The Balance of Apoptotic and Necrotic Cell Death in Mycobacterium tuberculosis Infected Macrophages Is Not Dependent on Bacterial Virulence

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Butler, Rachel E ^a   Brodin, Priscille ^b,c   Jang, Jichan ^b   Jang, Mi Seon ^b   Robertson, Brian D ^d   Gicquel, Brigitte ^e   Stewart, Graham R ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b Institute Pasteur Korea   (South Korea)

^c INSTITUT PASTEUR DE LILLE   (France)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CELL DEATH; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; IMAGE ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; TUBERCULOSIS;

ANIMALS; APOPTOSIS; CASPASES; MACROPHAGES; MICE; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; VIRULENCE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84868104362     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047573     Document Type: Article

References (50)

1. Lee J, Hartman M, Kornfeld H, (2009) Macrophage apoptosis in tuberculosis. Yonsei Med J 50: 1-11.
2. Lopez M, Sly LM, Luu Y, Young D, Cooper H, et al. (2003) The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J Immunol 170: 2409-2416.
3. Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, et al. (1998) Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 160: 5448-5454.
4. Lammas DA, Stober C, Harvey CJ, Kendrick N, Panchalingam S, et al. (1997) ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 7: 433-444.
5. Molloy A, Laochumroonvorapong P, Kaplan G, (1994) Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 180: 1499-1509.
6. Thoma-Uszynski S, Stenger S, Takeuchi O, Ochoa MT, Engele M, et al. (2001) Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 291: 1544-1547.
7. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, et al. (2003) Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9: 1039-1046.
8. Winau F, Kaufmann SH, Schaible UE, (2004) Apoptosis paves the detour path for CD8 T cell activation against intracellular bacteria. Cell Microbiol 6: 599-607.
9. Winau F, Weber S, Sad S, de Diego J, Hoops SL, et al. (2006) Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24: 105-117.
10. Golstein P, Kroemer G, (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32: 37-43.
11. Cho YS, Challa S, Moquin D, Genga R, Ray TD, et al. (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137: 1112-1123.
12. Lee J, Repasy T, Papavinasasundaram K, Sassetti C, Kornfeld H, (2011) Mycobacterium tuberculosis induces an atypical cell death mode to escape from infected macrophages. PLoS One 6: e18367.
13. Keane J, Remold HG, Kornfeld H, (2000) Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 164: 2016-2020.
14. O'Sullivan MP, O'Leary S, Kelly DM, Keane J, (2007) A caspase-independent pathway mediates macrophage cell death in response to Mycobacterium tuberculosis infection. Infect Immun 75: 1984-1993.
15. Lee J, Remold HG, Ieong MH, Kornfeld H, (2006) Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J Immunol 176: 4267-4274.
16. Park JS, Tamayo MH, Gonzalez-Juarrero M, Orme IM, Ordway DJ, (2006) Virulent clinical isolates of Mycobacterium tuberculosis grow rapidly and induce cellular necrosis but minimal apoptosis in murine macrophages. J Leukoc Biol 79: 80-86.
17. 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: 3707-3716.
18. Zhang J, Jiang R, Takayama H, Tanaka Y, (2005) 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.
19. Sohn H, Lee KS, Kim SY, Shin DM, Shin SJ, et al. (2009) Induction of cell death in human macrophages by a highly virulent Korean Isolate of Mycobacterium tuberculosis and the virulent strain H37Rv. Scand J Immunol 69: 43-50.
20. Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, et al. (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3: e110.
21. Hinchey J, Lee S, Jeon BY, Basaraba RJ, Venkataswamy MM, et al. (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 117: 2279-2288.
22. Derrick SC, Morris SL, (2007) The ESAT6 protein of Mycobacterium tuberculosis induces apoptosis of macrophages by activating caspase expression. Cell Microbiol 9: 1547-1555.
23. Santucci MB, Amicosante M, Cicconi R, Montesano C, Casarini M, et al. (2000) Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages: early membrane modifications and intracellular mycobacterial viability. J Infect Dis 181: 1506-1509.
24. Klingler K, Tchou-Wong KM, Brandli O, Aston C, Kim R, et al. (1997) Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect Immun 65: 5272-5278.
25. Placido R, Mancino G, Amendola A, Mariani F, Vendetti S, et al. (1997) Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection. J Pathol 181: 31-38.
26. Sturgill-Koszycki S, Schaible UE, Russell DG, (1996) Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 15: 6960-6968.
27. Armstrong JA, Hart PD, (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134: 713-740.
28. Caminero JA, Pena MJ, Campos-Herrero MI, Rodriguez JC, Garcia I, et al. (2001) Epidemiological evidence of the spread of a Mycobacterium tuberculosis strain of the Beijing genotype on Gran Canaria Island. Am J Respir Crit Care Med 164: 1165-1170.
29. Brodin P, Poquet Y, Levillain F, Peguillet I, Larrouy-Maumus G, et al. (2010) High content phenotypic cell-based visual screen identifies Mycobacterium tuberculosis acyltrehalose-containing glycolipids involved in phagosome remodeling. PLoS Pathog 6: e1001100.
30. Butler RE, Cihlarova V, Stewart GR, (2010) Effective generation of reactive oxygen species in the mycobacterial phagosome requires K+ efflux from the bacterium. Cell Microbiol 12: 1186-1193.
31. Fenistein D, Lenseigne B, Christophe T, Brodin P, Genovesio A, (2008) A fast, fully automated cell segmentation algorithm for high-throughput and high-content screening. Cytometry A 73: 958-964.
32. Eklund D, Welin A, Schon T, Stendahl O, Huygen K, et al. (2010) Validation of a medium-throughput method for evaluation of intracellular growth of Mycobacterium tuberculosis. Clin Vaccine Immunol 17: 513-517.
33. Rios-Barrera VA, Campos-Pena V, Aguilar-Leon D, Lascurain LR, Meraz-Rios MA, et al. (2006) Macrophage and T lymphocyte apoptosis during experimental pulmonary tuberculosis: their relationship to mycobacterial virulence. Eur J Immunol 36: 345-353.
34. Jaattela M, Tschopp J, (2003) Caspase-independent cell death in T lymphocytes. Nat Immunol 4: 416-423.
35. Yu L, Alva A, Su H, Dutt P, Freundt E, et al. (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502.
36. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, et al. (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228.
37. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L, et al. (2003) A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 278: 51613-51621.
38. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, et al. (2004) Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279: 10822-10828.
39. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, et al. (2012) Phagosomal Rupture by Mycobacterium tuberculosis Results in Toxicity and Host Cell Death. PLoS Pathog 8: e1002507.
40. Wong KW, Jacobs WR Jr, (2011) Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis. Cell Microbiol 13: 1371-1384.
41. Obregon-Henao A, Duque-Correa MA, Rojas M, Garcia LF, Brennan PJ, et al. (2012) Stable extracellular RNA fragments of Mycobacterium tuberculosis induce early apoptosis in human monocytes via a caspase-8 dependent mechanism. PLoS One 7: e29970.
42. Dao DN, Kremer L, Guerardel Y, Molano A, Jacobs WR Jr, et al. (2004) Mycobacterium tuberculosis lipomannan induces apoptosis and interleukin-12 production in macrophages. Infect Immun 72: 2067-2074.
43. Sanchez A, Espinosa P, Esparza MA, Colon M, Bernal G, et al. (2009) Mycobacterium tuberculosis 38-kDa lipoprotein is apoptogenic for human monocyte-derived macrophages. Scand J Immunol 69: 20-28.
44. Basu S, Pathak SK, Banerjee A, Pathak S, Bhattacharyya A, et al. (2007) Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-alpha. J Biol Chem 282: 1039-1050.
45. Loeuillet C, Martinon F, Perez C, Munoz M, Thome M, et al. (2006) Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. J Immunol 177: 6245-6255.
46. Ciaramella A, Cavone A, Santucci MB, Garg SK, Sanarico N, et al. (2004) Induction of apoptosis and release of interleukin-1 beta by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection. J Infect Dis 190: 1167-1176.
47. Balcewicz-Sablinska MK, Keane J, Kornfeld H, Remold HG, (1998) Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J Immunol 161: 2636-2641.
48. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR, (2003) 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.
49. Dhiman R, Raje M, Majumdar S, (2007) Differential expression of NF-kappaB in mycobacteria infected THP-1 affects apoptosis. Biochim Biophys Acta 1770: 649-658.
50. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM, (2010) Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 11: 751-758.