ESX-1-induced apoptosis is involved in cell-to-cell spread of Mycobacterium tuberculosis

Cellular Microbiology

Volumn 15, Issue 12, 2013, Pages 1994-2005

  Aguilo, J I ^a,b   Alonso, H ^a,b,g   Uranga, S ^a,b   Marinova, D ^a,b   Arbues A ^a,b,g   de Martino, A ^c   Anel, A ^a   Monzon, M ^a   Badiola, J ^a   Pardo, J ^a,d   Brosch, Roland ^e   Martin, Carlos ^a,b,f  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INSTITUTO DE INVESTIGACIÓN SANITARIA ARAGÓN IIS ARAGÓN   (Spain)

^d FUNDACIÓN ARAID   (Spain)

^e INSTITUT PASTEUR   (France)

^f HOSPITAL UNIVERSITARIO MIGUEL SERVET   (Spain)

^g INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CASPASE 3; EARLY SECRETORY ANTIGENIC TARGET 6; MITOGEN ACTIVATED PROTEIN KINASE P38; STAUROSPORINE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATTENUATION; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; CELL SPREADING; ENZYME ACTIVATION; FEMALE; HISTOPATHOLOGY; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL;

CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; APOPTOSIS; BACTERIAL PROTEINS; BCG VACCINE; FEMALE; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84887611505     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12169     Document Type: Article

References (50)

1. Aleman, M., Schierloh, P., de la Barrera, S.S., Musella, R.M., Saab, M.A., Baldini, M., etal. (2004) Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients. Infect Immun 72: 5150-5158.
2. Aporta, A., Arbues, A., Aguilo, J.I., Monzon, M., Badiola, J.J., de Martino, A., etal. (2012) Attenuated Mycobacterium tuberculosis SO2 vaccine candidate is unable to induce cell death. PLoS ONE 7: e45213.
3. Arbues, A., Aguilo, J.I, Gonzalo-Asensio, J., Marinova, D., Uranga, S., Puentes, E., etal. (2013) Construction, characterization and preclinical evaluation of MTBVAC, the first live-attenuated M. tuberculosis-based vaccine to enter clinical trials. Vaccine (in press). doi:10.1016/j.vaccine.2013.07.051
4. Behar, S.M., Martin, C.J., Booty, M.G., Nishimura, T., Zhao, X., Gan, H.X., etal. (2011) Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol 4: 279-287.
5. Briken, V., and Miller, J.L. (2008) Living on the edge: inhibition of host cell apoptosis by Mycobacterium tuberculosis. Future Microbiol 3: 415-422.
6. Camacho, L.R., Ensergueix, D., Perez, E., Gicquel, B., and Guilhot, C. (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34: 257-267.
7. Chen, M., Gan, H., and Remold, H.G. (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.
8. Choi, H.H., Shin, D.M., Kang, G., Kim, K.H., Park, J.B., Hur, G.M., etal. (2010) Endoplasmic reticulum stress response is involved in Mycobacterium tuberculosis protein ESAT-6-mediated apoptosis. FEBS Lett 584: 2445-2454.
9. Cooper, A.M. (2009) Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 27: 393-422.
10. Cox, J.S., Chen, B., McNeil, M., and Jacobs, W.R., Jr (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402: 79-83.
11. Davis, J.M., and Ramakrishnan, L. (2009) The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136: 37-49.
12. Derrick, S.C., and Morris, S.L. (2007) The ESAT6 protein of Mycobacterium tuberculosis induces apoptosis of macrophages by activating caspase expression. Cell Microbiol 9: 1547-1555.
13. Ernst, J.D., Trevejo-Nunez, G., and Banaiee, N. (2007) Genomics and the evolution, pathogenesis, and diagnosis of tuberculosis. J Clin Invest 117: 1738-1745.
14. Fan, T., Lu, H., Hu, H., Shi, L., McClarty, G.A., Nance, D.M., etal. (1998) Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 187: 487-496.
15. Frigui, W., Bottai, D., Majlessi, L., Monot, M., Josselin, E., Brodin, P., etal. (2008) Control of M. tuberculosis ESAT-6 secretion and specific T cell recognition by PhoP. PLoS Pathog 4: e33.
16. Gan, H., Lee, J., Ren, F., Chen, M., Kornfeld, H., and Remold, H.G. (2008) Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat Immunol 9: 1189-1197.
17. Gao, L.Y., Guo, S., McLaughlin, B., Morisaki, H., Engel, J.N., and Brown, E.J. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53: 1677-1693.
18. Gonzalo-Asensio, J., Soto, C.Y., Arbues, A., Sancho, J., Menendez, M., Garcia, M.J., etal. (2008) The Mycobacterium tuberculosis phoPR operon is positively autoregulated in the virulent strain H37Rv. J Bacteriol 190: 7068-7078.
19. Gordon, S.V., Brosch, R., Billault, A., Garnier, T., Eiglmeier, K., and Cole, S.T. (1999) Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol Microbiol 32: 643-655.
20. Grover, A., and Izzo, A.A. (2012) BAT3 regulates Mycobacterium tuberculosis protein ESAT-6-mediated apoptosis of macrophages. PLoS ONE 7: e40836.
21. Guiney, D.G. (2005) The role of host cell death in Salmonella infections. Curr Topics Microbiol Immunol 289: 131-150.
22. Guinn, K.M., Hickey, M.J., Mathur, S.K., Zakel, K.L., Grotzke, J.E., Lewinsohn, D.M., etal. (2004) Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 51: 359-370.
23. Gutierrez, M.G., Master, S.S., Singh, S.B., Taylor, G.A., Colombo, M.I., and Deretic, V. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
24. Houben, D., Demangel, C., van Ingen, J., Perez, J., Baldeon, L., Abdallah, A.M., etal. (2012) ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 14: 1287-1298.
25. Jagannath, C., Lindsey, D.R., Dhandayuthapani, S., Xu, Y., Hunter, R.L., Jr, and Eissa, N.T. (2009) Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 15: 267-276.
26. Keane, J., Balcewicz-Sablinska, M.K., Remold, H.G., Chupp, G.L., Meek, B.B., Fenton, M.J., and Kornfeld, H. (1997) Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 65: 298-304.
27. Kundu, M., Pathak, S.K., Kumawat, K., Basu, S., Chatterjee, G., Pathak, S., etal. (2009) A TNF- and c-Cbl-dependent FLIP(S)-degradation pathway and its function in Mycobacterium tuberculosis-induced macrophage apoptosis. Nat Immunol 10: 918-926.
28. Lim, Y.J., Choi, J.A., Choi, H.H., Cho, S.N., Kim, H.J., Jo, E.K., etal. (2011) Endoplasmic reticulum stress pathway-mediated apoptosis in macrophages contributes to the survival of Mycobacterium tuberculosis. PLoS ONE 6: e28531.
29. Martin, C., Williams, A., Hernandez-Pando, R., Cardona, P.J., Gormley, E., Bordat, Y., etal. (2006) The live Mycobacterium tuberculosis phoP mutant strain is more attenuated than BCG and confers protective immunity against tuberculosis in mice and guinea pigs. Vaccine 24: 3408-3419.
30. Martin, C.J., Booty, M.G., Rosebrock, T.R., Nunes-Alves, C., Desjardins, D.M., Keren, I., etal. (2012) Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 12: 289-300.
31. Martin, S.J., Reutelingsperger, C.P., McGahon, A.J., Rader, J.A., van Schie, R.C., LaFace, D.M., and Green, D.R. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556.
32. Mbawuike, I.N., and Herscowitz, H.B. (1989) MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J Leukoc Biol 46: 119-127.
33. Melo, M.D., and Stokes, R.W. (2000) Interaction of Mycobacterium tuberculosis with MH-S, an immortalized murine alveolar macrophage cell line: a comparison with primary murine macrophages. Tuber Lung Dis 80: 35-46.
34. Monack, D.M., Raupach, B., Hromockyj, A.E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
35. Novikov, A., Cardone, M., Thompson, R., Shenderov, K., Kirschman, K.D., Mayer-Barber, K.D., etal. (2011) Mycobacterium tuberculosis triggers host type I IFN signaling to regulate IL-1beta production in human macrophages. J Immunol 187: 2540-2547.
36. Pathak, S.K., Basu, S., Basu, K.K., Banerjee, A., Pathak, S., Bhattacharyya, A., etal. (2007) Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol 8: 610-618.
37. Pym, A.S., Brodin, P., Brosch, R., Huerre, M., and Cole, S.T. (2002) Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46: 709-717.
38. Romagnoli, A., Etna, M.P., Giacomini, E., Pardini, M., Remoli, M.E., Corazzari, M., etal. (2012) ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8: 1357-1370.
39. Schaible, U.E., Winau, F., Sieling, P.A., Fischer, K., Collins, H.L., Hagens, K., etal. (2003) Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med 9: 1039-1046.
40. Seimon, T.A., Kim, M.J., Blumenthal, A., Koo, J., Ehrt, S., Wainwright, H., etal. (2010) Induction of ER stress in macrophages of tuberculosis granulomas. PLoS ONE 5: e12772.
41. Simeone, R., Bobard, A., Lippmann, J., Bitter, W., Majlessi, L., Brosch, R., and Enninga, J. (2012) Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8: e1002507.
42. Sly, L.M., Hingley-Wilson, S.M., Reiner, N.E., and McMaster, W.R. (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.
43. Valdivia, R.H., Hromockyj, A.E., Monack, D., Ramakrishnan, L., and Falkow, S. (1996) Applications for green fluorescent protein (GFP) in the study of host-pathogen interactions. Gene 173: 47-52.
44. Walters, S.B., Dubnau, E., Kolesnikova, I., Laval, F., Daffe, M., and Smith, I. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60: 312-330.
45. Wang, C., Peyron, P., Mestre, O., Kaplan, G., van Soolingen, D., Gao, Q., etal. (2010) Innate immune response to Mycobacterium tuberculosis Beijing and other genotypes. PLoS ONE 5: e13594.
46. Wang, S., Engohang-Ndong, J., and Smith, I. (2007) Structure of the DNA-binding domain of the response regulator PhoP from Mycobacterium tuberculosis. Biochemistry 46: 14751-14761.
47. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., etal. (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129: 1287-1298.
48. WHO (2012) Global Tuberculosis Report.
49. Wolf, A.J., Desvignes, L., Linas, B., Banaiee, N., Tamura, T., Takatsu, K., and Ernst, J.D. (2008) Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 205: 105-115.
50. Zychlinsky, A., Prevost, M.C., and Sansonetti, P.J. (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.