Living on the edge: inhibition of host cell apoptosis by Mycobacterium tuberculosis

Papers of special note have been highlighted as either of interest (•) or of considerable interest (••) to readers.

Bibliography

• 1  Schnappinger D, Schoolnik GK, Ehrt S: Expression profiling of host pathogen interactions: how Mycobacterium tuberculosis and the macrophage adapt to one another. Microbes Infect.8,1132–1140 (2006).
  Medline CASGoogle Scholar
• 2  Deretic V, Singh S, Master S et al.: Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell. Microbiol.8,719–727 (2006).
  Medline CASGoogle Scholar
• 3  Houben EN, Nguyen L, Pieters J: Interaction of pathogenic mycobacteria with the host immune system. Curr. Opin. Microbiol.9,76–85 (2006).
  Medline CASGoogle Scholar
• 4  Russell DG: Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol.5,39–47 (2007).
  Medline CASGoogle Scholar
• 5  Abramovitch RB, Martin GB: Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol.7,356–364 (2004).
  Medline CASGoogle Scholar
• 6  Iriti M, Faoro F: Review of innate and specific immunity in plants and animals. Mycopathologia164,57–64 (2007).
  MedlineGoogle Scholar
• 7  Carmen JC, Sinai AP: Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Mol. Microbiol.64,904–916 (2007).
  Medline CASGoogle Scholar
• 8  Boya P, Pauleau AL, Poncet D, Gonzalez-Polo RA, Zamzami N, Kroemer G: Viral proteins targeting mitochondria: controlling cell death. Biochim. Biophys. Acta1659,178–189 (2004).
  Medline CASGoogle Scholar
• 9  Hilleman MR: Strategies and mechanisms for host and pathogen survival in acute and persistent viral infections. Proc. Natl Acad. Sci. USA101(Suppl. 2),14560–14566 (2004).
  Medline CASGoogle Scholar
• 10  Keckler MS: Dodging the CTL response: viral evasion of Fas and granzyme induced apoptosis. Front. Biosci.12,725–732 (2007).
  Medline CASGoogle Scholar
• 11  Klingler K, Tchou-Wong KM, Brandli O et al.: Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect. Immun.65,5272–5278 (1997).
  Medline CASGoogle Scholar
• 12  Placido R, Mancino G, Amendola A et al.: Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection. J. Pathol.181,31–38 (1997).
  Medline CASGoogle Scholar
• 13  Keane J, Balcewicz-Sablinska MK, Remold HG et al.: Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect. Immun.65,298–304 (1997).
  Medline CASGoogle Scholar
• 14  Danelishvili L, McGarvey J, Li YJ, Bermudez LE: Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell. Microbiol.5,649–660 (2003).
  Medline CASGoogle Scholar
• 15  Ciaramella A, Cavone A, Santucci MB et al.: Induction of apoptosis and release of interleukin-1-β by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection. J. Infect. Dis.190,1167–1176 (2004).
  Medline CASGoogle Scholar
• 16  Arcila ML, Sanchez MD, Ortiz B, Barrera LF, Garcia LF, Rojas M: Activation of apoptosis, but not necrosis, during Mycobacterium tuberculosis infection correlated with decreased bacterial growth: role of TNF-α, IL-10, caspases and phospholipase A2. Cell. Immunol.249,80–93 (2007).
  Medline CASGoogle Scholar
• 17  Rojas M, Barrera LF, Puzo G, Garcia LF: Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: role of nitric oxide and mycobacterial products. J. Immunol.159,1352–1361 (1997).•• Together with [23], this study proposes that the capacity of the host cell macrophage to undergo apoptosis but not necrosis is a factor in determining the susceptibility of a mouse strain to mycobacterial infections.
  Medline CASGoogle Scholar
• 18  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-α. J. Immunol.161,2636–2641 (1998).
  Medline CASGoogle Scholar
• 19  Velmurugan K, Chen B, Miller JL et al.: Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLOS Pathogens3,e110 (2007).•• Demonstrates via ‘gain-of-function’ and ‘loss-of-function’ genetic approaches that virulent Mycobacterium tuberculosis inhibits apoptosis, and that this is important for bacterial virulence.
  MedlineGoogle Scholar
• 20  Chaussabel D, Semnani RT, McDowell MA, Sacks D, Sher A, Nutman TB: Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood102,672–681 (2003).
  Medline CASGoogle Scholar
• 21  Lee J, Remold HG, Ieong MH, Kornfeld H: Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J. Immunol.176,4267–4274 (2006).• New caspase-independent cell death pathway may promote bacterial escape and extracellular replication.
  Medline CASGoogle Scholar
• 22  O’Sullivan MP, O’Leary S, Kelly DM, Keane J: A caspase-independent pathway mediates macrophage cell death in response to Mycobacterium tuberculosis infection. Infect. Immun.75,1984–1993 (2007).• New caspase-independent cell death pathway may promote bacterial escape and extracellular replication.
  MedlineGoogle Scholar
• 23  Pan H, Yan BS, Rojas M et al.: Ipr1 gene mediates innate immunity to tuberculosis. Nature434,767–772 (2005).•• Together with [17], proposes that the capacity of the host cell macrophage to undergo apoptosis but not necrosis is a factor in determining the susceptibility of a mouse strain to mycobacterial infections.
  Medline CASGoogle Scholar
• 24  Keane J, Remold HG, Kornfeld H: Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J. Immunol.164,2016–2020 (2000).•• Reports that only virulent mycobacterial species are able to inhibit apoptosis induction in primary human alveolar macrophages, and thus provides correlative evidence that host cell apoptosis inhibition is a virulence mechanism of M. tuberculosis.
  Medline CASGoogle Scholar
• 25  Riendeau CJ, Kornfeld H: THP-1 cell apoptosis in response to mycobacterial infection. Infect. Immun.71,254–259 (2003).• Demonstrates that the human acute monocytic leukemia cell line reflects the interaction of primary human alveolar macrophages with M. tuberculosis with regard to apoptosis induction, and is therefore a useful model cell line.
  Medline CASGoogle Scholar
• 26  Dhiman R, Raje M, Majumdar S: Differential expression of NF-κB in mycobacteria infected THP-1 affects apoptosis. Biochim. Biophys. Acta1770,649–658 (2007).
  Medline CASGoogle Scholar
• 27  Zhang J, Jiang R, Takayama H, Tanaka Y: Survival of virulent Mycobacterium tuberculosis involves preventing apoptosis induced by Bcl-2 upregulation and release resulting from necrosis in J774 macrophages. Microbiol. Immunol.49,845–852 (2005).
  Medline CASGoogle Scholar
• 28  Hinchey J, Lee S, Jeon BY et al.: Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J. Clin. Invest.117,2279–2288 (2007).•• First demonstration that a pro-apoptotic mutant of M. tuberculosis induces increased cross-presentation and cross-priming of CD8 T cells.
  Medline CASGoogle Scholar
• 29  Jayakumar D, Jacobs WR Jr, Narayanan S: Protein kinase E of Mycobacterium tuberculosis has a role in the nitric oxide stress response and apoptosis in a human macrophage model of infection. Cell. Microbiol.10(2),365–374 (2007).
  MedlineGoogle Scholar
• 30  Braunstein M, Espinosa BJ, Chan J, Belisle JT, Jacobs WR Jr: SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol.48,453–464 (2003).
  Medline CASGoogle Scholar
• 31  Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, Meylan PR: Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J. Immunol.160,5448–5454 (1998).• Establishes that M. tuberculosis inhibits Fas ligand (FasL)-mediated apoptosis.
  Medline CASGoogle Scholar
• 32  Fan T, Lu H, Hu H et al.: Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med.187,487–496 (1998).
  Medline CASGoogle Scholar
• 33  Chen M, Gan H, Remold HG: 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.176,3707–3716 (2006).
  Medline CASGoogle Scholar
• 34  Miyairi I, Byrne GI: Chlamydia and programmed cell death. Curr. Opin. Microbiol.9,102–108 (2006).
  Medline CASGoogle Scholar
• 35  Losick VP, Isberg RR: NF-κB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J. Exp. Med.203,2177–2189 (2006).
  Medline CASGoogle Scholar
• 36  Santic M, Asare R, Doric M, Abu Kwaik Y: Host-dependent trigger of caspases and apoptosis by Legionella pneumophila. Infect. Immun.75,2903–2913 (2007).
  Medline CASGoogle Scholar
• 37  Dobos KM, Spotts EA, Quinn FD, King CH: Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by cell permeation. Infect. Immun.68,6300–6310 (2000).
  Medline CASGoogle Scholar
• 38  Hsu T, Hingley-Wilson SM, Chen B et al.: The primary mechanism of attenuation of bacillus Calmette-Guérin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl Acad. Sci. USA100,12420–12425 (2003).
  Medline CASGoogle Scholar
• 39  Maiuri MC, Zalckvar E, Kimchi A, Kroemer G: Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell. Biol.8,741–752 (2007).
  Medline CASGoogle Scholar
• 40  Siegel RM: Caspases at the crossroads of immune-cell life and death. Nat. Rev. Immunol.6,308–317 (2006).
  Medline CASGoogle Scholar
• 41  Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR: Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J. Immunol.170,430–437 (2003).
  Medline CASGoogle Scholar
• 42  Kremer L, Estaquier J, Brandt E, Ameisen JC, Locht C: Mycobacterium bovis bacillus Calmette-Guérin infection prevents apoptosis of resting human monocytes. Eur. J. Immunol.27,2450–2456 (1997).
  Medline CASGoogle Scholar
• 43  Kausalya S, Somogyi R, Orlofsky A, Prystowsky MB: Requirement of A1-A for bacillus Calmette-Guérin-mediated protection of macrophages against nitric oxide-induced apoptosis. J. Immunol.166,4721–4727 (2001).
  Medline CASGoogle Scholar
• 44  Rohan D, Mahesh K, Manoj R, Sekhar M: Inhibition of bfl-1/A1 by siRNA inhibits mycobacterial growth in THP-1 cells by enhancing phagosomal acidification. Biochim. Biophys. Acta (2008) (Epub ahead of print).
  MedlineGoogle Scholar
• 45  Spira A, Carroll JD, Liu G et al.: Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor. Am. J. Respir. Cell. Mol. Biol.29,545–551 (2003).
  Medline CASGoogle Scholar
• 46  Maiti D, Bhattacharyya A, Basu J: Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem.276,329–333 (2001).
  Medline CASGoogle Scholar
• 47  Loeuillet C, Martinon F, Perez C, Munoz M, Thome M, Meylan PR: Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J. Immunol.177,6245–6255 (2006).• Establishes that M. tuberculosis inhibits FasL-mediated apoptosis.
  Medline CASGoogle Scholar
• 48  Fratazzi C, Arbeit RD, Carini C et al.: Macrophage apoptosis in mycobacterial infections. J. Leukoc. Biol.66,763–764 (1999).
  Medline CASGoogle Scholar
• 49  Molloy A, Laochumroonvorapong P, Kaplan G: Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guérin. J. Exp. Med.180,1499–1509 (1994).
  Medline CASGoogle Scholar
• 50  Fratazzi C, Arbeit RD, Carini C, Remold HG: Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J. Immunol.158,4320–4327 (1997).
  Medline CASGoogle Scholar
• 51  Keane J, Shurtleff B, Kornfeld H: TNF-dependent BALB/c murine macrophage apoptosis following Mycobacterium tuberculosis infection inhibits bacillary growth in an IFN-γ independent manner. Tuberculosis (Edinb.)82,55–61 (2002).
  Medline CASGoogle Scholar
• 52  Schaible UE, Winau F, Sieling PA et al.: Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med.9,1039–1046 (2003).•• Together with [54], demonstrates that the ‘detour’ pathways of cross-presentation leads to increased CD8 T-cell priming against mycobacterial antigens.
  Medline CASGoogle Scholar
• 53  Guermonprez P, Amigorena S: Pathways for antigen cross presentation. Springer Semin. Immunopathol.26,257–271 (2005).
  MedlineGoogle Scholar
• 54  Winau F, Weber S, Sad S et al.: Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity24,105–117 (2006).•• Together with [52], demonstrates that the detour pathways of cross-presentation leads to increased CD8 T-cell priming against mycobacterial antigens.
  Medline CASGoogle Scholar
• 55  Edwards KM, Cynamon MH, Voladri RK et al.: Iron-cofactored superoxide dismutase inhibits host responses to Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med.164,2213–2219 (2001).
  Medline CASGoogle Scholar
• 56  Briken V, Porcelli SA, Besra GS, Kremer L: Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol. Microbiol.53,391–403 (2004).
  Medline CASGoogle Scholar
• 57  Karakousis PC, Bishai WR, Dorman SE: Mycobacterium tuberculosis cell envelope lipids and the host immune response. Cell. Microbiol.6,105–116 (2004).
  Medline CASGoogle Scholar
• 58  Briken V: Molecular mechanisms of host–pathogen interactions and their potential for the discovery of new drug targets. Curr. Drug Targets9,150–157 (2008).
  Medline CASGoogle Scholar
• 59  Grode L, Seiler P, Baumann S et al.: Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guérin mutants that secrete listeriolysin. J. Clin. Invest.115,2472–2479 (2005).•• First demonstration that the vaccine capacity of Mycobacterium bovis Bacille Calmette-Guérin can be improved by increasing its pro-apoptotic potential.
  Medline CASGoogle Scholar