Role of Cathepsins in Mycobacterium tuberculosis Survival in Human Macrophages

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Pires, David ^a,b   Marques, Joana ^a   Pombo, João Palma ^a   Carmo, Nuno ^a,b   Bettencourt, Paulo ^a,b   Neyrolles, Olivier ^c,d   Lugo Villarino, Geanncarlo ^c,d   Anes, Elsa ^b  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

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

^d UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; CYSTATIN; ISOENZYME;

CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; MACROPHAGE; METABOLISM; MICROBIAL VIABILITY; MYCOBACTERIUM TUBERCULOSIS; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; VIROLOGY;

CATHEPSINS; CELL LINE, TUMOR; CELLS, CULTURED; CYSTATINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HOST-PATHOGEN INTERACTIONS; HUMANS; ISOENZYMES; MACROPHAGES; MICROBIAL VIABILITY; MYCOBACTERIUM TUBERCULOSIS; RNA INTERFERENCE;

EID: 84985995945     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32247     Document Type: Article

References (61)

1. WHO. Global Tuberculosis Report 2013. World Health Organization (World Health Organization Press, 2013).
2. Kang, D. D., Lin, Y., Moreno, J.-R., Randall, T. D. & Khader, S. A. Profiling early lung immune responses in the mouse model of tuberculosis. PLoS One 6, e16161 (2011).
3. Russell, D. G., Vanderven, B. C., Glennie, S., Mwandumba, H. & Heyderman, R. S. The macrophage marches on its phagosome: dynamic assays of phagosome function. Nat. Rev. Immunol. 9, 594-600 (2009).
4. Russell, D. G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat. Rev. Mol. Cell Biol. 2, 569-577 (2001).
5. Deretic, V. et al. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell. Microbiol. 8, 719-727 (2006).
6. Armstrong, J. A. & Hart, P. D. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134, 713-740 (1971).
7. Clemens, D. L. & Horwitz, M. A. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181, 257-270 (1995).
8. Jordao, L., Bleck, C. K. E., Mayorga, L., Griffiths, G. & Anes, E. On the killing of mycobacteria by macrophages. Cell. Microbiol. 10, 529-548 (2008).
9. Cooper, A. M. Cell-mediated immune responses in tuberculosis. Annu. Rev. Immunol. 27, 393-422 (2009).
10. Gutierrez, M. G. et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766 (2004).
11. Purdy, G. E. & Russell, D. G. Lysosomal ubiquitin and the demise of mycobacterium tuberculosis. Cell. Microbiol. 9, 2768-2774 (2007).
12. Herbst, S., Schaible, U. E. & Schneider, B. E. Interferon gamma activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS One 6 (2011).
13. Anes, E. et al. Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat. Cell Biol. 5, 793-802 (2003).
14. Gutierrez, M. G. et al. NF-kappa B activation controls phagolysosome fusion-mediated killing of mycobacteria by macrophages. J. Immunol. 181, 2651-2663 (2008).
15. Gutierrez, M. G., Gonzalez, A. P., Anes, E. & Griffiths, G. Role of lipids in killing mycobacteria by macrophages: Evidence for NF-κ B-dependent and -independent killing induced by different lipids. Cell. Microbiol. 11, 406-420 (2009).
16. Behar, S. M., Martin, C. J., Nunes-Alves, C., Divangahi, M. & Remold, H. G. Lipids, apoptosis, and cross-presentation: links in the chain of host defense against Mycobacterium tuberculosis. Microbes Infect. 13, 749-756 (2011).
17. Winau, F. et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24, 105-117 (2006).
18. Alonso, S., Pethe, K., Russell, D. G. & Purdy, G. E. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. USA 104, 6031-6036 (2007).
19. Turk, V. et al. Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta 1824, 68-88 (2012).
20. Conus, S. & Simon, H.-U. Cathepsins and their involvement in immune responses. Swiss Med. Wkly. 140, w13042 (2010).
21. Hole, C. R., Bui, H., Wormley, F. L. & Wozniak, K. L. Mechanisms of dendritic cell lysosomal killing of Cryptococcus. Sci. Rep. 2, 739 (2012).
22. Bewley, M. a et al. A cardinal role for cathepsin d in co-ordinating the host-mediated apoptosis of macrophages and killing of pneumococci. PLoS Pathog. 7, e1001262 (2011).
23. Steinwede, K. et al. Cathepsin G and neutrophil elastase contribute to lung-protective immunity against mycobacterial infections in mice. J. Immunol. 188, 4476-4487 (2012).
24. Rivera-Marrero, C. A., Stewart, J., Shafer, W. M. & Roman, J. The down-regulation of cathepsin G in THP-1 monocytes after infection with Mycobacterium tuberculosis is associated with increased intracellular survival of bacilli. Infect. Immun. 72, 5712-5721 (2004).
25. Soualhine, H. et al. Mycobacterium bovis bacillus Calmette-Guérin secreting active cathepsin S stimulates expression of mature MHC class II molecules and antigen presentation in human macrophages. J. Immunol. 179, 5137-5145 (2007).
26. Hsing, L. C. & Rudensky, A. Y. The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol. Rev. 207, 229-241 (2005).
27. Villadangos, J. A. & Ploegh, H. L. Proteolysis in MHC class II antigen presentation: who's in charge? Immunity 12, 233-239 (2000).
28. Beers, C. et al. Cathepsin S controls MHC class II-mediated antigen presentation by epithelial cells in vivo. J. Immunol. 174, 1205-1212 (2005).
29. Shi, G. P. et al. Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J. Exp. Med. 191, 1177-1186 (2000).
30. Tang, C.-H. et al. Murine cathepsin F deficiency causes neuronal lipofuscinosis and late-onset neurological disease. Mol. Cell. Biol. 26, 2309-2316 (2006).
31. Yates, R. M., Hermetter, A., Taylor, G. a & Russell, D. G. Macrophage activation downregulates the degradative capacity of the phagosome. Traffic 8, 241-250 (2007).
32. Savina, A. et al. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126, 205-218 (2006).
33. Savina, A. & Amigorena, S. Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219, 143-156 (2007).
34. Pierre, P. & Mellman, I. Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93, 1135-1145 (1998).
35. Simeone, R. et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog. 8 (2012).
36. Mishra, B. B. et al. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell. Microbiol. 12, 1046-1063 (2010).
37. Welin, A., Eklund, D., Stendahl, O. & Lerm, M. Human macrophages infected with a high burden of ESAT-6-expressing M. tuberculosis undergo caspase-1- and cathepsin B-independent necrosis. PLoS One 6, e20302 (2011).
38. Altaf, M., Miller, C. H., Bellows, D. S. & O'Toole, R. Evaluation of the Mycobacterium smegmatis and BCG models for the discovery of Mycobacterium tuberculosis inhibitors. Tuberculosis (Edinb). 90, 333-337 (2010).
39. Villeneuve, C. et al. Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process. J. Lipid Res. 46, 475-483 (2005).
40. Tailleux, L. et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 3, e1403 (2008).
41. Hanada, K. et al. Isolation and Characterization of E-64, a New Thiol Protease Inhibitor. Agric. Biol. Chem. 42, 523-528 (1978).
42. Rawlings, N. D., Waller, M., Barrett, A. J. & Bateman, A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 42, D503-D509 (2014).
43. Brix, K., Dunkhorst, A., Mayer, K. & Jordans, S. Cysteine cathepsins: cellular roadmap to different functions. Biochimie 90, 194-207 (2008).
44. Beers, C., Honey, K., Fink, S., Forbush, K. & Rudensky, a. Differential Regulation of Cathepsin S and Cathepsin L in Interferon -treated Macrophages. J. Exp. Med. 197, 169-179 (2003).
45. Armstrong, J. A. & Hart, P. D. 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. 142, 1-16 (1975).
46. Brooks, M. N. et al. NOD2 controls the nature of the inflammatory response and subsequent fate of Mycobacterium tuberculosis and M. bovis BCG in human macrophages. Cell. Microbiol. 13, 402-418 (2011).
47. Rudensky, A. & Beers, C. In Cytokines as Potential Therapeutic Targets for Inflammatory Skin Diseases (eds Numerof, R., Dinarello, C. A. & Asadullah, K.) 56, 81-95 (Springer Berlin Heidelberg, 2005).
48. Podinovskaia, M., Lee, W., Caldwell, S. & Russell, D. G. Infection of macrophages with Mycobacterium tuberculosis induces global modifications to phagosomal function. Cell. Microbiol. 15, 843-859 (2013).
49. Claus, V. et al. Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J. Biol. Chem. 273, 9842-9851 (1998).
50. Lautwein, A. et al. Inflammatory stimuli recruit cathepsin activity to late endosomal compartments in human dendritic cells. Eur. J. Immunol. 32, 3348-3357 (2002).
51. Willingham, S. B. et al. Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/ cryopyrin/NLRP3 and ASC. Cell Host Microbe 2, 147-159 (2007).
52. Nepal, R. M., Mampe, S., Shaffer, B., Erickson, A. H. & Bryant, P. Cathepsin L maturation and activity is impaired in macrophages harboring M. avium and M. tuberculosis. Int. Immunol. 18, 931-939 (2006).
53. Russell, D. G. Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol. Rev. 240, 252-268 (2011).
54. Beatty, W. L. et al. Trafficking and release of mycobacterial lipids from Infected Macrophages. Traffic 1, 1-13 (2000).
55. McLaughlin, B. et al. A mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog. 3, e105 (2007).
56. Romagnoli, A. et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8, 1357-1370 (2012).
57. Yates, R. M., Hermetter, A. & Russell, D. G. The kinetics of phagosome maturation as a function of phagosome/lysosome fusion and acquisition of hydrolytic activity. Traffic 6, 413-420 (2005).
58. Wang, C. et al. Innate immune response to Mycobacterium tuberculosis Beijing and other genotypes. PLoS One 5, e13594 (2010).
59. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
60. Troegeler, A. et al. An efficient siRNA-mediated gene silencing in primary human monocytes, dendritic cells and macrophages. Immunol. Cell Biol. 92, 699-708 (2014).
61. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).