Distinct protease requirements for antigen presentation in vitro and in vivo

Journal of Immunology

Volumn 184, Issue 5, 2010, Pages 2423-2431

  Matthews, Stephen P ^a   Werber, Ingrid ^b   Deussing, Jan ^c   Peters, Christoph ^b   Reinheckel, Thomas ^b   Watts, Colin ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE ENDOPEPTIDASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEINASE; TETANUS TOXIN; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE; LEGUMAIN; PEPTIDE FRAGMENT; TETANUS TOXIN FRAGMENT C;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CELL IMMORTALIZATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE; ANIMAL; ANTIGEN PRESENTING CELL; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOBLOTTING; IMMUNOLOGY; LYSOSOME; MALE; METABOLISM; MOUSE MUTANT;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; B-LYMPHOCYTES; CELL PROLIFERATION; CYSTEINE ENDOPEPTIDASES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNIZATION; IMMUNOBLOTTING; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; T-LYMPHOCYTES; TETANUS TOXIN;

EID: 77951904981     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901486     Document Type: Article

References (51)

1. Chapman, H. A. 2006. Endosomal proteases in antigen presentation. Curr. Opin. Immunol. 18: 78-84.
2. Watts, C. 2004. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat. Immunol. 5: 685-692.
3. Jensen, P. E. 2007. Recent advances in antigen processing and presentation. Nat. Immunol. 8: 1041-1048.
4. Plüger, E. B., M. Boes, C. Alfonso, C. J. Schröter, H. Kalbacher, H. L. Ploegh, and C. Driessen. 2002. Specific role for cathepsin S in the generation of antigenic peptides in vivo. Eur. J. Immunol. 32: 467-476.
5. Honey, K., T. Nakagawa, C. Peters, and A. Rudensky. 2002. Cathepsin L regulates CD4+ T cell selection independently of its effect on invariant chain: a role in the generation of positively selecting peptide ligands. J. Exp. Med. 195: 1349-1358.
6. Deussing, J., W. Roth, P. Saftig, C. Peters, H. L. Ploegh, and J. A. Villadangos. 1998. Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc. Natl. Acad. Sci. USA 95: 4516-4521.
7. Nakagawa, T., W. Roth, P. Wong, A. Nelson, A. Farr, J. Deussing, J. A. Villadangos, H. Ploegh, C. Peters, and A. Y. Rudensky. 1998. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280: 450-453. (Pubitemid 28208170)
8. Moss, C. X., J. A. Villadangos, and C. Watts. 2005. Destructive potential of the aspartyl protease cathepsin D in MHC class II-restricted antigen processing. Eur. J. Immunol. 35: 3442-3451.
9. Marturano, J., R. Longhi, V. Russo, and M. P. Protti. 2008. Endosomal proteases influence the repertoire of MAGE-A3 epitopes recognized in vivo by CD4+ T cells. Cancer Res. 68: 1555-1562. (Pubitemid 351346865)
10. Chain, B. M., P. Free, P. Medd, C. Swetman, A. B. Tabor, and N. Terrazzini. 2005. The expression and function of cathepsin E in dendritic cells. J. Immunol. 174: 1791-1800. (Pubitemid 40223918)
11. Chen, J.-M., P. M. Dando, R. A. E. Stevens, M. Fortunato, and A. J. Barrett. 1998. Cloning and expression of mouse legumain, a lysosomal endopeptidase. Biochem. J. 335: 111-117. (Pubitemid 28477056)
12. Manoury, B., E. W. Hewitt, N. Morrice, P. M. Dando, A. J. Barrett, and C. Watts. 1998. An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396: 695-699. (Pubitemid 29003950)
13. Watts, C., S. P. Matthews, D. Mazzeo, B. Manoury, and C. X. Moss. 2005. Asparaginyl endopeptidase: case history of a class II MHC compartment protease. Immunol. Rev. 207: 218-228.
14. Antoniou, A. N., S. L. Blackwood, D. Mazzeo, and C. Watts. 2000. Control of antigen presentation by a single protease cleavage site. Immunity 12: 391-398.
15. Costantino, C. M., H. C. Hang, S. C. Kent, D. A. Hafler, and H. L. Ploegh. 2008. Lysosomal cysteine and aspartic proteases are heterogeneously expressed and act redundantly to initiate human invariant chain degradation. J. Immunol. 180: 2876-2885.
16. Manoury, B., D. Mazzeo, L. Fugger, N. Viner, M. Ponsford, H. Streeter, G. Mazza, D. C. Wraith, and C. Watts. 2002. Destructive processing by asparagine endopeptidase limits presentation of a dominant T cell epitope in MBP. Nat. Immunol. 3: 169-174.
17. Beck, H., G. Schwarz, C. J. Schröter, M. Deeg, D. Baier, S. Stevanovic, E. Weber, C. Driessen, and H. Kalbacher. 2001. Cathepsin S and an asparaginespecific endoprotease dominate the proteolytic processing of human myelin basic protein in vitro. Eur. J. Immunol. 31: 3726-3736.
18. Manoury, B., D. Mazzeo, D. N. Li, J. Billson, K. Loak, P. Benaroch, and C. Watts. 2003. Asparagine endopeptidase can initiate the removal of the MHC class II invariant chain chaperone. Immunity 18: 489-498. (Pubitemid 36513631)
19. Davidson, H. W., P. A. Reid, A. Lanzavecchia, and C. Watts. 1991. Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell 67: 105-116.
20. Simitsek, P. D., D. G. Campbell, A. Lanzavecchia, N. Fairweather, and C. Watts. 1995. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J. Exp. Med. 181: 1957-1963.
21. Bernasconi, N. L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
22. Fritzell, B., and S. Plotkin. 1992. Efficacy and safety of a Haemophilus influenzae type b capsular polysaccharide-tetanus protein conjugate vaccine. J. Pediatr. 121: 355-362.
23. West, M. A., A. N. Antoniou, A. R. Prescott, T. Azuma, D. J. Kwiatkowski, and C. Watts. 1999. Membrane ruffling, macropinocytosis and antigen presentation in the absence of gelsolin in murine dendritic cells. Eur. J. Immunol. 29: 3450-3455.
24. West, M. A., R. P. Wallin, S. P. Matthews, H. G. Svensson, R. Zaru, H. G. Ljunggren, A. R. Prescott, and C. Watts. 2004. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305: 1153-1157.
25. Fairweather, N. F., and V. A. Lyness. 1986. The complete nucleotide sequence of tetanus toxin. Nucleic Acids Res. 14: 7809-7812.
26. Davidson, H. W., M. A. West, and C. Watts. 1990. Endocytosis, intracellular trafficking, and processing of membrane IgG and monovalent antigen/membrane IgG complexes in B lymphocytes. J. Immunol. 144: 4101-4109.
27. Li, D. N., S. P. Matthews, A. N. Antoniou, D. Mazzeo, and C. Watts. 2003. Multistep autoactivation of asparaginyl endopeptidase in vitro and in vivo. J. Biol. Chem. 278: 38980-38990.
28. Shirahama-Noda, K., A. Yamamoto, K. Sugihara, N. Hashimoto, M. Asano, M. Nishimura, and I. Hara-Nishimura. 2003. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice. J. Biol. Chem. 278: 33194-33199.
29. Loak, K., D. N. Li, B. Manoury, J. Billson, F. Morton, E. Hewitt, and C. Watts. 2003. Novel cell-permeable acyloxymethylketone inhibitors of asparaginyl endopeptidase. Biol. Chem. 384: 1239-1246.
30. Antoniou, A. N., and C. Watts. 2002. Antibody modulation of antigen presentation: positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcgammaRII. Eur. J. Immunol. 32: 530-540.
31. Burster, T., A. Beck, E. Tolosa, V. Marin-Esteban, O. Rötzschke, K. Falk, A. Lautwein, M. Reich, J. Brandenburg, G. Schwarz, et al. 2004. Cathepsin G, and not the asparagine-specific endoprotease, controls the processing of myelin basic protein in lysosomes from human B lymphocytes. J. Immunol. 172: 5495-5503.
32. Burster, T., A. Beck, E. Tolosa, P. Schnorrer, R. Weissert, M. Reich, M. Kraus, H. Kalbacher, H. U. Häring, E. Weber, et al. 2005. Differential processing of autoantigens in lysosomes from human monocyte-derived and peripheral blood dendritic cells. J. Immunol. 175: 5940-5949.
33. Moss, C. X., T. I. Tree, and C. Watts. 2007. Reconstruction of a pathway of antigen processing and class II MHC peptide capture. EMBO J. 26: 2137-2147. (Pubitemid 46625795)
34. Rawlings, N. D., F. R. Morton, C. Y. Kok, J. Kong, and A. J. Barrett. 2008. MEROPS: the peptidase database. Nucleic Acids Res. 36(Database issue): D320-D325.
35. Shi, G. P., J. A. Villadangos, G. Dranoff, C. Small, L. Gu, K. J. Haley, R. Riese, H. L. Ploegh, and H. A. Chapman. 1999. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10: 197-206.
36. Nakagawa, T. Y., W. H. Brissette, P. D. Lira, R. J. Griffiths, N. Petrushova, J. Stock, J. D. McNeish, S. E. Eastman, E. D. Howard, S. R. M. Clarke, et al. 1999. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10: 207-217.
37. Shen, L., L. J. Sigal, M. Boes, and K. L. Rock. 2004. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21: 155-165. (Pubitemid 39094046)
38. Tulone, C., Y. Uchiyama, M. Novelli, N. Grosvenor, P. Saftig, and B. M. Chain. 2007. Haematopoietic development and immunological function in the absence of cathepsin D. BMC Immunol. 8: 22. (Pubitemid 350048272)
39. Lanzavecchia, A. 1985. Antigen-specific interaction between T and B cells. Nature 314: 537-539.
40. Watts, C. 2001. Antigen processing in the endocytic compartment. Curr. Opin. Immunol. 13: 26-31.
41. Maehr, R., H. C. Hang, J. D. Mintern, Y. M. Kim, A. Cuvillier, M. Nishimura, K. Yamada, K. Shirahama-Noda, I. Hara-Nishimura, and H. L. Ploegh. 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: 7066-7074. (Pubitemid 40705672)
42. Sepulveda, F. E., S. Maschalidi, R. Colisson, L. Heslop, C. Ghirelli, E. Sakka, A. M. Lennon-Duménil, S. Amigorena, L. Cabanie, and B. Manoury. 2009. Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 31: 737-748.
43. Deol, P., D. M. Zaiss, J. J. Monaco, and A. J. Sijts. 2007. Rates of processing determine the immunogenicity of immunoproteasome-generated epitopes. J. Immunol. 178: 7557-7562. (Pubitemid 46898024)
44. Savina, A., C. Jancic, S. Hugues, P. Guermonprez, P. Vargas, I. C. Moura, A. M. Lennon-Duménil, M. C. Seabra, G. Raposo, and S. Amigorena. 2006. NOX2 controls phagosomal pH to regulate antigen processing during cross-presentation by dendritic cells. Cell 126: 205-218. (Pubitemid 44026552)
45. Delamarre, L., R. Couture, I. Mellman, and E. S. Trombetta. 2006. Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis. J. Exp. Med. 203: 2049-2055.
46. Burster, T., M. Reich, N. Zaidi, W. Voelter, B. O. Boehm, and H. Kalbacher. 2008. Cathepsin E regulates the presentation of tetanus toxin C-fragment in PMA activated primary human B cells. Biochem. Biophys. Res. Commun. 377: 1299-1303.
47. Delamarre, L., M. Pack, H. Chang, I. Mellman, and E. S. Trombetta. 2005. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307: 1630-1634. (Pubitemid 40354746)
48. Dudziak, D., A. O. Kamphorst, G. F. Heidkamp, V. R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H. W. Lee, C. G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
49. Stoeckle, C., V. Sommandas, E. Adamopoulou, K. Belisle, S. Schiekofer, A. Melms, E. Weber, C. Driessen, B. O. Boehm, E. Tolosa, and T. Burster. 2009. Cathepsin G is differentially expressed in primary human antigen-presenting cells. Cell. Immunol. 255: 41-45.
50. Fiebiger, E., P. Meraner, E. Weber, I. F. Fang, G. Stingl, H. Ploegh, and D. Maurer. 2001. Cytokines regulate proteolysis in major histocompatibility complex class II-dependent antigen presentation by dendritic cells. J. Exp. Med. 193: 881-892.
51. Burster, T., A. Beck, S. Poeschel, A. Øren, D. Baechle, M. Reich, O. Roetzschke, K. Falk, B. O. Boehm, S. Youssef, et al. 2007. Interferon-gamma regulates cathepsin G activity in microglia-derived lysosomes and controls the proteolytic processing of myelin basic protein in vitro. Immunology 121: 82-93.