Early endosomes are required for major histocompatibility complex class II transport to peptide-loading compartments

Molecular Biology of the Cell

Volumn 10, Issue 9, 1999, Pages 2891-2904

  Brachet, Valérie ^a   Péhau Arnaudet, Gérard ^b   Desaymard, Catherine ^b   Raposo, Graça ^b   Amigorena, Sebastian ^a  

^a INSERM   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; DIAMINOBENZIDINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CELL MEMBRANE; CELL SURFACE; CELL VACUOLE; CELLULAR DISTRIBUTION; CROSS LINKING; ENDOSOME; GOLGI COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; T LYMPHOCYTE;

ANIMALIA;

EID: 0344993904     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.9.2891     Document Type: Article

References (51)

1. Amigorena, S., Bonnerot, C., Drake, J., Choquet, D., Hunziker, W., Guillet, J., Webster, P., Sautes, C., Mellman, I., and Fridman, W. (1992). Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 256, 1808-1812.
2. Amigorena, S., Drake, J.R., Webster, P., and Mellman, I. (1994). Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369, 113-120.
3. Bénaroch, P.J., Yilla, M., Raposo, M.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.
4. Brachet, V., Raposo, G., Amigorena, S., and Mellman, I. (1997). Invariant chain controls the transport of MHC class II molecules to and from lysosomes. J. Cell Biol. 137, 51-65.
5. 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.
6. Choquet, D., Ku, G., Cassard, S., Malissen, B., Korn, H., Fridman, W., and Bonnerot, C. (1994). Different patterns of calcium signaling triggered through two components of the B lymphocyte antigen receptor. J. Biol. Chem. 269, 6491-6497.
7. Cresswell, P. (1985). Intracellular class II HLA antigens are accessible to transferrin-neuraminidase conjugates internalized by receptor-mediates endocytosis. Proc. Natl. Acad Sci. USA 82, 8188-8192.
8. Cresswell, P. (1994). Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 22, 259-293.
9. Cresswell, P. (1996). Invariant chain structure and MHC class II function. Cell 84, 505-507.
10. Denzin, L.K., and Cresswell, P. (1995). HLA-DM induces CLIP dissociation from MHC class II alpha/beta dimers and facilitates peptide loading. Cell 82, 155-165.
11. Denzin, L.K., Robbins, N.F., Carboy-Newcomb, C., and Cresswell, P. (1994). Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1, 595-606.
12. Eastman, S., Deftos, M., DeRoos, P., Hsu, D., Teyton, L., Braunstein, N., Hackett, C., and Rudensky, A. (1996). A study of complexes of class II invariant chain peptide: major histocompatibility complex class II molecules using a complex-specific monoclonal antibody. Eur. J. Immunol. 26, 385-393.
13. Fling, S.P., Arp, B., and Pious, D. (1994). HLA-DMA and-DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells. Nature 368, 554-558.
14. Futter, C.E., Pearse, A., Hewlett, L.J., and Hopkins, C. (1996). Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132, 1011-1023.
15. Germain, R.N. (1994). MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76, 287-299.
16. Germain, R.N., and Hendrix, L.R. (1991). MHC class II structure, occupancy and surface expression determined by postendoplasmic reticulum antigen binding. Nature 353, 134-139.
17. Glickman, J.N., Morton, P.A., Slot, J.W., Kornfeld, S., and Geuze, H.J. (1996). The biogenesis of MHC class II compartment in human I-cell disease B lymphoblasts. J. Cell Biol. 232, 769-785.
18. Gruenberg, J., and Maxfield, F. (1995). Membrane transport in the endocytic pathway. Curr. Biol. 7, 552-563.
19. Guy, K., Van Heyningen, V., Cohen, B.B., Deane, D.L., and Steel, C.M. (1982). Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to Ia alpha and beta chains. Eur. J. Immunol. 22, 942-948.
20. Hopkins, C.R., Gibson, A., Shipman, M., and Miller, K. (1990). Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 346, 318-319.
21. Janeway, C.A., Jr., Conrad, P.J., Lerner, E.A., Babich, J., Wettstein, P., and Murphy, D.B. (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.
22. Kleijmeer, M.J., Morkowski, S., Griffith, J.M., Rudensky, A.Y., and Geuze, H.J. (1997). Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J. Cell Biol. 339, 639-649.
23. Kropshofer, H., Hammerling, G.J., and Vogt, A.B. (1997). How HLA-DM edits the MHC class II peptide repertoire: survival of the fittest? Immunol. Today 18, 77-82.
24. Liu, S., Marks, M.S., and Brodsky, F. (1998). A dominant-negative clathrin mutant differentially affects trafficking of molecules with distinct sorting motifs in the class II major histocompatibility complex (MHC) pathway. J. Cell Biol. 140, 1023-1037.
25. Mallard, P., Antony, C., Tenza, D., Salamero, J., Goud, B., and Johannes, L. (1999). Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport J. Cell Biol. 143, 973-990.
26. Marsh, M., Griffiths, G., Dean, G.E., Mellman, I., and Helenius, A. (1986). Three-dimensional structure of endosomes in BHK-21 cells. Proc. Natl. Acad. Sci. USA 83, 2899-2903.
27. Mellman, I., and Plutner, H. (1984). Internalization and degradation of macrophage Fc receptors bound to polyvalent immune complexes. J. Cell Biol. 98, 1170-1177.
28. Morton, P.A., Zacheis, M.L., Giacoletto, K.S., Manning, J.A., and Schwartz, B.D. (1995). Delivery of nascent MHC class II-invariant chain by cystein proteases precedes peptide binding in B-lymphoblastoid cells. J. Immunol. 154, 137-150.
29. Neefjes, J.J., Stollorz, V., Peters, P.J., Geuze, H.J., and Ploegh, H.L. (1990). The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 63, 171-183.
30. Odorizzi, G., Cowles, C., and Emr, S. (1998). The AP-3 complex: a coat of many colors. Trends Cell Biol. 8, 282-288.
31. Peters, P., Raposo, G., Neefjes, J.J., Oorschot, V., Leijendekker, R.L., Geuze, H.J., and Ploegh, H.L. (1995). Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J. Exp. Med. 182, 325-334.
32. Peters, P.J., Neefjes, J.J., Oorschot, V., Ploegh, H.L., and Geuze, H.J. (1991). Segregation of MHC class II molecules from class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 349, 669-676.
33. Pierre, P., Denzin, L.K., Hammond, C., Drake, J.R., Amigorena, P., Cresswell, P., and Mellman, I. (1996). HLA-DM is localized to conventional and unconventional MHC class II-containing compartments. Immunity 4, 229-239.
34. Pierre, P., Turley, S.J., Gatti, E., Hull, M., Meltzer, J., Mirza, A., Inaba, K., Steinman, R.M., and Mellman, I. (1997). Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388, 787-792.
35. Pieters, J., Horstmann, H., Bakke, O., Griffiths, G., and Lipp, J. (1991). Intracellular transport and localization of major histocompatibility complex class II molecules and associated invariant chain. J. Cell Biol. 335, 1213-1223.
36. Pond, L., and Watts, C. (1997). Characterization of transport of newly assembled T cell-stimulatory MHC class II-peptide complexes form MHC class II compartments to the cell surface. J. Immunol. 159, 543-553.
37. Raposo, G., Kleijmeer, M.J., Posthuma, G., Slot, J.W., and Geuze, H.J. (1997). Immunogold labeling of ultrathin cryosections: application in immunology. In: Handbook of Experimental Immunology, 5th ed., ed. I. Blackwell, Cambridge, MA: Elsevier, 1-11.
38. Robinson, M.S. (1997). Coats and vesicle budding. Trends Cell Biol. 7, 99-102.
39. Roche, P. (1995). HLA-DM an in vivo facilitator of MHC class II peptide loading. Immunity 3, 259-262.
40. Roche, P., Teletski, C., Stang, E., Bakke, O., and Long, E. (1993). Cell surface HLA-DR-invariant chain complexes are targeted to endosomes by rapid internalization. Proc. Natl. Acad. Sci. USA 90, 8581-8585.
41. Rodionov, D.G., and Bakke, O. (1998). Medium chains of adaptor complexes AP-1 and AP-2 recognize Leucine-based sorting signals from the invariant chain. J. Biol. Chem. 273, 6005-6008.
42. Romagnoli, P., Layet, C., Yewdell, J., Bakke, O., and Germain, R.N. (1993). Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177, 583-596.
43. Salamero, J., Le Borgne, R., Saudrais, C., Goud, B., and Hoflack, B. (1996). Expression of major histocompatibility complex class II molecules in Hela cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes. J. Biol. Chem. 271, 30318-30321.
44. Saudrais, C., Spehner, D., de la Salle, H., Bohbot, A., Cazenave, J.P., Goud, B., and Salamero, J. (1998). Intracellular pathway for the generation of functional MHC class II peptide complexes in immature human dendritic cells. J. Immunol. 160, 2597-2607.
45. Shackelford, D., Lampson, L., and Strominger, J. (1981). Analysis of HLA antigens by using monoclonal antibodies: recognition of conformational difference in biosynthetic intermediates. J. Immunol. 127, 1403-1410.
46. Théry, C., Brachet, V., Regnault, A., Rescigno, M., Ricardi-Castagnoli, P., Bonnerot, C., and Amigorena, S. (1998). MHC class II transport from lysosomal compartments to the cell surface is determined by stable peptide binding but not by the cytosolic domains of the alpha- and beta-chains. J. Immunol. 161, 2106-2113.
47. Tulp, A., Verwoerd, D., Dobberstein, B., Ploegh, H.L., and Pieters, J. (1994). Isolation and characterization of the intracellular MHC class II compartment. Nature 369, 120-126.
48. Unkeless, J.C. (1979). Characterization of monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 150, 580-596.
49. Warmerdam, P.A.M., Long, E.O., and Roche, P.A. (1996). Isoforms of the invariant chain regulate transport of MHC class II molecules to antigen processing compartments. J. Cell Biol. 333, 281-291.
50. Watts, C. (1997). Capture and processing of exogenous antigens for presentation on MHC molecules. Annu. Rev. Immunol. 15, 821-850.
51. West, M.A., Lucocq, J.M., and Watts, C. (1994). Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature 369, 147-151.