Ii chain controls the transport of major histocompatibility complex class II molecules to and from lysosomes

Journal of Cell Biology

Volumn 137, Issue 1, 1997, Pages 51-65

  Brachet, Valérie ^a   Raposo, Graça ^a   Amigorena, Sebastian ^a,c   Mellman, Ira ^b  

^a CNRS   (France)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CULTURE; CELL SURFACE; ENDOSOME; IMMUNOELECTRON MICROSCOPY; IMMUNOPRECIPITATION; LYSOSOME; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ANIMALS; ANTIGENS, SURFACE; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL MEMBRANE; DIMERIZATION; ELECTROPHORESIS; HISTOCOMPATIBILITY ANTIGENS CLASS II; LEUPEPTINS; LYMPHOMA; LYSOSOMES; MICE; MICROSCOPY, IMMUNOELECTRON; PROTEIN STRUCTURE, TERTIARY; TUMOR CELLS, CULTURED;

EID: 0030985764     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.1.51     Document Type: Article

References (57)

1. Amigorena, S., J.R. Drake, P. Webster, and I. Mellman 1994. Transient accumulation of new class II molecules in a novel endocytic compartment in B lymphocytes. Nature (Lond.). 369:113-120.
2. Amigorena, S., P. Webster, J. Drake, J. Newcomb, P. Cresswell, and I. Mellman. 1995. Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J. Exp. Med. 181:1729-1741.
3. Arneson, L.S., and J. Miller. 1995. Efficient endosomal localization of major histocompatibility complex class II-invariant chain complexes requires multimerization of the invariant chain targeting sequence. J. Cell Biol. 129:1217-1228.
4. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell. 63:707-716.
5. 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.
6. Benaroch, P., M. Yilla, G. Raposo, K. Ito, K. Miwa, H.J. Geuze, and H.L. Ploegh. 1995. How MHC class II molecules reach the endocytic pathway. EMBO (Eur. Mol. Biol. Organ.) J. 14:37-49.
7. Bhattacharya, A., M.E. Dorf, and T.A. Springer. 1981. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J. Immunol. 127:2488-2495.
8. 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.
9. Bonnerot, C., D. Lankar, D. Hanau, D. Spehner, J. Davoust, J. Salamero, and W.H. Fridman. 1995. Role of B cell receptor Ig α and Ig β subunits in MHC class II-restricted antigen presentation. Immunity. 3:335-347.
10. Braunstein, N.S., R.N. Germain, K. Loney, and N. Berkowitz. 1990. Structurally interdependent and independent regions of allelic polymorphism in class II MHC molecules. J. Immunol. 145:1635-1645.
11. Castellino, F., and R.N. Germain. 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.
12. Cresswell, P. 1992. Chemistry and functional role of the invariant chain. Curr. Opin. Immunol. 4:87-92.
13. Cresswell, P. 1994. Antigen presentation. Getting peptides into MHC class II molecules. Curr. Biol. 4:541-543.
14. Cresswell, P. 1996. Invariant chain structure and MHC class II function. Cell. 84:505-507.
15. 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.
16. Denzin, L.K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell. 82:155-165.
17. Germain, R.N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 76:287-299.
18. Germain, R.N., and L.H. Hendrix. 1991. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature (Lond.). 353:134-139.
19. Granger, B.L., S.A. Green, C.A. Gabel, C.L. Howe, I. Mellman, and A. Helenius. 1990. Characterization and cloning of Igp110, a lysosomal membrane glycoprotein from mouse and rat cells. J. Biol. Chem. 265:12036-12043.
20. Janeway, C.A., Jr., P.J. Conrad, E.A. Lerner, J. Babich, P. Wettstein, and D.B. Murphy. 1984. Monoclonal antibodies specific for Ia glycoproteins raised by immunization with activated T cells: possible role of T cell-bound Ia antigens as targets of immunoregulatory T cells. J. Immunol. 132:662-667.
21. Karlsson, L., A. Peleraux, R. Lindstedt, M. Liljedahl, and P.A. Peterson. 1994. Reconstitution of an operational MHC class II compartment in nonantigen-presenting cells. Science (Wash. DC). 266:1569-1573.
22. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
23. Kleijmeer, M.J., G. Raposo, and J.G. Geuze. 1996. Characterization of MHC class II compartments by immunoelectron microscopy. Methods (Orlando). 10:191-207.
24. Liou, W., H.J. Geuze, and J.W. Slot. 1994. Improving structural integrity of cryo-sections for immunogold labeling. Histochem. Cell Biol. 106:41-58.
25. Lotteau, V., L. Teyton, A. Peleraux, T. Nilsson, L. Karlsson, S.L. Schmid, V. Quaranta, and P.A. Peterson. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature (Lond.). 348:600-605.
26. Marie, M.A., M.D. Taylor, and J.S. Blum. 1994. Endosomal aspartic proteinases are required for invariant-chain processing. Proc. Natl. Acad. Sci. USA. 91: 2171-2175.
27. Mellins, E., P. Cameron, M. Amaya, S. Goodman, D. Pious, L. Smith, and B. Arp. 1994. A mutant human histocompatibility leukocyte antigen DR molecule associated with invariant chain peptides. J. Exp. Med. 179:541-549.
28. Mellman, I. 1997. Endocytosis and molecular sorting. Ann. Rev. Cell. Biol. In press.
29. Mellman, I., P. Pierre, and S. Amigorena. 1995. Lonely MHC class II molecules seeking immunogenic peptides for meaningful relationships. Curr. Opin. Cell Biol. 7:564-572.
30. Miyazaki, T., P. Wolf, S. Tourne, A. Dierich, N. Barois, H. Ploegh, C. Benoist, and D. Mathis. 1996. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. Cell. 84:531-541.
31. Morton, P.A., M.L. Zacheis, K.S. Giacoletto, J.A. Manning, and B.D. Schwartz. 1995. Delivery of nascent MHC class II-invariant chain complexes to lysosomal compartments and proteolysis of invariant chain by cysteine proteases precedes peptide binding in B-lymphoblastoid cells. J. Immunol. 154:137-150.
32. 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. 11:411-416.
33. Neefjes, J.J., V. Stollorz, P.J. Peters, H.J. Geuze, and H.L. Ploegh. 1990. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell. 61:171-183.
34. Newcomb, J.R., and P. Cresswell. 1993. Structural analysis of proteolytic products of MHC class II-invariant chain complexes generated in vivo. J. Immunol. 151:4153-4163.
35. Nijenhuis, M., J. Calafat, K.C. Kuijpers, H. Janssen, M. de Haas, T.W. Nordeng, O. Bakke, and J.J. Neefjes. 1994. Targeting major histocompatibility complex class II molecules to the cell surface by invariant chain allows antigen presentation upon recycling. Eur. J. Immunol. 24:873-883.
36. Odorizzi, C.G., I.S. Trowbridge, L. Xue, C.R. Hopkins, C.D. Davis, and J.F. Collawn. 1994. Sorting signals in the MHC class II invariant chain cytoplasmic region determine trafficking to an endocytic processing compartment. J. Cell Biol. 126:317-330.
37. Peters, P.J., J.J. Neefjes, V. Oorschot, H.L. Ploegh, and H.J. Geuze. 1991. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature (Lond.). 349:669-676.
38. Peters, P.J., G. Raposo, J.J. Neefjes, V. Oorschot, R.L. Leijendekker, H.J. Geuze, and H.L. Ploegh. 1995. Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J. Exp. Med. 182:325-334.
39. Peterson, M., and J. Miller. 1990. Invariant chain influences the immunological recognition of MHC class II molecules. Nature (Lond.). 345:172-174.
40. Pierre, P., L.K. Denzin, C. Hammond, J.R. Drake, S. Amigorena, P. Cresswell, and I. Mellman. 1996. HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity. 4:229-239.
41. Pieters, J., O. Bakke, and B. Dobberstein. 1993. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 106:831-846.
42. Oiu, Y., X. Xu, A. Wandinger-Ness, D.P. Dalke, and S.K. Pierce. 1994. Separation of subcellular compartments containing distinct functional forms of MHC class II. J. Cell Biol. 125:595-605.
43. Raposo, G., H.W. Nijman, W. Stoorvogel, R. Leijendekker, C.V. Harding, C.J.M. Melief, and H.J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183:1161-1172.
44. 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 (Lond.). 360:474-177.
45. Riese, R.G., P.R. Wolf, D. Bromme, L.R. Nathin, J.A. Villadangos, H.L. Ploegh, and H.A. Chapman. 1996. Essential role for calhepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity. 4:357-366.
46. Roche, P.A. 1995. HLA-DM: an in vivo facilitator of MHC class II peptide loading. Immunity. 3:259-262.
47. Roche, P.A., and P. Cresswell. 1991. Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA. 88:3150-3154.
48. 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 (Lond.). 354:392-394.
49. Roche, P.A., C.L. Teletski, E. Stang, O. Bakke, and E.O. Long. 1993. Cell surface HLA-DR-invariant chain complexes are targeted to endosomes by rapid internalization. Proc. Natl. Acad. Sci. USA. 90:8581-8585.
50. Rudensky, A. Y., M. Maric, S. Eastman, L. Shoemaker, P.C. DeRoos, and J.S. Blum. 1994. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity. 1:585-594.
51. Sanderson, F., M.J. Kleijmeer, A. Kelly, D. Verwoerd, A. Tulp, J.J. Neefjes, H.J. Geuze, and J. Trowsdale. 1994. Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science (Wash. DC). 266:1566-1569.
52. Sette, A., S. Southwood, J. Miller, and E. Appella. 1995. Binding of major histocompatibilily complex class II to the invariant chain-derived peptide, CLIP, is regulated by allelic polymorphism in class II. J. Exp. Med. 181:677-683.
53. 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 (Lond). 375:802-806.
54. Tulp, A., D. Verwoerd, B. Dobberstein, H.L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature (Lond.). 369:120-126.
55. 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 (Lond.). 369:147-151.
56. 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.
57. Wubbolts, R., M. Fernandez-Borja, L. Oomen, D. Verwoerd, H. Janssen, J. Calat, A. Tulp, S. Duseljee, and J. Neefjes. 1996. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135:611-622.