Early endosomal maturation of MHC class II molecules independently of cysteine proteases and H-2DM

EMBO Journal

Volumn 19, Issue 5, 2000, Pages 882-891

  Villadangos, José A ^b   Driessen, Christoph ^a   Shi, Guo Ping ^a   Chapman, Harold A ^a   Ploegh, Hidde L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Endosomes; Invariant chain; MHC class II

Indexed keywords

CATHEPSIN S; CYSTEINE PROTEINASE; HLA DM ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING;

ANIMALIA;

EID: 0034161292     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.5.882     Document Type: Article

References (49)

1. Amigorena, S., Webster, P., Drake, J., Newcomb, J., Cresswell, P. and Mellman, I. (1995) Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J. Exp. Med., 181, 1729-1741.
2. Avva, R.R. and Cresswell, P. (1994) In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity, 1, 763-774.
3. Barois, N., Forquet, F, and Davoust, J. (1997) Selective modulation of the major histocompatibility complex class II antigen presentation pathway following B cell receptor ligation and protein kinase C activation. J. Biol. Chem., 272, 3641-3647.
4. Benaroch, P., Yilla, M., Raposo, G., Ito, K., Miwa, K., Geuze, H.J. and Ploegh, H.L. (1995) How MHC class II molecules reach the endocytic pathway. EMBO J., 14, 37-49.
5. Bijlmakers, M.J., Benaroch, P. and Ploegh, H.L. (1994) Assembly of HLA DR1 molecules translated in vitro: binding of peptide in the endoplasmic reticulum precludes association with invariant chain. EMBO J., 13, 2699-2707.
6. Bikoff, E.K., Germain, R.N. and Robertson, E.J. (1995) Allelic differences affecting invariant chain dependency of MHC class II subunit assembly. Immunity, 2, 301-310.
7. Brachet, V., Raposo, G., Amigorena, S. and Mellman, I. (1997) Ii chain controls the transport of major histocompatibility complex class II molecules to and from lysosomes. J. Cell Biol., 137, 51-65.
8. Busch, R., Cloutier, I., Sekaly, R.P. and Hammerling, G.J. (1996) Invariant chain protects class II histocompatibility antigens from binding intact polypeptides in the endoplasmic reticulum. EMBO J., 15, 418-428.
9. Castellino, F. and Germain, R.N. (1995) Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity, 2, 73-88.
10. Castellino, F., Zappacosta, F., Coligan, J.E. and Germain, R.N. (1998) Large protein fragments as substrates for endocytic antigen capture by MHC class II molecules. J. Immunol., 161, 4048-4057.
11. Chapman, H.A. (1998) Endosomal proteolysis and MHC class II function. Curr. Opin. Immunol., 10, 93-102.
12. Chicz, R.M., Urban, R.G., Gorga, J.C., Vignali, D.A., Lane, W.S. and Strominger, J.L. (1993) Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med., 178, 27-47.
13. Clague, M.J., Urbe, S., Aniento, F. and Gruenberg, J. (1994) Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem., 269, 21-24.
14. Cresswell, P. (1994) Assembly, transport and function of MHC class II molecules. Annu. Rev. Immunol., 12, 259-293.
15. Denzin, L.K., Hammond, C. and Cresswell, P. (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.
16. Denzin, L.K., Sant'Angelo, D.B., Hammond, C., Surman, M.J. and Cresswell, P. (1997) Negative regulation by HLA-DO of MHC class II-restricted antigen processing. Science, 278, 106-109.
17. 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, 4516-4521.
18. Driessen, C., Bryant, R.A., Lennon-Dumenil, A.M., Villadangos, J.A., Bryant, P.W., Shi, G.P., Chapman, H.A. and Ploegh, H.L. (1999) Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J. Cell Biol., 147, 775-790.
19. Fung-Leung, W.P., Surh, C.D., Liljedahl, M., Pang, J., Leturcq, D., Peterson, P.A., Webb, S.R. and Karlsson, L. (1996) Antigen presentation and T cell development in H2-M-deficient mice. Science, 271, 1278-1281.
20. Geuze, H.J. (1998) The role of endosomes and lysosomes in MHC class II functioning. Immunol. Today, 19, 282-287.
21. Ghosh, P., Amaya, M., Mellins, E. and Wiley, D.C. (1995) The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature, 378, 457-462.
22. Kasai, M., Hirokawa, K., Kajino, K., Ogasawara, K., Tatsumi, M., Hermel, E., Monaco, J.J. and Mizuochi, T. (1996) Difference in antigen presentation pathways between cortical and medullary thymic epithelial cells. Eur. J. Immunol., 26, 2101-2107.
23. Kropshofer, H., Vogt, A.B., Stern, L.J. and Hammerling, G.J. (1995) Self-release of CLIP in peptide loading of HLA-DR molecules. Science, 270, 1357-1359.
24. Kropshofer, H., Vogt, A.B., Thery, C., Armandola, E.A., Li, B.C., Moldenhauer, G., Amigorena, S. and Hammerling, G.J. (1998) A role for HLA-DO as a co-chaperone of HLA-DM in peptide loading of MHC class II molecules. EMBO J., 17, 2971-2981.
25. Lindner, R. and Unanue, E.R. (1996) Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J., 15, 6910-6920.
26. Martin, W.D., Hicks, G.G., Mendiratta, S.K., Leva, H.I., Ruley, H.E. and Van Kaer, L. (1996) H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation and T cell repertoire selection. Cell, 84, 543-550.
27. Metlay, J.P., Witmer-Pack, M.D., Agger, R., Crowley, M.T., Lawless, D. and Steinman, R.M. (1990) The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med., 171, 1753-1771.
28. Miyazaki, T., Wolf, P., Tourne, S., Waltzinger, C., Dierich, A., Barois, N., Ploegh, H., Benoist, C. and Mathis, D. (1996) Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. Cell, 84, 531-541.
29. Nakagawa, T. et al. (1998) Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science, 280, 450-453.
30. Nakagawa, T.Y. et al. (1999) Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity, 10, 207-217.
31. Pierre, P. and Mellman, I. (1998a) Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell, 93, 1135-1145.
32. Pierre, P and Mellman, J. (1998b) Exploring the mechanisms of antigen processing by cell fractionation. Curr. Opin. Immunol., 10, 145-153.
33. Riese, R.J., Wolf, P.R., Bromme, D., Natkin, L.R., Villadangos, J.A., Ploegh, H.L. and Chapman, H.A. (1996) Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity, 4, 357-366.
34. Riese, R.J., Mitchell, R.N., Villadangos, J.A., Shi, G.P., Palmer, J.T., Karp, E.R., De Sanctis, G.T., Ploegh, H.L. and Chapman, H.A. (1998) Cathepsin S activity regulates antigen presentation and immunity. J. Clin. Invest., 101, 2351-2363.
35. Romagnoli, P. and Germain, R.N. (1994) The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport and peptide occupancy. J. Exp. Med., 180, 1107-1113.
36. Rudensky, A., Rath, S., Preston-Hurlburt, P., Murphy, D.B. and Janeway, C.A., Jr (1991) On the complexity of self. Nature, 353, 660-662.
37. Sadegh-Nasseri, S., Stern, L.J., Wiley, D.C. and Germain, R.N. (1994) MHC class II function preserved by low-affinity peptide interactions preceding stable binding. Nature, 370, 647-650.
38. Sanderson, F., Thomas, C., Neefjes, J. and Trowsdale, J. (1996) Association between HLA-DM and HLA-DR in vivo. Immunity, 4, 87-96.
39. Sant, A.J., Hendrix, L.R., Coligan, J.E., Maloy, W.L. and Germain, R.N. (1991) Defective intracellular transport as a common mechanism limiting expression of inappropriately paired class II major histocompatibility complex α/β chains. J. Exp. Med., 174, 799-808.
40. Shi, G.P., Villadangos, J.A., Dranoff, G., Small, C., Gu, L., Haley, K.J., Riese, R., Ploegh, H.L. and Chapman, H.A. (1999) Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity, 10, 197-206.
41. Stebbins, C.C., Loss, G.E., Jr, Elias, C.G., Chervonsky, A. and Sant, A.J. (1995) The requirement for DM in class II-restricted antigen presentation and SDS-stable dimer formation is allele and species dependent. J. Exp. Med., 181, 223-234.
42. van Ham, S.M. et al. (1997) HLA-DO is a negative modulator of HLA-DM-mediated MHC class II peptide loading. Curr. Biol., 7, 950-957.
43. van Weert, A.W., Dunn, K.W., Gueze, H.J., Maxfield, F.R. and Stoorvogel, W. (1995) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol., 130, 821-834.
44. Villadangos, J.A., Riese, R.J., Peters, C., Chapman, H.A. and Ploegh, H.L. (1997) Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med., 186, 549-560.
45. Vogt, A.B. and Kropshofer, H. (1999) HLA-DM - an endosomal and lysosomal chaperone for the immune system. Trends Biochem. Sci., 24, 150-154.
46. Watts, C. (1997) Capture and processing of exogenous antigens for presentation on MHC molecules. Annu. Rev. Immunol., 15, 821-850.
47. Wolf, P.R. and Ploegh, H.L. (1995) How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol., 11, 267-306.
48. Yilla, M., Tan, A., Ito, K., Miwa, K. and Ploegh, H.L. (1993) Involvement of the vacuolar H (+)-ATPases in the secretory pathway of HepG2 cells. J. Biol. Chem., 268, 19092-19100.
49. Zhong, G., Castellino, F., Romagnoli, P. and Germain, R.N. (1996) Evidence that binding site occupancy is necessary and sufficient for effective major histocompatibility complex (MHC) class II transport through the secretory pathway redefines the primary function of class II-associated invariant chain peptides (CLIP). J. Exp. Med., 184, 2061-2066.