431PubMedCrossRef
87.
go back to reference Jayachandran R, Gatfield J, Massner J, Albrecht I, Zanolari B, Pieters J (2008) RNA interference in J774 macrophages reveals a role for Coronin 1 in mycobacterial trafficking but not in actin-dependent processes. Mol Biol Cell 19(3):1241–1251PubMedPubMedCentralCrossRef Jayachandran R, Gatfield J, Massner J, Albrecht I, Zanolari B, Pieters J (2008) RNA interference in J774 macrophages reveals a role for Coronin 1 in mycobacterial trafficking but not in actin-dependent processes. Mol Biol Cell 19(3):1241–1251PubMedPubMedCentralCrossRef
88.
go back to reference BoseDasgupta S, Pieters J (2014) Inflammatory stimuli reprogram macrophage phagocytosis to macropinocytosis for the rapid elimination of pathogens. PLoS Pathog 10(1):e1003879PubMedPubMedCentralCrossRef BoseDasgupta S, Pieters J (2014) Inflammatory stimuli reprogram macrophage phagocytosis to macropinocytosis for the rapid elimination of pathogens. PLoS Pathog 10(1):e1003879PubMedPubMedCentralCrossRef
89.
go back to reference Jeschke A, Haas A (2016) Deciphering the roles of phosphoinositide lipids in phagolysosome biogenesis. Communicative & integrative biology 9(3):e1174798CrossRef Jeschke A, Haas A (2016) Deciphering the roles of phosphoinositide lipids in phagolysosome biogenesis. Communicative & integrative biology 9(3):e1174798CrossRef
90.
go back to reference Bohdanowicz M, Grinstein S (2013) Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol Rev 93(1):69–106PubMedCrossRef Bohdanowicz M, Grinstein S (2013) Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol Rev 93(1):69–106PubMedCrossRef
91.
go back to reference Vieira OV, Harrison RE, Scott CC, Stenmark H, Alexander D, Liu J, Gruenberg J, Schreiber AD, Grinstein S (2004) Acquisition of Hrs, an essential component of phagosomal maturation is impaired by mycobacteria. Mol Cell Biol 24(10):4593–4604PubMedPubMedCentralCrossRef Vieira OV, Harrison RE, Scott CC, Stenmark H, Alexander D, Liu J, Gruenberg J, Schreiber AD, Grinstein S (2004) Acquisition of Hrs, an essential component of phagosomal maturation is impaired by mycobacteria. Mol Cell Biol 24(10):4593–4604PubMedPubMedCentralCrossRef
92.
go back to reference Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154(3):631–644PubMedPubMedCentralCrossRef Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154(3):631–644PubMedPubMedCentralCrossRef
93.
go back to reference Dickson EJ, Jensen JB, Hille B (2016) Regulation of calcium and phosphoinositides at endoplasmic reticulum–membrane junctions. Biochem Soc Trans 44(2):467–473PubMedPubMedCentralCrossRef Dickson EJ, Jensen JB, Hille B (2016) Regulation of calcium and phosphoinositides at endoplasmic reticulum–membrane junctions. Biochem Soc Trans 44(2):467–473PubMedPubMedCentralCrossRef
94.
go back to reference Burman C, Ktistakis NT (2010) Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett 584(7):1302–1312PubMedCrossRef Burman C, Ktistakis NT (2010) Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett 584(7):1302–1312PubMedCrossRef
95.
go back to reference Fairn GD, Grinstein S (2012) How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33(8):397–405PubMedCrossRef Fairn GD, Grinstein S (2012) How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33(8):397–405PubMedCrossRef
96.
97.
go back to reference Indrigo J, Hunter RL Jr, Actor JK (2003) Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149(Pt 8):2049–2059PubMedCrossRef Indrigo J, Hunter RL Jr, Actor JK (2003) Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149(Pt 8):2049–2059PubMedCrossRef
98.
go back to reference Axelrod S, Oschkinat H, Enders J, Schlegel B, Brinkmann V, Kaufmann SHE, Haas A, Schaible UE (2008) Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10(7):1530–1545PubMedCrossRef Axelrod S, Oschkinat H, Enders J, Schlegel B, Brinkmann V, Kaufmann SHE, Haas A, Schaible UE (2008) Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10(7):1530–1545PubMedCrossRef
99.
go back to reference Fratti RA et al (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100:5437PubMedPubMedCentralCrossRef Fratti RA et al (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100:5437PubMedPubMedCentralCrossRef
100.
go back to reference Vergne I, Chua J, Deretic V (2003) Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198(4):653–659PubMedPubMedCentralCrossRef Vergne I, Chua J, Deretic V (2003) Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198(4):653–659PubMedPubMedCentralCrossRef
101.
go back to reference Puri RV, Reddy PV, Tyagi AK (2013) Secreted acid phosphatase (SapM) of Mycobacterium tuberculosis is indispensable for arresting phagosomal maturation and growth of the pathogen in Guinea pig tissues. PLoS One 8(7):e70514PubMedPubMedCentralCrossRef Puri RV, Reddy PV, Tyagi AK (2013) Secreted acid phosphatase (SapM) of Mycobacterium tuberculosis is indispensable for arresting phagosomal maturation and growth of the pathogen in Guinea pig tissues. PLoS One 8(7):e70514PubMedPubMedCentralCrossRef
102.
go back to reference Walburger A, Koul A, Ferrari G, Nguyen L, Prescianotto-Baschong C, Huygen K, Klebl B, Thompson C, Bacher G, Pieters J (2004) Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304(5678):1800–1804PubMedCrossRef Walburger A, Koul A, Ferrari G, Nguyen L, Prescianotto-Baschong C, Huygen K, Klebl B, Thompson C, Bacher G, Pieters J (2004) Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304(5678):1800–1804PubMedCrossRef
103.
go back to reference Cowley S, Ko M, Pick N, Chow R, Downing KJ, Gordhan BG, Betts JC, Mizrahi V, Smith DA, Stokes RW, Av-Gay Y (2004) The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52(6):1691–1702PubMedCrossRef Cowley S, Ko M, Pick N, Chow R, Downing KJ, Gordhan BG, Betts JC, Mizrahi V, Smith DA, Stokes RW, Av-Gay Y (2004) The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52(6):1691–1702PubMedCrossRef
104.
go back to reference Houben EN, Walburger A, Ferrari G, Nguyen L, Thompson CJ, Miess C, Vogel G, Mueller B, Pieters J (2009) Differential expression of a virulence factor in pathogenic and non-pathogenic mycobacteria. Mol Microbiol 72(1):41–52PubMedPubMedCentralCrossRef Houben EN, Walburger A, Ferrari G, Nguyen L, Thompson CJ, Miess C, Vogel G, Mueller B, Pieters J (2009) Differential expression of a virulence factor in pathogenic and non-pathogenic mycobacteria. Mol Microbiol 72(1):41–52PubMedPubMedCentralCrossRef
105.
go back to reference van der Woude AD, Stoop EJ, Stiess M, Wang S, Ummels R, van Stempvoort G, Piersma SR, Cascioferro A, Jimenez CR, Houben EN, Luirink J, Pieters J, van der Sar AM, Bitter W (2014) Analysis of SecA2-dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector. Cell Microbiol 16(2):280–295PubMedCrossRef van der Woude AD, Stoop EJ, Stiess M, Wang S, Ummels R, van Stempvoort G, Piersma SR, Cascioferro A, Jimenez CR, Houben EN, Luirink J, Pieters J, van der Sar AM, Bitter W (2014) Analysis of SecA2-dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector. Cell Microbiol 16(2):280–295PubMedCrossRef
106.
go back to reference Zulauf KE, Sullivan JT, Braunstein M (2018) The SecA2 pathway of Mycobacterium tuberculosis exports effectors that work in concert to arrest phagosome and autophagosome maturation. PLoS Pathog 14(4):e1007011PubMedPubMedCentralCrossRef Zulauf KE, Sullivan JT, Braunstein M (2018) The SecA2 pathway of Mycobacterium tuberculosis exports effectors that work in concert to arrest phagosome and autophagosome maturation. PLoS Pathog 14(4):e1007011PubMedPubMedCentralCrossRef
107.
go back to reference Wolff KA, de la Pena AH, Nguyen HT, Pham TH, Amzel LM, Gabelli SB, Nguyen L (2015) A redox regulatory system critical for mycobacterial survival in macrophages and biofilm development. PLoS Pathog 11(4):e1004839PubMedPubMedCentralCrossRef Wolff KA, de la Pena AH, Nguyen HT, Pham TH, Amzel LM, Gabelli SB, Nguyen L (2015) A redox regulatory system critical for mycobacterial survival in macrophages and biofilm development. PLoS Pathog 11(4):e1004839PubMedPubMedCentralCrossRef
108.
go back to reference Wolff KA, Nguyen HT, Cartabuke RH, Singh A, Ogwang S, Nguyen L (2009) Protein kinase G is required for intrinsic antibiotic resistance in mycobacteria. Antimicrob Agents Chemother 53(8):3515–3519PubMedPubMedCentralCrossRef Wolff KA, Nguyen HT, Cartabuke RH, Singh A, Ogwang S, Nguyen L (2009) Protein kinase G is required for intrinsic antibiotic resistance in mycobacteria. Antimicrob Agents Chemother 53(8):3515–3519PubMedPubMedCentralCrossRef
109.
go back to reference Mueller P, Pieters J (2017) Identification of mycobacterial GarA as a substrate of protein kinase G from M. tuberculosis using a KESTREL-based proteome wide approach. J Microbiol Methods 136:34–39PubMedCrossRef Mueller P, Pieters J (2017) Identification of mycobacterial GarA as a substrate of protein kinase G from M. tuberculosis using a KESTREL-based proteome wide approach. J Microbiol Methods 136:34–39PubMedCrossRef
110.
go back to reference O'Hare HM, Duran R, Cervenansky C, Bellinzoni M, Wehenkel AM, Pritsch O, Obal G, Baumgartner J, Vialaret J, Johnsson K, Alzari PM (2008) Regulation of glutamate metabolism by protein kinases in mycobacteria. Mol Microbiol 70(6):1408–1423PubMedCrossRef O'Hare HM, Duran R, Cervenansky C, Bellinzoni M, Wehenkel AM, Pritsch O, Obal G, Baumgartner J, Vialaret J, Johnsson K, Alzari PM (2008) Regulation of glutamate metabolism by protein kinases in mycobacteria. Mol Microbiol 70(6):1408–1423PubMedCrossRef
111.
go back to reference Rieck B, Degiacomi G, Zimmermann M, Cascioferro A, Boldrin F, Lazar-Adler NR, Bottrill AR, le Chevalier F, Frigui W, Bellinzoni M, Lisa MN, Alzari PM, Nguyen L, Brosch R, Sauer U, Manganelli R, O'Hare HM (2017) PknG senses amino acid availability to control metabolism and virulence of Mycobacterium tuberculosis. PLoS Pathog 13(5):e1006399PubMedPubMedCentralCrossRef Rieck B, Degiacomi G, Zimmermann M, Cascioferro A, Boldrin F, Lazar-Adler NR, Bottrill AR, le Chevalier F, Frigui W, Bellinzoni M, Lisa MN, Alzari PM, Nguyen L, Brosch R, Sauer U, Manganelli R, O'Hare HM (2017) PknG senses amino acid availability to control metabolism and virulence of Mycobacterium tuberculosis. PLoS Pathog 13(5):e1006399PubMedPubMedCentralCrossRef
112.
113.
go back to reference Wang J, Ge P, Qiang L, Tian F, Zhao D, Chai Q, Zhu M, Zhou R, Meng G, Iwakura Y, Gao GF, Liu CH (2017) The mycobacterial phosphatase PtpA regulates the expression of host genes and promotes cell proliferation. Nat Commun 8(1):244PubMedPubMedCentralCrossRef Wang J, Ge P, Qiang L, Tian F, Zhao D, Chai Q, Zhu M, Zhou R, Meng G, Iwakura Y, Gao GF, Liu CH (2017) The mycobacterial phosphatase PtpA regulates the expression of host genes and promotes cell proliferation. Nat Commun 8(1):244PubMedPubMedCentralCrossRef
114.
go back to reference Desvignes L, Wolf AJ, Ernst JD (2012) Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. J Immunol 188(12):6205–6215PubMedCrossRef Desvignes L, Wolf AJ, Ernst JD (2012) Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. J Immunol 188(12):6205–6215PubMedCrossRef
115.
go back to reference Jouanguy E, Lamhamedi-Cherradi S, Altare F, Fondanèche MC, Tuerlinckx D, Blanche S, Emile JF, Gaillard JL, Schreiber R, Levin M, Fischer A, Hivroz C, Casanova JL (1997) Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guérin infection and a sibling with clinical tuberculosis. J Clin Investig 100(11):2658–2664PubMedCrossRefPubMedCentral Jouanguy E, Lamhamedi-Cherradi S, Altare F, Fondanèche MC, Tuerlinckx D, Blanche S, Emile JF, Gaillard JL, Schreiber R, Levin M, Fischer A, Hivroz C, Casanova JL (1997) Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guérin infection and a sibling with clinical tuberculosis. J Clin Investig 100(11):2658–2664PubMedCrossRefPubMedCentral
116.
go back to reference Okada S, Markle JG, Deenick EK, Mele F, Averbuch D, Lagos M, Alzahrani M, Al-Muhsen S, Halwani R, Ma CS, Wong N, Soudais C, Henderson LA, Marzouqa H, Shamma J, Gonzalez M, Martinez-Barricarte R, Okada C, Avery DT, Latorre D, Deswarte C, Jabot-Hanin F, Torrado E, Fountain J, Belkadi A, Itan Y, Boisson B, Migaud M, Arlehamn CSL, Sette A, Breton S, McCluskey J, Rossjohn J, de Villartay JP, Moshous D, Hambleton S, Latour S, Arkwright PD, Picard C, Lantz O, Engelhard D, Kobayashi M, Abel L, Cooper AM, Notarangelo LD, Boisson-Dupuis S, Puel A, Sallusto F, Bustamante J, Tangye SG, Casanova JL (2015) Immunodeficiencies. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science 349(6248):606–613PubMedPubMedCentralCrossRef Okada S, Markle JG, Deenick EK, Mele F, Averbuch D, Lagos M, Alzahrani M, Al-Muhsen S, Halwani R, Ma CS, Wong N, Soudais C, Henderson LA, Marzouqa H, Shamma J, Gonzalez M, Martinez-Barricarte R, Okada C, Avery DT, Latorre D, Deswarte C, Jabot-Hanin F, Torrado E, Fountain J, Belkadi A, Itan Y, Boisson B, Migaud M, Arlehamn CSL, Sette A, Breton S, McCluskey J, Rossjohn J, de Villartay JP, Moshous D, Hambleton S, Latour S, Arkwright PD, Picard C, Lantz O, Engelhard D, Kobayashi M, Abel L, Cooper AM, Notarangelo LD, Boisson-Dupuis S, Puel A, Sallusto F, Bustamante J, Tangye SG, Casanova JL (2015) Immunodeficiencies. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science 349(6248):606–613PubMedPubMedCentralCrossRef
118.
go back to reference Ehrt S, Schnappinger D, Bekiranov S, Drenkow J, Shi S, Gingeras TR, Gaasterland T, Schoolnik G, Nathan C (2001) Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J Exp Med 194(8):1123–1140PubMedPubMedCentralCrossRef Ehrt S, Schnappinger D, Bekiranov S, Drenkow J, Shi S, Gingeras TR, Gaasterland T, Schoolnik G, Nathan C (2001) Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J Exp Med 194(8):1123–1140PubMedPubMedCentralCrossRef
119.
go back to reference Feng CG, Collazo-Custodio CM, Eckhaus M, Hieny S, Belkaid Y, Elkins K, Jankovic D, Taylor GA, Sher A (2004) Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J Immunol 172(2):1163–1168PubMedCrossRef Feng CG, Collazo-Custodio CM, Eckhaus M, Hieny S, Belkaid Y, Elkins K, Jankovic D, Taylor GA, Sher A (2004) Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J Immunol 172(2):1163–1168PubMedCrossRef
120.
go back to reference Tiwari S, Choi H-P, Matsuzawa T, Pypaert M, MacMicking JD (2009) Targeting of the GTPase Irgm1 to the phagosomal membrane via PtdIns(3,4)P2 and PtdIns(3,4,5)P3 promotes immunity to mycobacteria. Nat Immunol 10(8):907–917PubMedPubMedCentralCrossRef Tiwari S, Choi H-P, Matsuzawa T, Pypaert M, MacMicking JD (2009) Targeting of the GTPase Irgm1 to the phagosomal membrane via PtdIns(3,4)P2 and PtdIns(3,4,5)P3 promotes immunity to mycobacteria. Nat Immunol 10(8):907–917PubMedPubMedCentralCrossRef
121.
go back to reference Duncan SA, Baganizi DR, Sahu R, Singh SR, Dennis VA (2017) SOCS proteins as regulators of inflammatory responses induced by bacterial infections: a review. Front Microbiol 8:2431PubMedPubMedCentralCrossRef Duncan SA, Baganizi DR, Sahu R, Singh SR, Dennis VA (2017) SOCS proteins as regulators of inflammatory responses induced by bacterial infections: a review. Front Microbiol 8:2431PubMedPubMedCentralCrossRef
122.
go back to reference Queval CJ, Song O-R, Carralot J-P, Saliou J-M, Bongiovanni A, Deloison G, Deboosère N, Jouny S, Iantomasi R, Delorme V, Debrie A-S, Park S-J, Gouveia JC, Tomavo S, Brosch R, Yoshimura A, Yeramian E, Brodin P (2017) Mycobacterium tuberculosis controls phagosomal acidification by targeting CISH-mediated signaling. Cell Rep 20(13):3188–3198PubMedPubMedCentralCrossRef Queval CJ, Song O-R, Carralot J-P, Saliou J-M, Bongiovanni A, Deloison G, Deboosère N, Jouny S, Iantomasi R, Delorme V, Debrie A-S, Park S-J, Gouveia JC, Tomavo S, Brosch R, Yoshimura A, Yeramian E, Brodin P (2017) Mycobacterium tuberculosis controls phagosomal acidification by targeting CISH-mediated signaling. Cell Rep 20(13):3188–3198PubMedPubMedCentralCrossRef
123.
go back to reference Mancuso G, Midiri A, Biondo C, Beninati C, Zummo S, Galbo R, Tomasello F, Gambuzza M, Macri G, Ruggeri A, Leanderson T, Teti G (2007) Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J Immunol 178(5):3126–3133PubMedCrossRef Mancuso G, Midiri A, Biondo C, Beninati C, Zummo S, Galbo R, Tomasello F, Gambuzza M, Macri G, Ruggeri A, Leanderson T, Teti G (2007) Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J Immunol 178(5):3126–3133PubMedCrossRef
124.
go back to reference Donovan ML, Schultz TE, Duke TJ, Blumenthal A (2017) Type I interferons in the pathogenesis of tuberculosis: molecular drivers and immunological consequences. Front Immunol 8:1633PubMedPubMedCentralCrossRef Donovan ML, Schultz TE, Duke TJ, Blumenthal A (2017) Type I interferons in the pathogenesis of tuberculosis: molecular drivers and immunological consequences. Front Immunol 8:1633PubMedPubMedCentralCrossRef
125.
go back to reference Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202(1):8–32PubMedCrossRef Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202(1):8–32PubMedCrossRef
126.
go back to reference Isaacs A, Lindenmann J (1957) Virus interference. I. The interferon. Proc R Soc B Biol Sci 147(927):258–267 Isaacs A, Lindenmann J (1957) Virus interference. I. The interferon. Proc R Soc B Biol Sci 147(927):258–267
127.
go back to reference Stanley SA, Johndrow JE, Manzanillo P, Cox JS (2007) The type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178(5):3143–3152PubMedCrossRef Stanley SA, Johndrow JE, Manzanillo P, Cox JS (2007) The type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178(5):3143–3152PubMedCrossRef
128.
go back to reference Jang A-R, Choi J-H, Shin SJ, Park J-H (2018) Mycobacterium tuberculosis ESAT6 induces IFN-β gene expression in macrophages via TLRs-mediated signaling. Cytokine 104:104–109PubMedCrossRef Jang A-R, Choi J-H, Shin SJ, Park J-H (2018) Mycobacterium tuberculosis ESAT6 induces IFN-β gene expression in macrophages via TLRs-mediated signaling. Cytokine 104:104–109PubMedCrossRef
129.
go back to reference Pandey AK, Yang Y, Jiang Z, Fortune SM, Coulombe F, Behr MA, Fitzgerald KA, Sassetti CM, Kelliher MA (2009) NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog 5(7):e1000500PubMedPubMedCentralCrossRef Pandey AK, Yang Y, Jiang Z, Fortune SM, Coulombe F, Behr MA, Fitzgerald KA, Sassetti CM, Kelliher MA (2009) NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog 5(7):e1000500PubMedPubMedCentralCrossRef
130.
go back to reference Ruangkiattikul N, Nerlich A, Abdissa K, Lienenklaus S, Suwandi A, Janze N, Laarmann K, Spanier J, Kalinke U, Weiss S, Goethe R (2017) cGAS-STING-TBK1-IRF3/7 induced interferon-β contributes to the clearing of non tuberculous mycobacterial infection in mice. Virulence 8(7):1303–1315PubMedPubMedCentralCrossRef Ruangkiattikul N, Nerlich A, Abdissa K, Lienenklaus S, Suwandi A, Janze N, Laarmann K, Spanier J, Kalinke U, Weiss S, Goethe R (2017) cGAS-STING-TBK1-IRF3/7 induced interferon-β contributes to the clearing of non tuberculous mycobacterial infection in mice. Virulence 8(7):1303–1315PubMedPubMedCentralCrossRef
131.
go back to reference Wiens KE, Ernst JD (2016) The mechanism for type I interferon induction by Mycobacterium tuberculosis is bacterial strain-dependent. PLoS Pathog 12(8):e1005809PubMedPubMedCentralCrossRef Wiens KE, Ernst JD (2016) The mechanism for type I interferon induction by Mycobacterium tuberculosis is bacterial strain-dependent. PLoS Pathog 12(8):e1005809PubMedPubMedCentralCrossRef
134.
go back to reference Moreira-Teixeira L, Mayer-Barber K, Sher A, O'Garra A (2018) Type I interferons in tuberculosis: foe and occasionally friend. J Exp Med 215(5):1273–1285PubMedCrossRefPubMedCentral Moreira-Teixeira L, Mayer-Barber K, Sher A, O'Garra A (2018) Type I interferons in tuberculosis: foe and occasionally friend. J Exp Med 215(5):1273–1285PubMedCrossRefPubMedCentral
135.
go back to reference Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, Gomez E, Klunker S, Meyer N, O’Mahony L, Palomares O, Rhyner C, Quaked N, Schaffartzik A, Van De Veen W, Zeller S, Zimmermann M, Akdis CA (2011) Interleukins, from 1 to 37, and interferon-γ: receptors, functions, and roles in diseases. J Allergy Clin Immunol 127(3):701–721.e70PubMedCrossRef Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, Gomez E, Klunker S, Meyer N, O’Mahony L, Palomares O, Rhyner C, Quaked N, Schaffartzik A, Van De Veen W, Zeller S, Zimmermann M, Akdis CA (2011) Interleukins, from 1 to 37, and interferon-γ: receptors, functions, and roles in diseases. J Allergy Clin Immunol 127(3):701–721.e70PubMedCrossRef
136.
go back to reference Saunders BM, Frank AA, Orme IM, Cooper AM (2000) Interleukin-6 induces early gamma interferon production in the infected lung but is not required for generation of specific immunity to Mycobacterium tuberculosis infection. Infect Immun 68(6):3322–3326PubMedPubMedCentralCrossRef Saunders BM, Frank AA, Orme IM, Cooper AM (2000) Interleukin-6 induces early gamma interferon production in the infected lung but is not required for generation of specific immunity to Mycobacterium tuberculosis infection. Infect Immun 68(6):3322–3326PubMedPubMedCentralCrossRef
137.
go back to reference Martinez AN, Mehra S, Kaushal D (2013) Role of interleukin 6 in innate immunity to Mycobacterium tuberculosis infection. J Infect Dis 207(8):1253–1261PubMedPubMedCentralCrossRef Martinez AN, Mehra S, Kaushal D (2013) Role of interleukin 6 in innate immunity to Mycobacterium tuberculosis infection. J Infect Dis 207(8):1253–1261PubMedPubMedCentralCrossRef
139.
go back to reference Domingo-Gonzalez R, Prince O, Cooper A, Khader SA (2016) Cytokines and chemokines in Mycobacterium tuberculosis infection. Microbiol Spectrum 4(5) Domingo-Gonzalez R, Prince O, Cooper A, Khader SA (2016) Cytokines and chemokines in Mycobacterium tuberculosis infection. Microbiol Spectrum 4(5)
140.
go back to reference de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ, Kabel PJ, Draaisma JM, van Dissel JT, Kroon FP, Casanova JL, Ottenhoff TH (1998) Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 280(5368):1435–1438PubMedCrossRef de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ, Kabel PJ, Draaisma JM, van Dissel JT, Kroon FP, Casanova JL, Ottenhoff TH (1998) Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 280(5368):1435–1438PubMedCrossRef
141.
go back to reference Jouanguy E, Döffinger R, Dupuis S, Pallier A, Altare F, Casanova J-L (1999) IL-12 and IFN-γ in host defense against mycobacteria and salmonella in mice and men. Curr Opin Immunol 11(3):346–351PubMedCrossRef Jouanguy E, Döffinger R, Dupuis S, Pallier A, Altare F, Casanova J-L (1999) IL-12 and IFN-γ in host defense against mycobacteria and salmonella in mice and men. Curr Opin Immunol 11(3):346–351PubMedCrossRef
142.
go back to reference Cooper AM, Roberts AD, Rhoades ER, Callahan JE, Getzy DM, Orme IM (1995) The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 84(3):423–432PubMedPubMedCentral Cooper AM, Roberts AD, Rhoades ER, Callahan JE, Getzy DM, Orme IM (1995) The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 84(3):423–432PubMedPubMedCentral
143.
145.
go back to reference Raphael I, Nalawade S, Eagar TN, Forsthuber TG (2015) T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 74(1):5–17PubMedCrossRef Raphael I, Nalawade S, Eagar TN, Forsthuber TG (2015) T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 74(1):5–17PubMedCrossRef
146.
go back to reference Harris J, De Haro SA, Master SS, Keane J, Roberts EA, Delgado M, Deretic V (2007) T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 27(3):505–517PubMedCrossRef Harris J, De Haro SA, Master SS, Keane J, Roberts EA, Delgado M, Deretic V (2007) T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 27(3):505–517PubMedCrossRef
147.
go back to reference Dahl KE, Shiratsuchi H, Hamilton BD, Ellner JJ, Toossi Z (1996) Selective induction of transforming growth factor beta in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect Immun 64(2):399–405PubMedPubMedCentralCrossRef Dahl KE, Shiratsuchi H, Hamilton BD, Ellner JJ, Toossi Z (1996) Selective induction of transforming growth factor beta in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis. Infect Immun 64(2):399–405PubMedPubMedCentralCrossRef
148.
go back to reference Jeong YH, Hur Y-G, Lee H, Kim S, Cho J-E, Chang J, Shin SJ, Lee H, Kang YA, Cho S-N, Ha S-J (2014) Discrimination between active and latent tuberculosis based on ratio of antigen-specific to mitogen-induced IP-10 production. J Clin Microbiol 53(2):504–510PubMedCrossRef Jeong YH, Hur Y-G, Lee H, Kim S, Cho J-E, Chang J, Shin SJ, Lee H, Kang YA, Cho S-N, Ha S-J (2014) Discrimination between active and latent tuberculosis based on ratio of antigen-specific to mitogen-induced IP-10 production. J Clin Microbiol 53(2):504–510PubMedCrossRef
149.
go back to reference O'Leary S, O'Sullivan MP, Keane J (2011) IL-10 blocks phagosome maturation in mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45(1):172–180PubMedCrossRef O'Leary S, O'Sullivan MP, Keane J (2011) IL-10 blocks phagosome maturation in mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45(1):172–180PubMedCrossRef
150.
go back to reference Harding CV, Boom WH (2010) Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 8(4):296–307PubMedPubMedCentralCrossRef Harding CV, Boom WH (2010) Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 8(4):296–307PubMedPubMedCentralCrossRef
151.
go back to reference Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302(5652):1963–1966PubMedCrossRef Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302(5652):1963–1966PubMedCrossRef
152.
go back to reference Pieters J, Ploegh H (2003) Microbiology. Chemical warfare and mycobacterial defense. Science 302(5652):1900–1902PubMedCrossRef Pieters J, Ploegh H (2003) Microbiology. Chemical warfare and mycobacterial defense. Science 302(5652):1900–1902PubMedCrossRef
153.
go back to reference Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322(5904):1104–1107PubMedPubMedCentralCrossRef Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322(5904):1104–1107PubMedPubMedCentralCrossRef
155.
go back to reference Striebel F, Imkamp F, Özcelik D, Weber-Ban E (2014) Pupylation as a signal for proteasomal degradation in bacteria. Biochim Biophys Acta Mol Cell Res 1843(1):103–113CrossRef Striebel F, Imkamp F, Özcelik D, Weber-Ban E (2014) Pupylation as a signal for proteasomal degradation in bacteria. Biochim Biophys Acta Mol Cell Res 1843(1):103–113CrossRef
156.
go back to reference Samanovic MI, Tu S, Novak O, Iyer LM, McAllister FE, Aravind L, Gygi SP, Hubbard SR, Strnad M, Darwin KH (2015) Proteasomal control of cytokinin synthesis protects Mycobacterium tuberculosis against nitric oxide. Mol Cell 57(6):984–994PubMedPubMedCentralCrossRef Samanovic MI, Tu S, Novak O, Iyer LM, McAllister FE, Aravind L, Gygi SP, Hubbard SR, Strnad M, Darwin KH (2015) Proteasomal control of cytokinin synthesis protects Mycobacterium tuberculosis against nitric oxide. Mol Cell 57(6):984–994PubMedPubMedCentralCrossRef
157.
go back to reference Shi X, Festa RA, Ioerger TR, Butler-Wu S, Sacchettini JC, Darwin KH, Samanovic MI (2014) The copper-responsive RicR regulon contributes to Mycobacterium tuberculosis virulence. mBio 5(1) Shi X, Festa RA, Ioerger TR, Butler-Wu S, Sacchettini JC, Darwin KH, Samanovic MI (2014) The copper-responsive RicR regulon contributes to Mycobacterium tuberculosis virulence. mBio 5(1)
158.
go back to reference Becker SH, Darwin KH (2017) Bacterial proteasomes: mechanistic and functional insights. Microbiol Mol Biol Rev 81(1) Becker SH, Darwin KH (2017) Bacterial proteasomes: mechanistic and functional insights. Microbiol Mol Biol Rev 81(1)
159.
go back to reference BoseDasgupta S, Moes S, Jenoe P, Pieters J (2015) Cytokine-induced macropinocytosis in macrophages is regulated by 14-3-3ζ through its interaction with serine-phosphorylated coronin 1. FEBS J 282(7):1167–1181PubMedCrossRef BoseDasgupta S, Moes S, Jenoe P, Pieters J (2015) Cytokine-induced macropinocytosis in macrophages is regulated by 14-3-3ζ through its interaction with serine-phosphorylated coronin 1. FEBS J 282(7):1167–1181PubMedCrossRef
160.
go back to reference Boehm U, Klamp T, Groot M, Howard JC (1997) Cellular responses to interferon-γ. Annu Rev Immunol 15(1):749–795PubMedCrossRef Boehm U, Klamp T, Groot M, Howard JC (1997) Cellular responses to interferon-γ. Annu Rev Immunol 15(1):749–795PubMedCrossRef
161.
162.
go back to reference Springer HM, Schramm M, Taylor GA, Howard JC (2013) Irgm1 (LRG-47), a regulator of cell-autonomous immunity, does not localize to mycobacterial or listerial phagosomes in IFN- -induced mouse cells. J Immunol 191(4):1765–1774PubMedCrossRef Springer HM, Schramm M, Taylor GA, Howard JC (2013) Irgm1 (LRG-47), a regulator of cell-autonomous immunity, does not localize to mycobacterial or listerial phagosomes in IFN- -induced mouse cells. J Immunol 191(4):1765–1774PubMedCrossRef
163.
go back to reference Astarie-Dequeker C, Le Guyader L, Malaga W, Seaphanh F-K, Chalut C, Lopez A, Guilhot C (2009) Phthiocerol Dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathogens 5(2):e1000289PubMedPubMedCentralCrossRef Astarie-Dequeker C, Le Guyader L, Malaga W, Seaphanh F-K, Chalut C, Lopez A, Guilhot C (2009) Phthiocerol Dimycocerosates of M. tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathogens 5(2):e1000289PubMedPubMedCentralCrossRef
164.
go back to reference Casanova JL, Abel L (2002) Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol 20:581–620PubMedCrossRef Casanova JL, Abel L (2002) Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol 20:581–620PubMedCrossRef
165.
go back to reference Bustamante J, Arias AA, Vogt G, Picard C, Galicia LB, Prando C, Grant AV, Marchal CC, Hubeau M, Chapgier A, de Beaucoudrey L, Puel A, Feinberg J, Valinetz E, Janniere L, Besse C, Boland A, Brisseau JM, Blanche S, Lortholary O, Fieschi C, Emile JF, Boisson-Dupuis S, Al-Muhsen S, Woda B, Newburger PE, Condino-Neto A, Dinauer MC, Abel L, Casanova JL, Germline CYBB (2011) Mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat Immunol 12(3):213–221PubMedPubMedCentralCrossRef Bustamante J, Arias AA, Vogt G, Picard C, Galicia LB, Prando C, Grant AV, Marchal CC, Hubeau M, Chapgier A, de Beaucoudrey L, Puel A, Feinberg J, Valinetz E, Janniere L, Besse C, Boland A, Brisseau JM, Blanche S, Lortholary O, Fieschi C, Emile JF, Boisson-Dupuis S, Al-Muhsen S, Woda B, Newburger PE, Condino-Neto A, Dinauer MC, Abel L, Casanova JL, Germline CYBB (2011) Mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat Immunol 12(3):213–221PubMedPubMedCentralCrossRef
166.
go back to reference Mattila JT, Ojo OO, Kepka-Lenhart D, Marino S, Kim JH, Eum SY, Via LE, Barry CE 3rd, Klein E, Kirschner DE, Morris SM Jr, Lin PL, Flynn JL (2013) Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J Immunol 191(2):773–784PubMedCrossRef Mattila JT, Ojo OO, Kepka-Lenhart D, Marino S, Kim JH, Eum SY, Via LE, Barry CE 3rd, Klein E, Kirschner DE, Morris SM Jr, Lin PL, Flynn JL (2013) Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J Immunol 191(2):773–784PubMedCrossRef
167.
169.
go back to reference Kaufmann SHE (2001) How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 1(1):20–30PubMedCrossRef Kaufmann SHE (2001) How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 1(1):20–30PubMedCrossRef
170.
go back to reference Ramachandra L, Chu RS, Askew D, Noss EH, Canaday DH, Potter NS, Johnsen A, Krieg AM, Nedrud JG, Boom WH, Harding CV (1999) Phagocytic antigen processing and effects of microbial products on antigen processing and T-cell responses. Immunol Rev 168(1):217–239PubMedCrossRef Ramachandra L, Chu RS, Askew D, Noss EH, Canaday DH, Potter NS, Johnsen A, Krieg AM, Nedrud JG, Boom WH, Harding CV (1999) Phagocytic antigen processing and effects of microbial products on antigen processing and T-cell responses. Immunol Rev 168(1):217–239PubMedCrossRef
171.
go back to reference Pieters J (2001) Evasion of host cell defense mechanisms by pathogenic bacteria. Curr Opin Immunol 13(1):37–44PubMedCrossRef Pieters J (2001) Evasion of host cell defense mechanisms by pathogenic bacteria. Curr Opin Immunol 13(1):37–44PubMedCrossRef
172.
go back to reference Espinosa-Cueto P, Magallanes-Puebla A, Castellanos C, Mancilla R (2017) Dendritic cells that phagocytose apoptotic macrophages loaded with mycobacterial antigens activate CD8 T cells via cross-presentation. PLoS One 12(8):e0182126PubMedPubMedCentralCrossRef Espinosa-Cueto P, Magallanes-Puebla A, Castellanos C, Mancilla R (2017) Dendritic cells that phagocytose apoptotic macrophages loaded with mycobacterial antigens activate CD8 T cells via cross-presentation. PLoS One 12(8):e0182126PubMedPubMedCentralCrossRef
173.
go back to reference Harriff MJ, Purdy GE, Lewinsohn DM (2012) Escape from the phagosome: the explanation for MHC-I processing of mycobacterial antigens? Front Immunol 3:40PubMedPubMedCentralCrossRef Harriff MJ, Purdy GE, Lewinsohn DM (2012) Escape from the phagosome: the explanation for MHC-I processing of mycobacterial antigens? Front Immunol 3:40PubMedPubMedCentralCrossRef
174.
go back to reference Nunes-Alves C, Booty MG, Carpenter SM, Jayaraman P, Rothchild AC, Behar SM (2014) In search of a new paradigm for protective immunity to TB. Nat Rev Microbiol 12(4):289–299PubMedPubMedCentralCrossRef Nunes-Alves C, Booty MG, Carpenter SM, Jayaraman P, Rothchild AC, Behar SM (2014) In search of a new paradigm for protective immunity to TB. Nat Rev Microbiol 12(4):289–299PubMedPubMedCentralCrossRef
175.
go back to reference Silva CL, Lowrie DB (2000) Identification and characterization of murine cytotoxic T cells that kill Mycobacterium tuberculosis. Infect Immun 68(6):3269–3274PubMedPubMedCentralCrossRef Silva CL, Lowrie DB (2000) Identification and characterization of murine cytotoxic T cells that kill Mycobacterium tuberculosis. Infect Immun 68(6):3269–3274PubMedPubMedCentralCrossRef
176.
go back to reference Vyas JM, Van der Veen AG, Ploegh HL (2008) The known unknowns of antigen processing and presentation, nature reviews. Immunology 8(8):607–618PubMed Vyas JM, Van der Veen AG, Ploegh HL (2008) The known unknowns of antigen processing and presentation, nature reviews. Immunology 8(8):607–618PubMed
178.
go back to reference Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV (2001) Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 167(2):910–918PubMedCrossRef Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV (2001) Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 167(2):910–918PubMedCrossRef
179.
go back to reference Garg A, Barnes PF, Roy S, Quiroga MF, Wu S, Garcia VE, Krutzik SR, Weis SE, Vankayalapati R (2008) Mannose-capped lipoarabinomannan- and prostaglandin E2-dependent expansion of regulatory T cells in human Mycobacterium tuberculosis infection. Eur J Immunol 38(2):459–469PubMedPubMedCentralCrossRef Garg A, Barnes PF, Roy S, Quiroga MF, Wu S, Garcia VE, Krutzik SR, Weis SE, Vankayalapati R (2008) Mannose-capped lipoarabinomannan- and prostaglandin E2-dependent expansion of regulatory T cells in human Mycobacterium tuberculosis infection. Eur J Immunol 38(2):459–469PubMedPubMedCentralCrossRef
180.
go back to reference Holla S, Stephen-Victor E, Prakhar P, Sharma M, Saha C, Udupa V, Kaveri SV, Bayry J, Balaji KN (2016) Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1- and prostaglandin E2-induced regulatory T cell expansion. Sci Rep 6(1) Holla S, Stephen-Victor E, Prakhar P, Sharma M, Saha C, Udupa V, Kaveri SV, Bayry J, Balaji KN (2016) Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1- and prostaglandin E2-induced regulatory T cell expansion. Sci Rep 6(1)
181.
go back to reference Cohen NR, Garg S, Brenner MB (2009) Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv Immunol 102:1–94PubMedCrossRef Cohen NR, Garg S, Brenner MB (2009) Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv Immunol 102:1–94PubMedCrossRef
183.
go back to reference Gagliardi MC, Teloni R, Giannoni F, Mariotti S, Remoli ME, Sargentini V, Videtta M, Pardini M, De Libero G, Coccia EM, Nisini R (2009) Mycobacteria exploit p38 signaling to affect CD1 expression and lipid antigen presentation by human dendritic cells. Infect Immun 77(11):4947–4952PubMedPubMedCentralCrossRef Gagliardi MC, Teloni R, Giannoni F, Mariotti S, Remoli ME, Sargentini V, Videtta M, Pardini M, De Libero G, Coccia EM, Nisini R (2009) Mycobacteria exploit p38 signaling to affect CD1 expression and lipid antigen presentation by human dendritic cells. Infect Immun 77(11):4947–4952PubMedPubMedCentralCrossRef
184.
go back to reference Gold MC, Napier RJ, Lewinsohn DM (2015) MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol Rev 264(1):154–166PubMedPubMedCentralCrossRef Gold MC, Napier RJ, Lewinsohn DM (2015) MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol Rev 264(1):154–166PubMedPubMedCentralCrossRef
185.
go back to reference Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O'Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491(7426):717–723PubMedCrossRef Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O'Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491(7426):717–723PubMedCrossRef
186.
go back to reference Mori L, Lepore M, De Libero G (2016) The immunology of CD1- and MR1-restricted T cells. Annu Rev Immunol 34:479–510PubMedCrossRef Mori L, Lepore M, De Libero G (2016) The immunology of CD1- and MR1-restricted T cells. Annu Rev Immunol 34:479–510PubMedCrossRef
187.
go back to reference Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Barrell BG et al (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685):537–544PubMedCrossRef Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Barrell BG et al (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685):537–544PubMedCrossRef
188.
go back to reference McDonough KA, Kress Y, Bloom BR (1993) Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages [published erratum appears in iInfect Immun 1993 Sep;61(9):4021-4]. Infect Immun 61(7):2763–2773PubMedPubMedCentralCrossRef McDonough KA, Kress Y, Bloom BR (1993) Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages [published erratum appears in iInfect Immun 1993 Sep;61(9):4021-4]. Infect Immun 61(7):2763–2773PubMedPubMedCentralCrossRef
189.
go back to reference Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, Enninga J (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8(2):e1002507PubMedPubMedCentralCrossRef Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, Enninga J (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8(2):e1002507PubMedPubMedCentralCrossRef
190.
go back to reference Simeone R, Sayes F, Song O, Gröschel MI, Brodin P, Brosch R, Majlessi L (2015) Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLoS Pathog 11(2):e1004650PubMedPubMedCentralCrossRef Simeone R, Sayes F, Song O, Gröschel MI, Brodin P, Brosch R, Majlessi L (2015) Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLoS Pathog 11(2):e1004650PubMedPubMedCentralCrossRef
191.
go back to reference Houben D, Demangel C, van Ingen J, Perez J, Baldeón L, Abdallah AM, Caleechurn L, Bottai D, van Zon M, de Punder K, van der Laan T, Kant A, Bossers-de Vries R, Willemsen P, Bitter W, van Soolingen D, Brosch R, van der Wel N, Peters PJ (2012) ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 14(8):1287–1298PubMedCrossRef Houben D, Demangel C, van Ingen J, Perez J, Baldeón L, Abdallah AM, Caleechurn L, Bottai D, van Zon M, de Punder K, van der Laan T, Kant A, Bossers-de Vries R, Willemsen P, Bitter W, van Soolingen D, Brosch R, van der Wel N, Peters PJ (2012) ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 14(8):1287–1298PubMedCrossRef
192.
go back to reference Houben ENG, Bestebroer J, Ummels R, Wilson L, Piersma SR, Jiménez CR, Ottenhoff THM, Luirink J, Bitter W (2012) Composition of the type VII secretion system membrane complex. Mol Microbiol 86(2):472–484PubMedCrossRef Houben ENG, Bestebroer J, Ummels R, Wilson L, Piersma SR, Jiménez CR, Ottenhoff THM, Luirink J, Bitter W (2012) Composition of the type VII secretion system membrane complex. Mol Microbiol 86(2):472–484PubMedCrossRef
193.
go back to reference Kinhikar AG, Verma I, Chandra D, Singh KK, Weldingh K, Andersen P, Hsu T, Jacobs WR Jr, Laal S (2010) Potential role for ESAT6 in dissemination of M. tuberculosis via human lung epithelial cells. Mol Microbiol 75(1):92–106PubMedCrossRef Kinhikar AG, Verma I, Chandra D, Singh KK, Weldingh K, Andersen P, Hsu T, Jacobs WR Jr, Laal S (2010) Potential role for ESAT6 in dissemination of M. tuberculosis via human lung epithelial cells. Mol Microbiol 75(1):92–106PubMedCrossRef
194.
go back to reference Lou Y, Rybniker J, Sala C, Cole ST (2016) EspC forms a filamentous structure in the cell envelope of Mycobacterium tuberculosis and impacts ESX-1 secretion. Mol Microbiol 103(1):26–38PubMedCrossRef Lou Y, Rybniker J, Sala C, Cole ST (2016) EspC forms a filamentous structure in the cell envelope of Mycobacterium tuberculosis and impacts ESX-1 secretion. Mol Microbiol 103(1):26–38PubMedCrossRef
195.
go back to reference Demangel C, Brodin P, Cockle PJ, Brosch R, Majlessi L, Leclerc C, Cole ST (2004) Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-Kilodalton culture filtrate protein and ESAT-6. Infect Immun 72(4):2170–2176PubMedPubMedCentralCrossRef Demangel C, Brodin P, Cockle PJ, Brosch R, Majlessi L, Leclerc C, Cole ST (2004) Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-Kilodalton culture filtrate protein and ESAT-6. Infect Immun 72(4):2170–2176PubMedPubMedCentralCrossRef
196.
go back to reference Manzanillo PS, Ayres JS, Watson RO, Collins AC, Souza G, Rae CS, Schneider DS, Nakamura K, Shiloh MU, Cox JS (2013) The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501(7468):512–516PubMedPubMedCentralCrossRef Manzanillo PS, Ayres JS, Watson RO, Collins AC, Souza G, Rae CS, Schneider DS, Nakamura K, Shiloh MU, Cox JS (2013) The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501(7468):512–516PubMedPubMedCentralCrossRef
197.
go back to reference Watson RO, Manzanillo PS, Cox JS (2012) Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150(4):803–815PubMedPubMedCentralCrossRef Watson RO, Manzanillo PS, Cox JS (2012) Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150(4):803–815PubMedPubMedCentralCrossRef
198.
go back to reference Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6(1):10–21PubMedPubMedCentralCrossRef Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6(1):10–21PubMedPubMedCentralCrossRef
199.
go back to reference Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119(6):753–766PubMedCrossRef Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119(6):753–766PubMedCrossRef
200.
go back to reference Delgado MA, Deretic V (2009) Toll-like receptors in control of immunological autophagy. Cell Death Differ 16(7):976–983PubMedCrossRef Delgado MA, Deretic V (2009) Toll-like receptors in control of immunological autophagy. Cell Death Differ 16(7):976–983PubMedCrossRef
201.
go back to reference Liu PT, Stenger S, Tang DH, Modlin RL (2007) Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 179(4):2060–2063PubMedCrossRef Liu PT, Stenger S, Tang DH, Modlin RL (2007) Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 179(4):2060–2063PubMedCrossRef
202.
go back to reference Shin D-M, Yuk J-M, Lee H-M, Lee S-H, Son JW, Harding CV, Kim J-M, Modlin RL, Jo E-K (2010) Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signalling. Cell Microbiol 12(11):1648–1665PubMedPubMedCentralCrossRef Shin D-M, Yuk J-M, Lee H-M, Lee S-H, Son JW, Harding CV, Kim J-M, Modlin RL, Jo E-K (2010) Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signalling. Cell Microbiol 12(11):1648–1665PubMedPubMedCentralCrossRef
203.
go back to reference Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11(5):469–480PubMedPubMedCentralCrossRef Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11(5):469–480PubMedPubMedCentralCrossRef
204.
go back to reference Schmeisser H, Fey SB, Horowitz J, Fischer ER, Balinsky CA, Miyake K, Bekisz J, Snow AL, Zoon KC (2013) Type I interferons induce autophagy in certain human cancer cell lines. Autophagy 9(5):683–696PubMedPubMedCentralCrossRef Schmeisser H, Fey SB, Horowitz J, Fischer ER, Balinsky CA, Miyake K, Bekisz J, Snow AL, Zoon KC (2013) Type I interferons induce autophagy in certain human cancer cell lines. Autophagy 9(5):683–696PubMedPubMedCentralCrossRef
205.
go back to reference Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, Falasca L, Goletti D, Gafa V, Simeone R, Delogu G, Piacentini M, Brosch R, Fimia GM, Coccia EM (2012) ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8(9):1357–1370PubMedPubMedCentralCrossRef Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, Falasca L, Goletti D, Gafa V, Simeone R, Delogu G, Piacentini M, Brosch R, Fimia GM, Coccia EM (2012) ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8(9):1357–1370PubMedPubMedCentralCrossRef
207.
go back to reference Lammas DA, Stober C, Harvey CJ, Kendrick N, Panchalingam S, Kumararatne DS (1997) ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 7(3):433–444PubMedCrossRef Lammas DA, Stober C, Harvey CJ, Kendrick N, Panchalingam S, Kumararatne DS (1997) ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 7(3):433–444PubMedCrossRef
208.
go back to reference Amaral EP, Lasunskaia EB, D'Império-Lima MR (2016) Innate immunity in tuberculosis: how the sensing of mycobacteria and tissue damage modulates macrophage death. Microbes Infect 18(1):11–20PubMedCrossRef Amaral EP, Lasunskaia EB, D'Império-Lima MR (2016) Innate immunity in tuberculosis: how the sensing of mycobacteria and tissue damage modulates macrophage death. Microbes Infect 18(1):11–20PubMedCrossRef
209.
go back to reference Petit-Jentreau L, Tailleux L, Coombes JL (2017) Purinergic signaling: a common path in the macrophage response against Mycobacterium tuberculosis and toxoplasma gondii. Front Cell Infect Microbiol 7:347PubMedPubMedCentralCrossRef Petit-Jentreau L, Tailleux L, Coombes JL (2017) Purinergic signaling: a common path in the macrophage response against Mycobacterium tuberculosis and toxoplasma gondii. Front Cell Infect Microbiol 7:347PubMedPubMedCentralCrossRef
210.
211.
go back to reference Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, Hsu T, Glickman M, Jacobs WR Jr, Porcelli SA, Briken V (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3(7):e110PubMedPubMedCentralCrossRef Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, Hsu T, Glickman M, Jacobs WR Jr, Porcelli SA, Briken V (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3(7):e110PubMedPubMedCentralCrossRef
212.
go back to reference Hinchey J, Lee S, Jeon BY, Basaraba RJ, Venkataswamy MM, Chen B, Chan J, Braunstein M, Orme IM, Derrick SC, Morris SL, Jacobs WR Jr, Porcelli SA (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 117(8):2279–2288PubMedPubMedCentralCrossRef Hinchey J, Lee S, Jeon BY, Basaraba RJ, Venkataswamy MM, Chen B, Chan J, Braunstein M, Orme IM, Derrick SC, Morris SL, Jacobs WR Jr, Porcelli SA (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 117(8):2279–2288PubMedPubMedCentralCrossRef
213.
go back to reference Briken V, Miller JL (2008) Living on the edge: inhibition of host cell apoptosis by Mycobacterium tuberculosis. Future Microbiol 3(4):415–422PubMedCrossRef Briken V, Miller JL (2008) Living on the edge: inhibition of host cell apoptosis by Mycobacterium tuberculosis. Future Microbiol 3(4):415–422PubMedCrossRef
214.
go back to reference Miller JL, Velmurugan K, Cowan MJ, Briken V (2010) The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-alpha-mediated host cell apoptosis. PLoS Pathog 6(4):e1000864PubMedPubMedCentralCrossRef Miller JL, Velmurugan K, Cowan MJ, Briken V (2010) The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-alpha-mediated host cell apoptosis. PLoS Pathog 6(4):e1000864PubMedPubMedCentralCrossRef
215.
go back to reference Srinivasan L, Gurses SA, Hurley BE, Miller JL, Karakousis PC, Briken V (2016) Identification of a transcription factor that regulates host cell exit and virulence of Mycobacterium tuberculosis. PLoS Pathog 12(5):e1005652PubMedPubMedCentralCrossRef Srinivasan L, Gurses SA, Hurley BE, Miller JL, Karakousis PC, Briken V (2016) Identification of a transcription factor that regulates host cell exit and virulence of Mycobacterium tuberculosis. PLoS Pathog 12(5):e1005652PubMedPubMedCentralCrossRef
216.
go back to reference Chen M, Gan H, Remold HG (2006) A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 176(6):3707–3716PubMedCrossRef Chen M, Gan H, Remold HG (2006) A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 176(6):3707–3716PubMedCrossRef
217.
go back to reference Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM, Remold HG (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 10(8):899–906PubMedPubMedCentralCrossRef Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM, Remold HG (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 10(8):899–906PubMedPubMedCentralCrossRef
218.
go back to reference Miller JL, Velmurugan K, Cowan MJ, Briken V (2010) The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-α-mediated host cell apoptosis. PLoS Pathog 6(4):e1000864PubMedPubMedCentralCrossRef Miller JL, Velmurugan K, Cowan MJ, Briken V (2010) The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-α-mediated host cell apoptosis. PLoS Pathog 6(4):e1000864PubMedPubMedCentralCrossRef
219.
go back to reference Gengenbacher M, Kaufmann SHE (2012) Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 36(3):514–532PubMedCrossRef Gengenbacher M, Kaufmann SHE (2012) Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 36(3):514–532PubMedCrossRef
220.
go back to reference Doddam SN, Peddireddy V, Ahmed N (2017) Mycobacterium tuberculosis DosR regulon gene Rv2004c encodes a novel antigen with pro-inflammatory functions and potential diagnostic application for detection of latent tuberculosis. Front Immunol 8:712PubMedPubMedCentralCrossRef Doddam SN, Peddireddy V, Ahmed N (2017) Mycobacterium tuberculosis DosR regulon gene Rv2004c encodes a novel antigen with pro-inflammatory functions and potential diagnostic application for detection of latent tuberculosis. Front Immunol 8:712PubMedPubMedCentralCrossRef
221.
go back to reference Chen Z, Hu Y, Cumming BM, Lu P, Feng L, Deng J, Steyn AJC, Chen S (2016) Mycobacterial WhiB6 differentially regulates ESX-1 and the dos regulon to modulate granuloma formation and virulence in zebrafish. Cell Rep 16(9):2512–2524PubMedCrossRef Chen Z, Hu Y, Cumming BM, Lu P, Feng L, Deng J, Steyn AJC, Chen S (2016) Mycobacterial WhiB6 differentially regulates ESX-1 and the dos regulon to modulate granuloma formation and virulence in zebrafish. Cell Rep 16(9):2512–2524PubMedCrossRef
223.
go back to reference Hu Y, Movahedzadeh F, Stoker NG, Coates ARM (2006) Deletion of the Mycobacterium tuberculosis -crystallin-like hspX gene causes increased bacterial growth in vivo. Infect Immun 74(2):861–868PubMedPubMedCentralCrossRef Hu Y, Movahedzadeh F, Stoker NG, Coates ARM (2006) Deletion of the Mycobacterium tuberculosis -crystallin-like hspX gene causes increased bacterial growth in vivo. Infect Immun 74(2):861–868PubMedPubMedCentralCrossRef
224.
go back to reference Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan B-S, Kramnik I, Agarwal A, Steyn AJC (2008) Heme Oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 283(26):18032–18039PubMedPubMedCentralCrossRef Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan B-S, Kramnik I, Agarwal A, Steyn AJC (2008) Heme Oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 283(26):18032–18039PubMedPubMedCentralCrossRef
225.
go back to reference Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14(8):849–854PubMedPubMedCentralCrossRef Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14(8):849–854PubMedPubMedCentralCrossRef
226.
go back to reference Botella H, Vaubourgeix J, Lee MH, Song N, Xu W, Makinoshima H, Glickman MS, Ehrt S (2017) Mycobacterium tuberculosis protease MarP activates a peptidoglycan hydrolase during acid stress. EMBO J 36(4):536–548PubMedPubMedCentralCrossRef Botella H, Vaubourgeix J, Lee MH, Song N, Xu W, Makinoshima H, Glickman MS, Ehrt S (2017) Mycobacterium tuberculosis protease MarP activates a peptidoglycan hydrolase during acid stress. EMBO J 36(4):536–548PubMedPubMedCentralCrossRef
Metadata
Title
Macrophage-microbe interaction: lessons learned from the pathogen Mycobacterium tuberculosis
Authors
Somdeb BoseDasgupta
Jean Pieters
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 6/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-018-0710-0

Other articles of this Issue 6/2018

Seminars in Immunopathology 6/2018 Go to the issue