Suppression of autophagy and antigen presentation by Mycobacterium tuberculosis PE-PGRS47

Nature Microbiology

Volumn 1, Issue , 2016, Pages

  Saini, Neeraj K ^a   Baena, Andres ^a,b   Ng, Tony W ^a   Venkataswamy, Manjunatha M ^a,c   Kennedy, Steven C ^a   Kunnath Velayudhan, Shajo ^a   Carreño, Leandro J ^a,d   Xu, Jiayong ^a   Chan, John ^a   Larsen, Michelle H ^a   Jacobs, William R ^a   Porcelli, Steven A ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

^d UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HLA ANTIGEN CLASS 2;

ADAPTIVE IMMUNITY; ANIMAL; ANTIGEN PRESENTATION; AUTOPHAGY; C57BL MOUSE; CELL LINE; DENDRITIC CELL; FEMALE; GENE DELETION; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN PRESENTATION; AUTOPHAGY; BACTERIAL PROTEINS; CELL LINE; DENDRITIC CELLS; FEMALE; GENE DELETION; GENE EXPRESSION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84982232986     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.133     Document Type: Article

References (51)

1. Wolf, A. J. et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol. 179, 2509-2519 (2007).
2. Mogues, T., Goodrich, M. E., Ryan, L., LaCourse, R. & North, R. J. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 193, 271-280 (2001).
3. Repique, C. J. et al. Susceptibility of mice deficient in the MHC class II transactivator to infection with Mycobacterium tuberculosis. Scand. J. Immunol. 58, 15-22 (2003).
4. Scanga, C. A. et al. Depletion of CD4+ T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon gamma and nitric oxide synthase 2. J. Exp. Med. 192, 347-358 (2000).
5. Baena, A. & Porcelli, S. A. Evasion and subversion of antigen presentation by Mycobacterium tuberculosis. Tissue Antigens 74, 189-204 (2009).
6. Harding, C. V. & Boom, W. H. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nature Rev. Microbiol. 8, 296-307 (2010).
7. Pai, R. K., Convery, M., Hamilton, T. A., Boom, W. H. & Harding, C. V. Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J. Immunol. 171, 175-184 (2003).
8. Pennini, M. E. et al. CCAAT/enhancer-binding protein β and δ binding to CIITA promoters is associated with the inhibition of CIITA expression in response to Mycobacterium tuberculosis 19-kDa lipoprotein. J. Immunol. 179, 6910-6918 (2007).
9. Dengjel, J. et al. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl Acad. Sci. USA 102, 7922-7927 (2005).
10. Paludan, C. et al. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307, 593-596 (2005).
11. Schmid, D., Pypaert, M. & Munz, C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 26, 79-92 (2007).
12. Zhou, D. et al. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22, 571-581 (2005).
13. Singh, S. B., Davis, A. S., Taylor, G. A. & Deretic, V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438-1441 (2006).
14. Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766 (2004).
15. Shin, D. M. et al. Mycobacterium tuberculosis Eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathogens 6, e1001230 (2010).
16. Romagnoli, A. et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8, 1357-1370 (2012).
17. Espert, L., Beaumelle, B. & Vergne, I. Autophagy in Mycobacterium tuberculosis and HIV infections. Front. Cell. Infect. Microbiol. 5, 49 (2015).
18. Rudensky, A., Preston-Hurlburt, P., Hong, S. C., Barlow, A. & Janeway, C. A. Jr. Sequence analysis of peptides bound to MHC class II molecules. Nature 353, 622-627 (1991).
19. Deretic, V., Saitoh, T. & Akira, S. Autophagy in infection, inflammation and immunity. Nature Rev. Immunol. 13, 722-737 (2013).
20. Munz, C. Enhancing immunity through autophagy. Annu. Rev. Immunol. 27, 423-449 (2009).
21. Mizushima, N., Yoshimori, T. & Levine, B. Methods in mammalian autophagy research. Cell 140, 313-326 (2010).
22. Tian, C. & Jian-Ping, X. Roles of PE-PGRS family in Mycobacterium tuberculosis pathogenesis and novel measures against tuberculosis. Microb. Pathog. 49, 311-314 (2010).
23. Brennan, M. J. & Delogu, G. The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol. 10, 246-249 (2002).
24. Bardarov, S. et al. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007-3017 (2002).
25. Rusten, T. E. & Stenmark, H. p62, an autophagy hero or culprit? Nature Cell Biol. 12, 207-209 (2010).
26. Bold, T. D., Banaei, N., Wolf, A. J. & Ernst, J. D. Suboptimal activation of antigen-specific CD4+ effector cells enables persistence of M. tuberculosis in vivo. PLoS Pathogens 7, e1002063 (2011).
27. Reiley, W. W. et al. ESAT-6-specific CD4T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc. Natl Acad. Sci. USA. 105, 10961-10966 (2008).
28. Kruh, N. A., Troudt, J., Izzo, A., Prenni, J. & Dobos, K. M. Portrait of a pathogen: the Mycobacterium tuberculosis proteome in vivo. PLoS ONE 5, e13938 (2010).
29. Simeone, R., Bottai, D., Frigui, W., Majlessi, L. & Brosch, R. ESX/type VII secretion systems of mycobacteria: insights into evolution, pathogenicity and protection. Tuberculosis (Edinb.) 95(Suppl 1), S150-S154 (2015).
30. Srivastava, V., Jain, A., Srivastava, B. S. & Srivastava, R. Selection of genes of Mycobacterium tuberculosis upregulated during residence in lungs of infected mice. Tuberculosis (Edinb.) 88, 171-177 (2008).
31. Copin, R. et al. Sequence diversity in the pe-pgrs genes of Mycobacterium tuberculosis is independent of human T cell recognition. mBio 5, e00960-e00913 (2014).
32. Lee, H. K. et al. In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 32, 227-239 (2010).
33. Deretic, V. Autophagy, an immunologic magic bullet: Mycobacterium tuberculosis phagosome maturation block and how to bypass it. Future Microbiol. 3, 517-524 (2008).
34. Koul, A., Herget, T., Klebl, B. & Ullrich, A. Interplay between mycobacteria and host signalling pathways. Nature Rev. Microbiol. 2, 189-202 (2004).
35. Watson, R. O., Manzanillo, P. S. & Cox, J. S. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150, 803-815 (2012).
36. Ouimet, M. et al. Mycobacterium tuberculosis induces the miR-33 locus to reprogram autophagy and host lipid metabolism. Nature Immunol. 17, 677-686 (2016).
37. Kimmey, J. M. et al. Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection. Nature 528, 565-569 (2015).
38. Cadieux, N. et al. Induction of cell death after localization to the host cell mitochondria by the Mycobacterium tuberculosis PE-PGRS33 protein. Microbiology 157, 793-804 (2011).
39. Braunstein, M., Bardarov, S. S. & Jacobs, W. R. Jr. Genetic methods for deciphering virulence determinants of Mycobacterium tuberculosis. Methods Enzymol. 358, 67-99 (2002).
40. Stover, C. K. et al. New use of BCG for recombinant vaccines. Nature 351, 456-460 (1991).
41. Hinchey, J. et al. Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J. Clin. Invest. 117, 2279-2288 (2007).
42. Lutz, M. B. et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92 (1999).
43. Houben, E. N., Nguyen, L. & Pieters, J. Interaction of pathogenic mycobacteria with the host immune system. Curr. Opin. Microbiol. 9, 76-85 (2006).
44. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. & Ohsumi, Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101-1111 (2004).
45. Forestier, C. et al. Improved outcomes in NOD mice treated with a novel Th2 cytokine-biasing NKT cell activator. J. Immunol. 178, 1415-1425 (2007).
46. Yuk, J. M. et al. Vitamin D3 induces autophagy in human monocytes/ macrophages via cathelicidin. Cell Host Microbe 6, 231-243 (2009).
47. Averill, L. E. et al. Screening of a cosmid library of Mycobacterium bovis BCG in Mycobacterium smegmatis for novel T-cell stimulatory antigens. Res. Microbiol. 144, 349-362 (1993).
48. Barlow, A. K., He, X. & Janeway, C. Jr. Exogenously provided peptides of a selfantigen can be processed into forms that are recognized by self-T cells. J. Exp. Med. 187, 1403-1415 (1998).
49. Clarke, L. & Carbon, J. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome. Cell 9, 91-99 (1976).
50. Pavelka, M. S. Jr & Jacobs, W. R. Jr. Comparison of the construction of unmarked deletion mutations in Mycobacterium smegmatis, Mycobacterium bovis bacillus Calmette-Guerin, and Mycobacterium tuberculosis H37Rv by allelic exchange. J. Bacteriol. 181, 4780-4789 (1999).
51. Prados-Rosales, R. et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest. 121, 1471-1483 (2011).