Cathepsin L maturation and activity is impaired in macrophages harboring M. avium and M. tuberculosis

International Immunology

Volumn 18, Issue 6, 2006, Pages 931-939

  Nepal, Rajeev M ^a   Mampe, Stephanie ^a   Shaffer, Brian ^a   Erickson, Ann H ^b   Bryant, Paula ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen presenting cell; Class II MHC; Cysteine protease; Endocytic pathway

Indexed keywords

CATHEPSIN B; CATHEPSIN L; CATHEPSIN S; CYSTEINE PROTEINASE; EPITOPE; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW CELL; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; IMMUNOBLOTTING; MACROPHAGE; MOUSE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; BONE MARROW CELLS; CATHEPSIN B; CATHEPSINS; CYSTEINE ENDOPEPTIDASES; ENZYME ACTIVATION; EPITOPES, T-LYMPHOCYTE; GENES, MHC CLASS II; INTERFERON TYPE II; MACROPHAGES; MICE; MICE, KNOCKOUT; MYCOBACTERIUM AVIUM; MYCOBACTERIUM TUBERCULOSIS; PEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; TUBERCULOSIS;

EID: 33745625884     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxl029     Document Type: Article

References (73)

1. Flynn, J. L. and Chan, J. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93.
2. North, R. J. and Jung, Y. J. 2004. Immunity to tuberculosis. Annu. Rev. Immunol. 22:599.
3. Laupeze, B., Fardel, O., Onno, M. et al. 1999. Differential expression of major histocompatibility complex class Ia, Ib, and II molecules on monocytes-derived dendritic and macrophagic cells. Hum. Immunol. 60:591.
4. Fleischer, J., Soeth, E., Reiling, N., Grage-Griebenow, E., Flad, H. D. and Ernst, M. 1996. Differential expression and function of CD80 (B7-1) and CD86 (B7-2) on human peripheral blood monocytes. J. Immunol. 89:592.
5. Bryant, P. W. and Ploegh, H. 2004. Class II MHC peptide loading by the professionals. Curr. Opin. Immunol. 16:96.
6. Honey, K. and Rudensky, A. Y. 2003. Lysosomal cysteine proteases regulate antigen presentation. Nat. Rev. Immunol. 3:472.
7. Duclos, S., Corsini, R. and Desjardins, M. 2003. Remodeling of endosomes during lysosome biogenesis involves 'kiss and run' fusion events regulated by rab5. J. Cell Sci. 116:907.
8. Bakke, O. and Dobberstein, B. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
9. Benaroch, P., Yilla, M., Raposo, G. et al. 1995. How MHC class II molecules reach the endocytic pathway. EMBO J. 14:37.
10. Lotteau, V., Teyton, L., Peleraux, A. et al. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348:600.
11. Bryant, P. W., Lennon-Dumenil, A. M., Fiebiger, E., Lagaudriere-Gesbert, C. and Pleogh, H. L. 2002. Proteolysis and antigen presentation by MHC class II molecules. Adv. Immunol. 80:71.
12. Driessen, C., Lennon-Dumenil, A. M. and Ploegh, H. 2001. Individual cathepsins degrade immune complexes internalized by antigen-presenting cells via Fc-gamma receptors. Eur. J. Immunol. 31:1592.
13. Pluger, E. B. E., Boes, M., Alfonso, C. et al. 2002. Specific role for cathepsin S in the generation of antigenic peptides in vivo. Eur. J. Immunol. 32:467.
14. Hsieh, C.-S., deRoos, P., Honey, K., Beers, C. and Rudensky, A. Y. 2002. A role for cathepsin L and cathepsin S in peptide generation for MHC class II presentation. J. Immunol. 168:2618.
15. Manoury, B., Mazzeo, D., Ni Li, D. et al. 2003. Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18:489.
16. Nakagawa, T. Y., Brissette, W. H., Lira, P. D. et al. 1999. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10:207.
17. Shi, G. P., Villadangos, J. A., Dranoff, G. et al. 1999. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10:197.
18. Nakagawa, T., Roth, W., Wong, P. et al. 1998. Cathepsin L: Critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280:450.
19. Shi, G. P., Bryant, R. A., Riese, R. et al. 2000. Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J. Exp. Med. 191:1177.
20. Beers, C., Honey, K., Fink, S., Forbush, K. and Rudensky, A. Y. 2003. Differential regulation of cathepsin S and cathepsin L in interferon γ-treated macrophages. J. Exp. Med. 197:169.
21. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P. et al. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678.
22. Clemens, D. L. and Horwitz, M. A. 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J. Exp. Med. 184:1349.
23. Ullrich, H.-J., Beatty, W. L. and Russell, D. G. 2000. Interaction of Mycobacterium avium-containing phagosomes with the antigen presentation pathway. J. Immunol. 165:6073.
24. Walburger, A., Koul, A., Ferrari, G. et al. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304:1800.
25. Vergne, I., Chua, J., Lee, H.-H., Lucas, M., Belisle, J. and Deretic, V. 2005. Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 102:4033.
26. Pancholi, P., Mirza, A., Bhardwaj, N. and Steinman, R. M. 1993. Sequestration from immune CD4+ Tcells of mycobacteria growing in human macrophages. Science 260:984.
27. Gercken, J., Pryjma, J., Ernst, M. and Flad, H.-D. 1994. Defective antigen presentation by Mycobacterium tuberculosis-infected monocytes. Infect. Immun. 62:3472.
28. Hmama, Z., Gabathuler, R., Jefferies, W., de Jong, G. and Reiner, N. E. 1998. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161:4882.
29. Wojciechowski, W., DeSanctis, J., Skamene, E. and Radzioch, D. 1999. Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette-Guerin involves class II transactivator and depends on the Nramp 1 gene. J. Immunol. 163:2688.
30. Hussain, S., Zwilling, B. S. and Lafuse, W. P. 1999. Mycobacterium avium infection of mouse macrophages inhibits IFN-γ Janus kinase-STAT signaling and gene induction by down-regulation of the IFN-γ receptor. J. Immunol. 163:2041.
31. Noss, E. H., Pai, R. K., Sellati, T. J. et al. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167:910.
32. Ramachandra, L., Noss, E. H., Boom, W. H. and Harding, C. V. 2001. Processing of Mycobacterium tuberculosis antigen 85B involves intraphagosomal formation of peptide-major histocompatibility complex II complexes and is inhibited by live bacilli that decrease phagosome maturation. J. Exp. Med. 194:1421.
33. Pai, R. K., Convrey, M., Hamilton, T. A., Boom, W. H. and Harding, C. V. 2003. 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.
34. Fulton, S. A., Reba, S. M., Pai, R. K. et al. 2004. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. J. Immunol. 72:2101.
35. Sendide, K., Deghmane, A.-E., Pechkovsky, D., Av-Gay, Y., Talal, A. and Hmama, Z. 2005. Mycobacterium bovis BCG attenuates surface expression of mature class II molecules through IL-10-dependent inhibition of cathepsin S. J. Immunol. 175:5324.
36. Wang, Y., Curry, H. M., Zwilling, B. S. and Lafuse, W. P. 2005. Mycobacteria inhibition of IFN-gamma induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J. Immunol. 174:5687.
37. Beatty, W. L., Ullrich, H.-J. and Russell, D. G. 2001. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur. J. Cell Biol. 80:31.
38. Lennon-Dumenil, A. M., Bakker, A. H., Maehr, R. et al. 2002. Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J. Exp. Med. 196:529.
39. Lennon-Dumenil, A. M., Roberts, R. A., Valentijn, K. et al. 2001. The p41 isoform of invariant chain is a chaperone for cathepsin L. EMBO J. 20:4055.
40. Deussing, J., Roth, W., Saftig, P., Peters, C., Ploegh, H. L. and Villadangos, J. A. 1998. Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc. Natl Acad. Sci. USA 95:4516.
41. Inaba, K., Inaba, M., Romani, N. et al. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176:1693.
42. McIntyre, G. F. and Erickson, A. H. 1993. The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. Proc. Natl Acad. Sci. USA 90:10588.
43. Wolf, P. R., Tourne, S., Miyazaki, T., Benoist, C., Mathis, D. and Ploegh, H. L. 1998. The phenotype of H-2M-deficient mice is dependent on the MHC class II molecules expressed. Eur. J. Immunol. 28:2605.
44. Palmer, J. T., Rasnick, D., Klaus, J. L. and Bromme, D. 1995. Vinyl sulfones as mechanism-based cysteine protease inhibitors. J. Med. Chem. 38:3193.
45. Collette, J., Bocock, J. P., Ahn, K. et al. 2004. Biosynthesis and alternate targeting of the lysosomal cysteine protease cathepsin L. Int. Rev. Cytol. 241:1.
46. Erickson, A. H. 1989. Biosynthesis of lysosomal endopeptidases. J. Cell. Biochem. 40:31.
47. Ishidoh, K., Saido, T. C., Kawashima, S. et al. 1998. Multiple processing of procathepsin L to cathepsin L in vivo. Biochem. Biophys. Res. Commun. 252:202.
48. McGrath, M. E. 1999. The lysosomal cysteine proteases. Annu. Rev. Biophys. Biomol. Struct. 28:181.
49. Punturieri, A., Filippov, S., Allen, E. et al. 2000. Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J. Exp. Med. 192:789.
50. Reddy, V., Zhang, Q. Y. and Weiss, S. J. 1995. Pericellular mobilization of the tissue-destructive cysteine proteinases, cathepsins B, L, and S, by human monocyte-derived macrophages. Proc. Natl Acad. Sci. USA 92:3849.
51. Fiebiger, E., Maehr, R., Villadangos, J. A. et al. 2002. Invariant chain controls the activity of extracellular cathepsin L. J. Exp. Med. 196:1263.
52. Menard, R., Carmona, E., Takebe, S. et al. 1998. Autocatalytic processing of recombinant human procathepsin L. J. Biol. Chem. 273:4478.
53. Ting, L. M., Kim, A. C., Cattamanchi, A. and Ernst, J. D. 1999. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898.
54. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H. and Russell, D. G. 1998. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160:1290. 1290.
55. Sturgill-Koszycki, S., Schaible, U. E. and Russell, D. G. 1996. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J. 15:6960.
56. Ullrich, H.-J., Beatty, W. L. and Russell, D. G. 1999. Direct delivery of procathepsin D to phagosomes: Implications for phagosome biogenesis and parasitism by Mycobacterium. Eur. J. Cell Biol. 78:739.
57. Mills, S. D. and Finlay, B. B. 1998. Isolation and characterization of Salmonella typhimurium and Yersinia pseudotuberculosis-containing phagosomes from infected mouse macrophages: Y. pseudotuberculosis traffics to terminal lysosomes where they are degraded. Eur. J. Cell Biol. 77:35.
58. Guerin, I. and de Chastellier, C. 2000. Pathogenic mycobacteria disrupt the macrophage actin filament network. Infect. Immun. 68:2655.
59. Pietersen, R., Thilo, L. and de Chastellier, C. 2004. Mycobacterium tuberculosis and Mycobacterium avium modify the composition of the phagosomal membrane in infected macrophages by selective depletion of cell surface-derived glycoconjugates. Eur. J. Cell Biol. 83:153.
60. Miller, B. H., Fratti, R. A., Poschet, J. F. et al. 2004. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect. Immun. 72:2872.
61. Anes, E., Kuhnel, M. P., Bos, E., Moniz-Pereira, J., Habermann, A. and Griffiths, G. 2003. Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat. Cell Biol. 5:793.
62. Shirahama-Noda, K., Yamamoto, A., Sugihara, K., Hashimoto, N., Asano, M., Nishimura, T. and Hara-Nishimura, I. 2003. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase deficient mice. J. Biol. Chem. 278:33194.
63. Maehr, R., Hang, H. D., Mintern, J. D. et al. 2005. Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in mice. J. Immunol. 174:7066.
64. Russell, D. G., Purdy, G. E., Owens, R. M., Rohde, K. H. and Yates, R. M. 2005. Mycobacterium tuberculosis and the four-minute phagosome. ASM News 71:459.
65. Vergne, I., Chua, J. and Deretic, V. 2003. Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J. Exp. Med. 198:653.
66. Fratti, R. A., Chua, J., Vergne, I. and Deretic, V. 2003. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl Acad. Sci. USA 100:5437.
67. Rivera-Marrero, C. A., Stewart, J., Shafer, W. M. and Roman, J. 2004. 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.
68. Gehring, A. J., Dobos, K. M., Belisle, J., Harding, C. V. and Boom, W. H. 2004. Mycobacterium tuberculosis LprG (Rv1411c): A novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J. Immunol. 173:2660.
69. Pai, R. K., Pennini, M. E., Tobian, A. A. R., Canaday, D. H., Boom, W. H. and Harding, C. V. 2004. Prolonged toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits gamma interferon-induced regulation of selected genes in macrophages. Infect. Immun. 72:6603.
70. Ogrinc, T., Dolenc, I., Ritonja, A. and Turk, V. 1993. Purification of the complex of cathepsin L and the MHC class II-associated invariant chain fragment from human kidney. FEBS Lett. 336:555.
71. Guncar, G., Pungercic, G., Klemencic, I., Turk, V. and Turk, D. 1999. Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 18:793.
72. Fineschi, B., Arneson, L. S., Naujokas, M. F. and Miller, J. 1995. Proteolysis of major histocompatibility complex class II-associated invariant chain is regulated by the alternatively spliced gene product, p41. Proc. Natl Acad. Sci. USA 92:10257.
73. Ohashi, K., Naruto, M., Nakaki, T. and Sano, E. 2003. Identification of interleukin-8 converting enzyme as cathepsin L. Biochim. Biophys. Acta 1649:30.