Skip to main content
SpringerLink
Log in

Innate Immune Recognition in Tuberculosis Infection

  • Chapter
Target Pattern Recognition in Innate Immunity

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 653))

Abstract

In this review, an overview of the host’s innate immune response against Mycobacterium tuberculosis will be provided. In particular, M. tuberculosis interaction with Toll-like receptors (TLRs), lung surfactant proteins and the antimicrobial mechanisms in the macrophage will be discussed along with their importance in shaping adaptive immunity to tuberculosis infection.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Dye C, Scheele S, Dolin P et al. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 1999; 282(7):677–686.

    Article  CAS  PubMed  Google Scholar 

  2. Russell DG. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2001; 2(8):569–577.

    Article  CAS  PubMed  Google Scholar 

  3. Kishore U, Bernai AL, Kamran MF et al. Surfactant proteins SP-A and SP-D in human health and disease. Arch Immunol Ther Exp (Warsz) 2005; 53(5):399–417.

    CAS  Google Scholar 

  4. Tsolaki AG, Hirsh AE, DeRiemer K et al. Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc Natl Acad Sci USA 2004; 101(14):4865–4870.

    Article  CAS  PubMed  Google Scholar 

  5. Caws M, Thwaites G, Dunstan S et al. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 2008; 4(3):e1000034.

    Article  PubMed  Google Scholar 

  6. Tsolaki AG, Gagneux S, Pym AS et al. Genomic deletions classify the Beijing/W strains as a distinct genetic lineage of Mycobacterium tuberculosis. J Clin Microbiol 2005; 43(7):3185–3191.

    Article  CAS  PubMed  Google Scholar 

  7. Schlesinger LS, Bellinger-Kawahara CG, Payne NR et al. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 1990; 144(7):2771–2780.

    CAS  PubMed  Google Scholar 

  8. Le Cabec V, Cols C, Maridonneau-Parini I. Nonopsonic phagocytosis of zymosan and Mycobacterium kansasii by CR3 (CD11b/CD18) involves distinct molecular determinants and is or is not coupled with NADPH oxidase activation. Infect Immun 2000; 68(8):4736–4745.

    Article  PubMed  Google Scholar 

  9. Sturgill-Koszycki S, Haddix PL, Russell DG. The interaction between Mycobacterium and the macrophage analyzed by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis 1997; 18(14):2558–2565.

    Article  CAS  PubMed  Google Scholar 

  10. Schorey JS, Carroll MC, Brown EJ. A macrophage invasion mechanism of pathogenic mycobacteria. Science 1997; 277(5329):1091–1093.

    Article  CAS  PubMed  Google Scholar 

  11. Hu C, Mayada-Norton T, Tanaka K et al. Mycobacterium tuberculosis infection in complement receptor 3-deficient mice. J Immunol 2000; 165(5):2596–2602.

    CAS  PubMed  Google Scholar 

  12. Schlesinger LS, Kaufman TM, Iyer S et al. Differences in mannose receptor-mediated uptake of lipoarabinomannan from virulent and attenuated strains of Mycobacterium tuberculosis by human macrophages. J Immunol 1996; 157(10):4568–4575.

    CAS  PubMed  Google Scholar 

  13. Kang PB, Azad AK, Torrelles JB et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 2005; 202(7):987–999.

    Article  CAS  PubMed  Google Scholar 

  14. Schlesinger LS. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 1993; 150(7):2920–2930.

    CAS  PubMed  Google Scholar 

  15. Peterson PK, Gekker G, Hu S et al. CD14 receptor-mediated uptake of nonopsonized Mycobacterium tuberculosis by human microglia. Infect Immun 1995; 63(4):1598–1602.

    CAS  PubMed  Google Scholar 

  16. Khanna M, Srivastava LM. Release of Superoxide anion from activated mouse peritoneal macrophages during Mycobacterium tuberculosis infection. Indian J Exp Biol 1996; 34(5):468–471.

    CAS  PubMed  Google Scholar 

  17. Shams H, Wizel B, Lakey DL et al. The CD14 receptor does not mediate entry of Mycobacterium tuberculosis into human mononuclear phagocytes. FEMS Immunol Med Microbiol 2003; 36(1–2):63–69.

    Article  CAS  PubMed  Google Scholar 

  18. Zimmerli S, Edwards S, Ernst JD. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am J Respir Cell Mol Biol 1996; 15(6):760–770.

    CAS  PubMed  Google Scholar 

  19. Armstrong JA, Hart PD. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 1975; 142(1):1–16.

    Article  CAS  PubMed  Google Scholar 

  20. Downing JF, Pasula R, Wright JR et al. Surfactant protein a promotes attachment of Mycobacterium tuberculosis to alveolar macrophages during infection with human immunodeficiency virus. Proc Natl Acad Sci USA 1995; 92(11):4848–4852.

    Article  CAS  PubMed  Google Scholar 

  21. Gaynor CD, McCormack FX, Voelker DR et al. Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 1995; 155(11):5343–5351.

    CAS  PubMed  Google Scholar 

  22. Pasula R, Wright JR, Kachel DL et al. Surfactant protein A suppresses reactive nitrogen intermediates by alveolar macrophages in response to Mycobacterium tuberculosis. J Clin Invest 1999; 103(4):483–490.

    Article  CAS  PubMed  Google Scholar 

  23. Tenner AJ, Robinson SL, Borchelt J, Wright JR et al. Human pulmonary surfactant protein (SP-A), a protein structurally homologous to C1q, can enhance FcR-and CR1-mediated phagocytosis. J Biol Chem 1989; 264(23):13923–13928.

    CAS  PubMed  Google Scholar 

  24. Beharka AA, Gaynor CD, Kang BK et al. Pulmonary surfactant protein A up-regulates activity of the mannose receptor, a pattern recognition receptor expressed on human macrophages. J Immunol 2002; 169(7):3565–3573.

    CAS  PubMed  Google Scholar 

  25. Ferguson JS, Voelker DR, McCormack FX et al. Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 1999; 163(1):312–321.

    CAS  PubMed  Google Scholar 

  26. Gatfield J, Pieters J. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 2000; 288(5471):1647–1650.

    Article  CAS  PubMed  Google Scholar 

  27. Armstrong JA, Hart PD. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 1971; 134(3 Pt 1):713–740.

    Article  CAS  PubMed  Google Scholar 

  28. Sturgill-Koszycki S, Schaible UE, Russell DG. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 1996; 15(24):6960–6968.

    CAS  PubMed  Google Scholar 

  29. Schaible UE, Collins HL, Priem F et al. Correction of the iron overload defect in beta-2-microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J Exp Med 2002; 196(11):1507–1513.

    Article  CAS  PubMed  Google Scholar 

  30. Russell DG, Dant J, Sturgill-Koszycki S. Mycobacterium avium-and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from the host cell plasmalemma. J Immunol 1996; 156(12):4764–4773.

    CAS  PubMed  Google Scholar 

  31. Clemens DL, Horwitz MA. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 1996; 184(4):1349–1355.

    Article  CAS  PubMed  Google Scholar 

  32. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994; 263(5147):678–681.

    Article  CAS  PubMed  Google Scholar 

  33. Via LE, Deretic D, Ulmer RJ et al. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 1997; 272(20):13326–13331.

    Article  CAS  PubMed  Google Scholar 

  34. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005; 122(5):735–749.

    Article  CAS  PubMed  Google Scholar 

  35. Fratti RA, Backer JM, Gruenberg J et al. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 2001; 154(3):631–644.

    Article  CAS  PubMed  Google Scholar 

  36. Deretic V, Vergne I, Chua J et al. Endosomal membrane traffic: convergence point targeted by Mycobacterium tuberculosis and HIV. Cell Microbiol 2004; 6(11):999–1009.

    Article  CAS  PubMed  Google Scholar 

  37. Kusner DJ. Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 2005; 114(3):239–247.

    Article  CAS  PubMed  Google Scholar 

  38. Vergne I, Chua J, Deretic V. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 2003; 198(4):653–659.

    Article  PubMed  Google Scholar 

  39. Thompson CR, Iyer SS, Melrose N et al. Sphingosine kinase 1 (SKI) is recruited to nascent phagosomes in human macrophages: inhibition of SK1 translocation by Mycobacterium tuberculosis. J Immunol 2005; 174(6):3551–3561.

    CAS  PubMed  Google Scholar 

  40. Anes E, Kiihnel MP, Bos E et al. Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat Cell Biol 2003; 5(9):793–802.

    Article  CAS  PubMed  Google Scholar 

  41. Kelley VA, Schorey JS. Mycobacterium’s arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron. Mol Biol Cell 2003; 14(8):3366–3377.

    Article  CAS  PubMed  Google Scholar 

  42. Walburger A, Koul A, Ferrari G et al. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 2004; 304(5678):1800–1804.

    Article  CAS  PubMed  Google Scholar 

  43. Tailleux L, Neyrolles O, Honoré-Bouakline S et al. Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J Immunol 2003; 170(4):1939–1948.

    CAS  PubMed  Google Scholar 

  44. Brightbill HD, Libraty DH, Krutzik SR et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999; 285(5428):732–736.

    Article  CAS  PubMed  Google Scholar 

  45. Pecora ND, Gehring AJ, Canaday DH et al. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J Immunol 2006; 177(1):422–429.

    CAS  PubMed  Google Scholar 

  46. Gehring AJ, Dobos KM, Belisle JT et al. Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J Immunol 2004; 173(4):2660–2668.

    CAS  PubMed  Google Scholar 

  47. Abel B, Thieblemont N, Quesniaux VJ et al. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J Immunol 2002; 169(6):3155–3162.

    CAS  PubMed  Google Scholar 

  48. Jung SB, Yang CS, Lee JS et al. The mycobacterial 38-kilodalton glycolipoprotein antigen activates the mitogen-activated protein kinase pathway and release of proinflammatory cytokines through Toll-like receptors 2 and 4 in human monocytes. Infect Immun 2006; 74(5):2686–2696.

    Article  CAS  PubMed  Google Scholar 

  49. Doz E, Rose S, Nigou J et al. Acylation determines the toll-like receptor (TLR)-dependent positive versus TLR2-, mannose receptor-, and SIGNR1-independent negative regulation of pro-inflammatory cytokines by mycobacterial lipomannan. J Biol Chem 2007; 282(36):26014–26025.

    Article  CAS  PubMed  Google Scholar 

  50. Hemmi H, Takeuchi O, Kawai T et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408(6813):740–745.

    Article  CAS  PubMed  Google Scholar 

  51. Tjarnlund A, Guirado E, Julián E et al. Determinant role for Toll-like receptor signalling in acute mycobacterial infection in the respiratory tract. Microbes Infect 2006; 8(7):1790–1800.

    Article  PubMed  Google Scholar 

  52. Underhill DM, Ozinsky A, Smith KD, Aderem A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc Natl Acad Sci USA 1999; 96(25):14459–14463.

    Article  CAS  PubMed  Google Scholar 

  53. Jang S, Uematsu S, Akira S, Salgame P. IL-6 and IL-10 induction from dendritic cells in response to Mycobacterium tuberculosis is predominantly dependent on TLR2-mediated recognition. J Immunol 2004; 173(5):3392–3397.

    CAS  PubMed  Google Scholar 

  54. Salgame P. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol 2005; 17(4):374–380.

    Article  CAS  PubMed  Google Scholar 

  55. Reiling N, Hölscher C, Fehrenbach A et al. Cutting edge: Toll-like receptor (TLR)2-and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 2002; 169(7):3480–3484.

    CAS  PubMed  Google Scholar 

  56. Branger J, Leemans JC, Florquin S et al. Toll-like receptor 4 plays a protective role in pulmonary tuberculosis in mice. Int Immunol 2004; 16(3):509–516.

    Article  CAS  PubMed  Google Scholar 

  57. Bafica A, Scanga CA, Feng CG et al. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 2005; 202(12): 1715–1724.

    Article  CAS  PubMed  Google Scholar 

  58. Estaquier J, Idziorek T, Zou W et al. T helper type 1/T helper type 2 cytokines and T cell death: preventive effect of interleukin 12 on activation-induced and CD95 (FAS/APO-1)-mediated apoptosis of CD4+ T cells from human immunodeficiency virus-infected persons. J Exp Med 1995; 182(6):1759–1767.

    Article  CAS  PubMed  Google Scholar 

  59. Ladel CH, Szalay G, Riederl D et al. Interleukin-12 secretion by Mycobacterium tuberculosis-infected macrophages. Infect Immun 1997; 65(5):1936–1938.

    CAS  PubMed  Google Scholar 

  60. Giacomini E, Iona E, Ferroni L et al. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 2001; 166(12):7033–7041.

    CAS  PubMed  Google Scholar 

  61. Flynn JL, Goldstein MM, Triebold KJ et al. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J Immunol 1995; 155(5):2515–2524.

    CAS  PubMed  Google Scholar 

  62. Feng CG, Jankovic D, Kullberg M et al. Maintenance of pulmonary Th1 effector function in chronic tuberculosis requires persistent IL-12 production. J Immunol 2005; 174(7):4185–4192.

    CAS  PubMed  Google Scholar 

  63. Wozniak TM, Ryan AA, Britton WJ. Interleukin-23 restores immunity to Mycobacterium tuberculosis infection in IL-12p40-deficient mice and is not required for the development of IL-17-secreting T cell responses. J Immunol 2006; 177(12):8684–8692.

    CAS  PubMed  Google Scholar 

  64. Takeda K, Akira S. Toll-like receptors. Curr Protoc Immunol 2007; Chapter 14:Unit 14 12.

    Google Scholar 

  65. Hölscher C, Hölscher A, Rückerl D et al. The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis. J Immunol 2005; 174(6):3534–3544.

    PubMed  Google Scholar 

  66. Pearl JE, Khader SA, Solache A et al. IL-27 signaling compromises control of bacterial growth in mycobacteria-infected mice. J Immunol 2004; 173(12):7490–7496.

    CAS  PubMed  Google Scholar 

  67. Flynn JL, Goldstein MM, Chan J et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995; 2(6):561–572.

    Article  CAS  PubMed  Google Scholar 

  68. Flynn JL. Immunology of tuberculosis and implications in vaccine development. Tuberculosis (Edinb) 2004; 84(1–2):93–101.

    Article  Google Scholar 

  69. Keane J, Balcewicz-Sablinska MK, Remold HG et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997; 65(1):298–304.

    CAS  PubMed  Google Scholar 

  70. Winau F, Weber S, Sad S et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 2006; 24(1):105–117.

    Article  CAS  PubMed  Google Scholar 

  71. Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 1998; 161(5):2636–2641.

    CAS  PubMed  Google Scholar 

  72. Boussiotis VA, Tsai EY, Yunis EJ et al. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J Clin Invest 2000; 105(9):1317–1325.

    Article  CAS  PubMed  Google Scholar 

  73. Bhatt K, Salgame P. Host innate immune response to Mycobacterium tuberculosis. J Clin Immunol 2007; 27(4):347–362.

    Article  CAS  PubMed  Google Scholar 

  74. Peters W, Scott HM, Chambers HF et al. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 2001; 98(14):7958–7963.

    Article  CAS  PubMed  Google Scholar 

  75. Scott HM, Flynn JL. Mycobacterium tuberculosis in chemokine receptor 2-deficient mice: influence of dose on disease progression. Infect Immun 2002; 70(11):5946–5954.

    Article  CAS  PubMed  Google Scholar 

  76. Algood HM, Flynn JL. CCR5-deficient mice control Mycobacterium tuberculosis infection despite increased pulmonary lymphocytic infiltration. J Immunol 2004; 173(5):3287–3296.

    PubMed  Google Scholar 

  77. Floto RA, MacAry PA, Boname JM et al. Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science 2006; 314(5798):454–458.

    Article  CAS  PubMed  Google Scholar 

  78. Bhatt K, Hickman SP, Salgame P. Cutting edge: a new approach to modeling early lung immunity in murine tuberculosis. J Immunol 2004; 172(5):2748–2751.

    CAS  PubMed  Google Scholar 

  79. Makino M, Maeda Y, Mukai T et al. Impaired maturation and function of dendritic cells by mycobacteria through IL-1beta. Eur J Immunol 2006; 36(6):1443–1452.

    Article  CAS  PubMed  Google Scholar 

  80. Demangel C, Brodin P, Cockie PJ et al. Cell envelope protein PPE68 contributes to Mycobacterium tuberculosis RD1 immunogenicity independently of a 10-kilodalton culture filtrate protein and ESAT-6. Infect Immun 2004; 72(4):2170–2176.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Human Immunology and Infection Biology. Division of Biosciences, School of Health Sciences and Social Care, Brunel University, Uxbridge, UB8 3PH, London, UK

    Anthony G. Tsolaki

Authors
  1. Anthony G. Tsolaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Laboratory of Human Immunology and Infection Biology, Biosciences Division, School of Health Sciences and Social Care, Brunei University, Uxbridge, London, UK

    Uday Kishore PhD

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Tsolaki, A.G. (2009). Innate Immune Recognition in Tuberculosis Infection. In: Kishore, U. (eds) Target Pattern Recognition in Innate Immunity. Advances in Experimental Medicine and Biology, vol 653. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0901-5_13

Download citation

Publish with us

Policies and ethics

Search

Navigation