Distinct intracellular compartments involved in invariant chain degradation and antigenic peptide loading of major histocompatibility complex (MHC) class II molecules

Journal of Cell Biology

Volumn 139, Issue 6, 1997, Pages 1433-1446

  Ferrari, Giorgio ^a   Knight, Andrew M ^b   Watts, Colin ^b   Pieters, Jean ^a  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HLA D ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN PRESENTATION; ARTICLE; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; LYSOSOME; PRIORITY JOURNAL; PROTEIN TRANSPORT;

ANTIBODIES, BACTERIAL; CELL FRACTIONATION; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; HLA-D ANTIGENS; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN LIGHT CHAINS; LYSOSOMES; MELANOMA; ORGANELLES; PEPTIDE FRAGMENTS; RECOMBINANT PROTEINS; TETANUS TOXIN; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0031438151     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.6.1433     Document Type: Article

References (84)

1. Amigorena, S., J.R. Drake, P. Webster, and I. Mellman. 1994. Transient accumulation of new MHC molecules in a novel endocytic compartment in B lymphocytes. Nature. 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. Anderson, M.S., and J. Miller. 1992. Invariant chain can function as a chaperone protein for class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci. USA. 89:2282-2286.
4. 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.
5. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell. 63:707-716.
6. 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.
7. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Busch, R., I. Cloutier, R.-P. Sekaly, and G.J. Hammerling. 1996. Invariant chain protects class II histocompatibility antigens from binding intact polypeptides in the endoplasmic reticulum. EMBO (Eur. Mol. Biol. Organ.) J. 15:418-4-8.
9. 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.
10. Cella, M., A. Engering, V. Pinet, J. Pieters, and A. Lanzavecchia. 1997. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature. 388:782-786.
11. Chen, Q., and P. Hersey. 1992. MHC-restricted responses of CD8+ and CD4+ T-cell clones from regional lymph nodes of melanoma patients. Int. J. Cancer. 51:218-224.
12. Chervonsky, A.V., L. Gordon, and A. Sant. 1994. A segment in the MHC class II β chain plays a critical role in targeting class II molecules to the endocytic pathway. Int. Immunol. 6:973-982.
13. Cho, S., M. Attaya, and J.J. Monaco. 1991. New class II-like genes in the murine MHC. Nature. 353:573-576.
14. Copier, J., M.J. Kleijmeer, S. Ponnambalam, V. Oorschot, P. Potter, J. Trowsdale and A. Kelly. 1996. Targeting signal and subcellular compartments involved in the intracellular trafficking of HLA-DMB. J. Immunol. 157:1017-1027.
15. Cresswell, P. 1994a. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:259-293.
16. Cresswell, P. 1994b. Antigen presentation. Getting peptides into MHC class II molecules. Curr. Biol. 4:541-543.
17. De Duve, C. 1965. The separation and characterization of subcellular particles. Harvey Lect. 59:49-87.
18. Denzin, L.K., and P. Cresswell. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell. 82:155-165.
19. Engering, A., I. Lefkovits, and J. Pieters. 1997. Molecular analysis of organelles involved in MHC class II restricted antigen presentation. Electrophoresis. In press.
20. Germain, R.N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 76:287-299.
21. Germain, R.N., and L.R. Hendrix. 1991. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature. 353:134-139.
22. Germain, R.N., and A.C. Rinker. 1993. Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes surface expression of occupied molecules. Nature. 363:725-728.
23. Ghosh, P., M. Amaya, E. Mellins, and D.C. Wiley. 1995. The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature. 378:457-462.
24. Griffiths, G., and J. Gruenberg. 1991. The arguments for pre-existing early and late endosomes. Trends Cell Biol. 1:5-9.
25. Griffiths, G., B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52: 329-341.
26. Gruenberg, J., G. Griffiths, and K.E. Howell. 1989. Characterization of the early endosomes and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108:1301-1316.
27. Harms, E., H. Kern, and J.A. Schneider. 1980. Human lysosomes can be purified from diploid skin fibroblasts by free-flow electrophoresis. Proc. Natl. Acad. Sci. USA. 77:6139-6143.
28. Hunziker, W., and C. Fumey. 1994. A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:2963-2967.
29. Johnson, J.P., M. Demmer-Dieckmann, T. Meo, M.R. Hadam, and G. Rietmuller. 1981. Surface antigens of human melanoma cells defined by monoclonal antibodies. I. Biochemical characterization of two antigens found on cell lines and fresh tumors of diverse tissue origin. Eur. J. Immunol. 11:825-831.
30. 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. 266:1569-1573.
31. Katz, J.F., C. Stebbins, E. Appella, and A.J. Sant. 1996. Invariant chain and DM edit self-peptide presentation by major histocompatibility complex (MHC) class II molecules. J. Exp. Med. 184:1747-1753.
32. Kelly, A.P., J.J. Monaco, S. Cho, and J. Trowsdale. 1991. A new human HLA class II-related locus, DM. Nature. 353:517-573.
33. Knight, A.M., J.M. Luccocq, A.R. Prescott, S. Ponnambalam, and C. Watts. 1997. Antigen endocytosis and presentation mediated by human membrane IgG1 in the absence of the Igα/Igβ dimer. EMBO (Eur. Mol. Biol. Organ.) J. 16:3842-3850.
34. Koldovsky, O., and M. Palmieri. 1971. Cortisone-evoked decrease of acid β-galactosidase, β-glucuronidase, N-acetyl-β-glucosaminidase and acrylsulphatase in the ileum of sucling rats. Biochem. J. 125:697-701.
35. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
36. Kropshofer, H., A.B. Vogt, G. Moldenhauer, J. Hammer, J.S. Blum, and G.J. Hammerling. 1996. Editing of the HLA-DR-peptide repertoire by HLA-DM. EMBO (Eur. Mol. Biol. Organ.) J. 15:6144-6154.
37. Kropshofer, H., S.O. Arndt, G. Moldenhauer, C.J. Hammerling, and A.B. Vogt. 1997. HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity. 6:293-302.
38. Kvist, S., K. Wiman, L. Claesson, P.A. Peterson, and B. Dobberstein. 1982. Membrane insertion and oligomeric assembly of HLA-DR histocompatibility antigens. Cell. 29:61-69.
39. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
40. Lanzavecchia, A. 1987. Antigen uptake and accumulation in antigen-specific B cells. Immunol. Rev. 99:39-51.
41. Lanzavecchia, A. 1996. Mechanisms of antigen uptake for presentation. Curr. Opin. Immunol. 8:348-354.
42. 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. 348:600-605.
43. Marks, M.S., P.A. Roche, E. van Donselaar, L. Woodruff, P.J. Peters, and J.S. Bonifacino. 1995. A lysosomal targeting signal in the cytoplasmic tail of the beta chain directs HLA-DM to MHC class II compartments. J. Cell Biol. 131:351-369.
44. Marks, M.S., L. Woodruff, H. Ohno, and J.S. Bonifacino. 1996. Protein targeting by tvrosine- and di-leucine-based signals: Evidence for distinct saturable components. J. Cell Biol. 135:341-354.
45. Markwell, M.A. 1982. A new solid-state reagent to iodinate proteins. I. Conditions for the efficient labeling of antiserum. Anal. Biochem. 125:427-432.
46. Marsh, M., S. Schmid, H. Kern, E. Harms, P. Male, I. Mellman, and A. Helenius. 1987. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis. J. Cell Biol. 104:875-886.
47. Mellins, E., L. Smith, B. Arp, T. Cotner, E. Cells, and D. Pious. 1990. Defective-processing and presentation of exogenous antigens in mutants with normal HLA class II genes. Nature. 343:71-74.
48. Mellman, I. 1996. Endocytosis and molecular sorting. Ann. Rev. Cell. Dev. Biol. 12:575-625.
49. Mitchell, R.N., K.A. Barnes, S.A. Grupp, M. Sanchez, Z. Misulovin, M.C. Nussenzweig, and A.K. Abbas. 1995. Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J. Exp. Med. 181: 1705-1714.
50. Murphy, R.F. 1991. Maturation models for endosome and lysosome biogenesis. Trends Cell Biol. 1:77-82.
51. Ohno, H., J. Stewart, M.C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J.S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 269: 1872-1875.
52. Parton, R.G., K. Prydz, M. Bomsel, K. Simons, and G. Griffiths. 1989. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J. Cell Biol. 109:3259-3272.
53. 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. 349:669-676.
54. 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 lymphohlastoid cells are distinct from early endosomes. J. Exp. Med. 182:325-334.
55. 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.
56. Pieters, J. 1997a. MHC class II restricted antigen presentation. Curr. Opin. Immunol. 9:89-96.
57. Pieters, A. 1997a. MHC Class II compartments: specialized organelles of the endocytic pathway in antigen presenting cells. Biol. Chem. 378:751-758.
58. Pieters, J., H. Horstmann, O. Bakke, G. Griffiths, and J. Lipp. 1991. Intracellular transport and localization of Major Histocompatibility Complex class II molecules and associated invariant chain. J. Cell Biol. 115:1213-1223.
59. Pieters, J., O. Bakke, and B. Dobberstein. 1993. The MHC class II-associated Invariant chain contains two endosomal sorting signals within its cytoplasmic tail. J. Cell Sci. 106:831-846.
60. Pinet, V., M. Vergelli, R. Martin, O. Bakke, and E.O. Long. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature. 375:603-606.
61. Pond, L., C. Watts. 1997. Characterization of transport of newly assembled, T cell-stimulatory MHC class II-peptide complexes from MHC class II compartments to the cell surface. J. Immunol. 159:543-553.
62. Qiu, 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.
63. Raposo, G., H.W. Nijman, W. Stoorvogel, R. Leijendekker, C.V. Harding, C.J. Melief, and H.J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183:1161-1172.
64. 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. 360:474-477.
65. Roche, P.A. 1995. HLA-DM: an in vivo facilitator of MHC class II peptide loading. Immunity. 3:259-262.
66. Roche, P.A. 1996. Out, damned CLIP! Out, I say! Science. 274:326-527.
67. 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.
68. 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. 266:1566-1569.
69. Sanderson, F., C. Thomas, J. Neefjes, and J. Trowsdale. 1996. Association between HLA-DM and HLA-DR in vivo. Immunity. 4:87-96.
70. 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.
71. 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.
72. Stebbins, C.C., M.E. Peterson, W.M. Suh, and A.J. Sant. 1996. DM-mediated release of a naturally occurring invariant chain degradation intermediate from MHC class II molecules. J. Immunol. 157:4892-4898.
73. Steinman, R.M., and J. Swanson. 1995. The endocytic activity of dendritic cells. J. Exp. Med. 182:283-288.
74. Stern, L.J., J.H. Brown, T.S. Jardetzky, J.C. Gorga, R.G. Urban, J.L. Strominger, and D.C. Wiley. 1994. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature. 368:215-221.
75. Teyton, L., D. O'Sullivan, P.W. Dickson, V. Lotteau, A. Sette, P. Fink, and P.A. Peterson. 1990. Invariant chain distinguishes between the exogenous and endogenous antigen presentation pathways. Nature. 348:39-44.
76. Tulp, A., D. Verwoerd, and J. Pieters. 1993. Application of an improved density gradient electrophoresis apparatus to the separation of proteins, cells and subcellular organelles. Eletrophoresis. 14:1295-1301.
77. Tulp, A., D. Verwoerd, B. Dobberstein, H.L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature. 369:120-126.
78. van Ham, S.M., U. Gruneberg, G. Malcherek, I. Broker, A. Melms, and J. Trowsdale. 1996. Human histocompatibility leukocyte antigen (HLA)-DM edits peptides presented by HLA-DR according to their ligand binding motifs. J. Exp. Med. 184:2019-2024.
79. Warmerdam, P.A., E.O. Long, and P.A. Roche. 1996. Isoforms of the invariant chain regulate transport of MHC class II molecules to antigen processing compartments. J. Cell Biol. 133:281-291.
80. Watts, C. and H.W. Davidson. 1988. Endocytosis and recycling of specific antigen by human B cell lines. EMBO (Eur. Mol. Biol. Organ.) J. 7:1937-1945.
81. Weber, D.A., B.D. Evavold, and P.E. Jensen. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 274:618-620.
82. 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.
83. 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.
84. Zachgo, S., B. Dobberstein, and G. Griffiths. 1992. A block in degradation of MHC class II-associated invariant chain correlates with a reduction in transport from endosome carrier vesicles to the prelysosomal compartments. J. Cell Sci. 103:811-822.