Cathepsin S activity regulates antigen presentation and immunity

Journal of Clinical Investigation

Volumn 101, Issue 11, 1998, Pages 2351-2363

  Riese, Richard J ^a   Mitchell, Richard N ^a   Villadangos, Jose A ^b   Shi, Guo Ping ^a   Palmer, James T ^c   Karp, Elena R ^a   De Sanctis, George T ^a   Ploegh, Hidde L ^b   Chapman, Harold A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Arris Pharmaceuticals   (United States)

Author keywords

Class II; Histocompatibility; Inhibitor; Ovalbumin; Proteinase

Indexed keywords

CATHEPSIN S; CYSTEINE PROTEINASE INHIBITOR; IMMUNOGLOBULIN E; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; ASTHMA; AUTOIMMUNE DISEASE; CELL INFILTRATION; COMPLEX FORMATION; FEMALE; HYPERSENSITIVITY; IMMUNOREGULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DEGRADATION;

EID: 0032103322     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1158     Document Type: Article

References (59)

1. Cresswell, P. 1994. Antigen presentation. Getting peptides onto MHC class II molecules. Curr. Biol. 4:541-543.
2. Germain, R.N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 76:287-299.
3. Wolf, P.R., and H.L. Ploegh. 1995. How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol. 11:267-306.
4. Roche, P.A., M.S. Marks, and P. Cresswell. 1991. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature. 354:392-394.
5. Lamb, C., and P. Cresswell. 1992. Assembly and transport properties of invariant chain trimers and HLA-DR-invariant chain complexes. J. Immunol. 148:3478-3482.
6. Bijlmakers, M.-J.E., P. Benaroch, and H.L. Ploegh. 1994. Mapping functional regions in the lumenal domain of the class II-associated invariant chain. J. Exp. Med. 180:623-629.
7. Ghosh, P., M. Amaya, E. Mellins, and D.C. Wiley. 1995. The structure of an intermediate in class II maturation: CLIP bound to HLA-DR3. Nature. 378: 457-462.
8. Rudensky, A.Y., P. Preston-Hurlburt, S.C. Hong, A. Barlow, and C.A. Janeway, Jr. 1991. Sequence analysis of peptides bound to MHC class II molecules. Nature. 353:622-627.
9. Riberdy, J.M., J.R. Newcomb, M.J. Surman, J.A. Barbosa, and P. Cresswell. 1992. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature. 360:474-476.
10. Chicz, R.M., R.G. Urban, W.S. Lane, J.C. Gorga, L.J. Stern, D.A.A. Vignali, and J.L. Strominger. 1992. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature. 358:764-768.
11. Amigorena, S., J.R. Drake, P. Webster, and I. Melman. 1994. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature. 349:113-120.
12. Tulp, A., D. Verwoerd, B. Dobberstein, H.L. Ploegh, and J. Peters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature. 349:120-126.
13. West, M.A., J.M. Lucocq, and C. Watts. 1994. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature. 369:147-151.
14. Denzin, L.K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers. Cell. 82:155-165.
15. Sherman, M.A., D.A. Weber, and P.E. Jensen. 1995. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity. 3:197-205.
16. Sloan, V.S., P. Cameron, G. Porter, M. Gammon, M. Amaya, E. Mellins, and D.M. Zaller. 1995. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature. 375:802-806.
17. Roche, P.A., and P. Cresswell. 1990. Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature. 345:615-618.
18. Blum, J.S., and P. Cresswell. 1988. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA. 85:3975-3979.
19. Nguyen, Q., V. Knapp, and R.E. Humphreys. 1988. Inhibition by leupeptin and antipain of the intracellular proteolysis of Ii. Hum. Immunol. 24: 153-163.
20. Newcomb, J.R., and P. Cresswell. 1993. Structural analysis of proteolytic products of MHC class II-invariant chain complexes generated in vivo. J. Immunol. 151:4153-1163.
21. Neefjes, J.J., and H.L. Ploegh. 1992. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistant αβ heterodimers in endosomes. EMBO (Eur. Mol. Biol. Organ.) J. 11:411-116.
22. Reyes, V.E., S. Lu, und R.E. Humphreys. 1991. Cathepsin B cleavage of Ii from MHC α-and β-chains. J. Immunol. 146:3877-3880.
23. Bevec, T., V. Stoka, G. Pungercic, I. Dolenc, and V. Turk. 1996. Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J. Exp. Med. 183:1331-1338.
24. Fineschi, B., K. Sakaguchi, E. Appella, and J. Miller. 1996. The proteolytic environment involved in MHC class II-restricted antigen presentation can be modified by the p41 form of invariant chain. J. Immunol. 157:3211-3215.
25. Van Noort, J.M., and A.C.M. Van der Drift. 1984. The selectivity of cathepsin D suggests an involvement of the enzyme in the generation of T-cell epitopes. J. Biol. Chem. 264:14159-14164.
26. Rodriguez, G.M., and S. Diment. 1992. Role of cathepsin D in antigen presentation of ovalbumin. J. Immunol. 149:2894-2898.
27. Riese, R.J., P.R. Wolf, D. Bromme, L.R. Natkin, J.A. Villadangos, H.L. Ploegh, and H.A. Chapman. 1996. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity. 4:357-366.
28. Villadangos, J.A., R.J. Riese, C. Peters, H.A. Chapman, and H.L. Ploegh. 1997. Degradation of mouse Ii: roles of cathepsins S and D and the influence of allelic polymorphism. J. Exp. Med. 186:549-560.
29. Palmer, J.T., D. Rasnick, J.L. Klaus, and D. Bromme. 1995. Vinyl sulfones as mechanism-based cysteine protease inhibitors. J. Med. Chem. 38:3193-3196.
30. Buus, S., S. Colon, C. Smith, J.H. Freed, C. Miles, and H.M. Grey. 1986. Interaction between a "processed" ovalbumin peptide and Ia molecules. Proc. Natl. Acad. Sci. USA. 83:3968-3971.
31. Shaw, A.C., R.N. Mitchell, Y.K. Weaver, J. Campos-Torres, A.K. Abbas, and P. Leder. 1990. Mutations of immunoglobulin transmembrane and cytoplasmic domains: effects on intracellular signaling and antigen presentation. Cell. 63:381-392.
32. Metlay, J.P., M.D. Witmer-Pack, R. Agger, M.T. Crowley, D. Lawless, and R.M. Steinman. 1990. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 17:1753-1771.
33. Shi, G.-P., A.C. Webb, K.E. Foster, J.H.M. Knoll, C.A. Lemere, J.S. Munger, and H.A. Chapman. 1994. Human cathepsin S: chromosomal localization, gene structure, and tissue distribution. J. Biol. Chem. 269:11530-11536.
34. White, J., M. Blackman, J. Bill, J. Kappler, P. Marrack, and W. Born. 1989. Two better cell lines for making hybridomas expressing specific T cell receptors. J. Immunol. 143:1822-1825.
35. Griffith, J.L. N. Nabavi, Z. Ghogawala, C.G. Chase, M. Rodriguez, D.J. McKean, and L.H. Glimcher. 1988. Structural mutation affecting intracellular transport and cell surface expression of murine class II molecules. J. Exp. Med. 167:541-555.
36. Mason, R.W., D. Wilcox, P. Wikstrom, and E.N. Shaw. 1989. The identification of active forms of cysteine proteinases in Kirsten-virus-transformed mouse fibroblasts by use of specific radiolabeled inhibitor. Biochem. J. 257:125-129.
37. Barnes, K.A., and R.N. Mitchell. 1995. Detection of functional class II-associated antigen: role of a low density endosomal compartment in antigen processing. J. Exp. Med. 181:1715-1727.
38. Karasuyama, H., and F. Melcher. 1988. Establishment of mouse cell clones which constitutively secrete large quantities of interleukin 2, 3, 4, or 5 using modified cDNA expression vectors. Eur. J. Immunol. 18:97-104.
39. Grusby, M.J., H. Auchincloss, Jr., R. Lee, R.S. Johnson, J.P. Spencer, M. Zijlstra, R. Jaenisch, V.E. Papaioannou, and L.H. Glimcher. 1993. Mice lacking major histocompatibility complex class I and class II molecules. Proc. Natl. Acad. Sci. USA. 90:3913-3917.
40. Kung, T.T., H. Jones, G.K. Adams III. S.P. Umland, W. Kreutner, R.W. Egan, R.W. Chapman, and A.S. Watnick. 1994. Characterization of a murine model of allergic pulmonary inflammation. Int. Arch. Allergy Immunol. 105:83-90.
41. Ohkawara, Y., X.-F. Lei, M.R. Stampfli, J.S. Marshall, Z. Xing, and M. Jordana. 1997. Cytokine and eosinophil responses in the lung, peripheral blood and bone marrow compartments in a murine model of allergen-induced airways inflammation. Am. J. Respir. Cell Mol. Biol. 16:510-520.
42. Krinzman, S.J., G.T. De Sanctis, M. Cernadas, D. Mark, Y. Wang, J. Listman, L. Kobzik, C. Donovan, K. Nassr, I. Katona, et al. 1996. Inhibition of T cell costimulation abrogates airway hyperresponsiveness in a murine model. J. Clin. Invest. 98:2693-2699.
43. Bozic, C.R., L.F. Kolakowski, Jr., N.P. Gerard, C. Garcia-Rodriguez, C. von Uexkull-Guldenband, M.J. Conklyn, R. Breslow, H.J. Showell, and C. Gerard. 1995. Expression and biologic characterization of the murine chemokine KC. J. Immunol. 154:6048-6057.
44. Frevert, C.W., S. Huang, H. Danaee, J.D. Paulauskis, and L. Kobzik. 1995. Functional characterization of the rat chemokine KC and its importance in neutrophil recruitment in a rat model of pulmonary inflammation. J. Immunol. 154:335-344.
45. Diment, S. 1990. Different roles for thiol and aspartyl proteases in antigen presentation of ovalbumin. J. Immunol. 145:417-122.
46. Viville, S., J. Neefjes, V. Lotteau, A. Dierich, M. Lemeur, H. Ploegh, C. Benoist, and D. Mathis. 1993. Mice lacking the MHC class II-associated invariant chain. Cell. 72:635-648.
47. Griscelli, C. B. Lisowska-Grospierre, and B. Mach. 1989. Combined immunodeficiency with defective expression in MHC class II genes. Immunodefic. Rev. 1:135-153.
48. Shachar, I., and R.A. Flavell. 1996. Requirement for invariant chain in B cell maturation and function. Science. 274:106-108.
49. Denzin, L.K., C. Hammond, and P. Cresswell. 1996. HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J. Exp. Med. 184:2153-2165.
50. + T helper cell phenotype development in a T cell receptor αβ transgenic model. J. Exp. Med. 182:1579-1584.
51. Pfeiffer, C., J. Stein, S. Southwood, H. Ketelaar, A. Seite, and K. Bottomly. 1995. Altered peptide ligands can control CD4 T lymphocyte differentiation in vivo. J. Exp. Med. 181:1569-1574.
52. Gajewski, T.F., M. Pinas, T. Wong, and F.W. Fitch. 1991. Murine Th1 and Th2 clones proliferate optimally in response to distinct antigen-presenting cell populations. J. Immunol. 146:1750-1758.
53. Mudde, G.C., I.G. Reischl, N. Corvaia, S. Hren, and E.-M. Poellabauer. 1996. Antigen presentation in allergic sensitization. Immunol. Cell Biol. 74:167-173.
54. Beasley, R., W.R. Roche, J. A. Roberts, and S.T. Holgate. 1989. Cellular events in the bronchi in mild asthma and after bronchial provocation. Am. Rev. Respir. Dis. 139:806-817.
55. Venge, P., and L. Hakansson. 1991. Current understanding of the role of the eosinophil granulocyte in asthma. Clin. Exp. Allergy. 21(Suppl. 3):31-37.
56. Woolcock, A.J. 1994. Asthma. In Textbook of Respiratory Medicine. J.F. Murray and J.A. Nadel, editors. W.B. Saunders Co., Philadelphia. 1288-1330.
57. Linsley, P.S., P.M. Wallace, J. Johnson, M.G. Gibson, J.L. Greene, J.A. Ledbetter, C. Singh, and M.A. Tepper. 1992. Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science. 257:789-792.
58. Brachet, V., G. Raposo, S. Amigorena, and I. Mellman. 1997. Ii controls the transport of major histocompatibility class II molecules to and from lysosomes. J. Cell Biol. 137:51-65.
59. Matsunaga, Y., T. Saibara, H. Kido, and N. Katunuma. 1993. Participation of cathepsin B in processing of antigen to MHC class II. FEBS Lett. 324: 325-330.