MHC class II compartments: Specialized organelles of the endocytic pathway in antigen presenting cells

Biological Chemistry

Volumn 378, Issue 8, 1997, Pages 751-758

  Pieters, Jean ^a  

^a BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

Author keywords

Antigen presentation; Endocytic pathway; MHC class II molecules; Subcellular organelles

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE FRAGMENT; T LYMPHOCYTE RECEPTOR;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELL ORGANELLE; CELL SURFACE; CELL TYPE; ENDOCYTOSIS; ENDOSOME; HELPER CELL; HUMAN; IMMUNE RESPONSE; LYSOSOME; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; ENDOCYTOSIS; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; ORGANELLES;

EID: 0030862819     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. Amigorena, S., Drake, J.R., Webster, P., and Mellman, I. (1994). Transient accumulation of new MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369, 113-120.
2. Arunachalam, B., and Cresswell, P. (1995). Molecular requirements for the interaction of class II major histocompatibility complex molecules and invariant chain with calnexin. J. Biol. Chem. 270, 2784-2790.
3. Bakke, O., and Dobberstein, B. (1990). MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63, 707-716.
4. Bevec, T., Stoka, V., Pungercic, G., Dolenc, I., and Turk, V. (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.
5. Blum, J.S., and Cresswell, P. (1988). Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA 85, 3975-3979.
6. Boon, T., and van der Bruggen, P. (1996). Human tumor antigens recognized by T lymphocytes. J. Exp. Med. 183, 725-729.
7. Cella, M., Engering, A., Pinet, V., Pieters, J., Lanzavecchia, A. (1997a). Accumulation of long-lived peptide MHC class II complexes induced in dendritic cells by inflammatory stimuli. Nature, in press.
8. Cella, M., Sallusto, F., and Lanzavecchia, A. (1997b). Origin, maturation and antigen presenting function of dendritic cells. Curr. Opin. Immunol. 9, 10-16.
9. Chang, C.H., and Flavell, R.A. (1995). Class II transactivator regulates the expression of multiple genes involved in antigen presentation. J. Exp. Med. 181, 765-767.
10. Clift, O.G.L., Linstedt, A.D., Lowe, A.W., Grote, E., and Kelly, R.B. (1990). Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J. Cell Biol. 110, 1693-1703.
11. Cresswell, P. (1985). Intracellular class II HLA antigens are accessible to transferrin-neuraminidase conjugates internalized by receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA 82, 8188-8192.
12. Cresswell, P. (1996). Invariant chain structure and MHC class II function. Cell 84, 505-507.
13. Cresswell, P., Blum, J.S., Kelner, D.N., and Marks, M.S. (1987). Biosynthesis and processing of class II histocompatibility antigens. Crit. Rev. Immunol. 7, 31-53.
14. Davidson, H.W., Reid, P.A., Lanzavecchia, A., and Watts, C. (1991). Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell 67, 105-116.
15. De Camilli, P. (1995). The eighth Datta Lecture. Molecular mechanisms in synaptic vesicle recycling. FEBS Lett. 369, 3-12.
16. 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.
17. 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.
18. Deverson, E.V., Gow, I.R., Coadwell, W.J., Monaco, J.J., Butcher, G.W., and Howard, J. C. (1990). MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters. Nature 348, 738-741.
19. Dobberstein, B., Garoff, H., Warren, G., and Robinson, P.J. (1979). Cell-free synthesis and membrane insertion of mouse H-2Dd histocompatibility antigen and beta2-microglobulin. Cell 17, 759-769.
20. Engering, A.J., Cella, M., Fluitsma, D.M., Hoefsmit, E.C.M., Lanzavecchia, A., and Pieters, J. (1997). The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol., in press.
21. 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.
22. Germain, R.N. (1994). MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76, 287-299.
23. Griffiths, G.M. (1995). The cell biology of CTL killing. Curr. Opin Immunol. 7, 343-348.
24. Griffiths, G.M. (1996). Secretory lysosomes - A special mechanism of regulated secretion in haemopoietic cells. Tr. Cell Biol. 6, 329-332.
25. Griffiths, G.M., and Argon, Y. (1995). Structure and biogenesis of lytic granules. Curr. Top. Microbiol. Immunol. 198, 39-58.
26. Griffiths, G.M., and Isaaz, S. (1993). Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120, 885-896.
27. Hansen, T.H., Carreno, B.M., and Sachs, D.H. (1993). The major histocompartibility complex. In: Fundamental Immunology, W. E. Paul, ed. (New York: Raven Press, Ltd.), pp. 577-628.
28. Herman, G.A., Bonzelius, F., Cieutat, A.M., and Kelly, R.B. (1994). A distinct class of intracellular storage vesicles, identified by expression of the glucose transporter GLUT4. Proc. Natl. Acad. Sci. USA 91, 12750-12754.
29. Hudson, A.W., Fingar, D.C., Seidner, G.A., Griffiths, G., Burke, B., and Birnbaum, M.J. (1993). Targeting of the "insulin-responsive" glucose transporter (GLUT4) to the regulated secretory pathway in PC12 cells. J. Cell Biol. 122, 579-588.
30. Hurtley, S.M., and Helenius, A. (1989). Protein oligomerization in the endoplasmic reticulum. Ann. Rev. Cell Biol. 5, 277-307.
31. Isaaz, S., Baetz, K., Olsen, K., Podack, E., and Griffiths, G.M. (1995). Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway. Eur. J. Immunol. 25, 1071-1079.
32. Jackson, M.R., and Peterson, P.A. (1993). Assembly and intracellular transport of MHC class I molecules. Annu. Rev. Cell Biol. 9, 207-235.
33. James, D.E., and Piper, R.C. (1994). Insulin resistance, diabetes, and the insulin-regulated trafficking of GLUT-4. J. Cell Biol. 126, 1123-1126.
34. Johnson, J.P., Demmer-Dieckmann, M., Meo, T., Hadam, M.R., and Rietmuller, G. (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.
35. Jones, P.P., Murphy, D.B., Hewgill, D., and McDevitt, M.O. (1978). Detection of a common polypeptide chain in I-A and I-E subregion immunoprecipitates. Immunocytochemistry 16, 51-60.
36. Kagi, D., Ledermann, B., Burki, K., Zinkernagel, R.M., and Hengartner, H. (1996). Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14, 207-232.
37. Kelly, R.B. (1993). A question of endosomes. Nature 364, 487-488.
38. Kern, I., Steimle, V., Siegrist, C.A., and Mach, B. (1995). The two novel MHC class II transactivators RFX5 and CIITA both control expression of HLA-DM genes. Int. Immunol. 7, 1295-1299.
39. Koopmann, J.O., Hammerling, G.J., and Momburg, F. (1997). Generation, intracellular transport and loading of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 9, 80-88.
40. Kvist, S., Wiman, K., Claesson, L., Peterson, P.A., and Dobberstein, B. (1982). Membrane insertion and oligomeric assembly of HLA-DR histocompatibility antigens. Cell 29, 61-69.
41. Lindstedt, R., Liljedahl, M., Peleraux, A., Peterson, P.A., and Karlsson, L. (1995). The MHC class II molecule H2-M is targeted to an endosomal compartment by a tyrosine-based targeting motif. Immunity 3, 561-572.
42. Lotteau, V., Teyton, L., Peleraux, A., Nilsson, T., Karlsson, L., Schmid, S.L., Quaranta, V., and Peterson, P.A. (1990). Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348, 600-605.
43. Marks, M.S., Germain, R.N., and Bonifacino, J.S. (1995). Transient aggregation of major histocompatibility complex class II chains during assembly in normal spleen cells. J. Biol. Chem. 270, 10475-10481.
44. Marks, M.S., Roche, P.A., van Donselaar, E., Woodruff, L., Peters, P.J., and Bonifacino, J.S. (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.
45. Marks, M.S., Woodruff, L., Ohno, H., and Bonifacino, J.S. (1996). Protein targeting by tyrosine- and di-leucine-based signals: Evidence for distinct saturable components. J. Cell Biol. 135, 341-354.
46. Martin, W.D., Hicks, G.G., Mendiratta, S.K., Leva, H.I., Ruley, H.E., and Vankaer, 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.
47. Maycox, P.R., Link, E., Reetz, A., Morris, S.A., and Jahn, R. (1992). Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118, 1379-1388.
48. Mellins, E., Smith, L., Arp, B., Cotner, T., Celis, E., and Pious, D. (1990). Defective processing and presentation of exogenous antigens in mutants with normal HLA class II genes. Nature 343, 71-74.
49. Mellman, I. (1996). Endocytosis and molecular sorting. Ann. Rev. Cell Dev. Biol. 12, 575-625.
50. 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.
51. 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 61, 171-183.
52. Nijman, H.W., Kleijmeer, M.J., Ossevoort, M.A., Oorschot, V.M., Vierboom, M.P., van de Keur, M., Kenemans, P., Kast, W.M., Geuze, H.J., and Melief, C.J. (1995). Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J. Exp. Med. 182, 163-174.
53. Noelle, R., and Snow, E.C. (1992). T helper cells. Curr. Opin. Immunol. 4, 333-337.
54. Peters, P.J., Neefjes, J.J., Oorschot, V., Ploegh, H.L., and Geuze, H.J. (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.
55. Pierre, P., Denzin, L.K., Hammond, C., Drake, J.R., Amigorena, S., Cresswell, P., and Mellman, I. (1996). HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity 4, 229-239.
56. Pieters, J. (1997). MHC class II restricted antigen presentation. Curr. Opin. Immunol. 9, 89-96.
57. 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. 115, 1213-1223.
58. Pieters, J., Bakke, O., and Dobberstein, B. (1993).The MHC class II-associated Invariant chain contains two endosomal sorting signals within its cytoplasmic tail. J. Cell Sci. 106, 831-846.
59. Pinet, V., Vergelli, M., Martin, R., Bakke, O., and Long, E.O. (1995). Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 375, 603-606.
60. Ploegh, H.L., Cannon, L.E., and Strominger, J.L. (1979). Cell-free translation of the mRNAs for the heavy and light chains of HLA-A and HLA-B antigens. Proc. Natl. Acad. Sci. USA 76, 2273-2277.
61. Pober, J.S., Collins, T., Gimbrone, M.A., Jr., Cotran, R.S., Gitlin, J.D., Fiers, W., Clayberger, C., Krensky, A.M., Burakoff, S.J., and Reiss, C.S. (1983). Lymphocytes recognize human vascular endothelial and dermal fibroblast la antigens induced by recombinant immune interferon. Nature 305, 726-729.
62. 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.
63. Roche, P.A., and Cresswell, P. (1990). Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345, 615-618.
64. Roche, P.A., Marks, M.S., and Cresswell, P. (1991). Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 354, 392-394.
65. Sallusto, F., Cella, M., Danieli, C., and Lanzavecchia, A. (1995). Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182, 389-400.
66. Sallusto, F., and Lanzavecchia, A. (1994). Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179, 1109-1118.
67. Sanderson, F., Kleijmeer, M.J., Kelly, A., Verwoerd, D., Tulp, A., Neefjes, J.J., Geuze, H.J., and Trowsdale, J. (1994). Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 266, 1566-1569.
68. Sant, A.J., and Miller, J. (1994). MHC class II antigen processing: biology of invariant chain. Curr. Opin. Immunol. 6, 57-63.
69. Satoh, S., Nishimura, H., Clark, A.E., Kozka, I.J., Vannucci, S.J., Simpson, I.A., Quon, M.J., Cushman, S.W., and Holman, G.D. (1993). Use of bismannose photolabel to elucidate insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. Evidence that exocytosis is a critical site of hormone action. J. Biol. Chem. 268, 17820-17829.
70. Schaiff, W.T., Hruska, K.A., Jr., McCourt, D.W., Green, M., and Schwartz, B.D. (1992). HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells. J. Exp. Med. 176, 657-666.
71. Schmidt, A., Hannah, M.J., Huttner, W.B. (1997). Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J. Cell Biol. 137, 445-458.
72. Sherman, M.A., Weber, D.A., and Jensen, P.E. (1995). DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity 3, 197-205.
73. Sloan, V.S., Cameron, P., Porter, G., Gammon, M., Amaya, M., Mellins, E., and Zaller, D.M. (1995). Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375, 802-806.
74. Slot, J.W., Geuze, H.J., Gigengack, S., Lienhard, G.E., and James, D.E. (1991). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113, 123-135.
75. Spies, T., Bresnahan, M., Bahram, S., Arnold, D., Blanck, G., Mellins, E., Pious, D., and DeMars, R. (1990). A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway. Nature 348, 744-747.
76. Steimle, V., Otten, L.A., Zufferey, M., and Mach, B. (1993). Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75, 135-146.
77. Steinman, R.M. (1991). The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9, 271-296.
78. Steinman, R.M., and Swanson, J. (1995). The endocytic activity of dendritic cells. J. Exp. Med. 182, 283-288.
79. Strubin, M., Berte, C., and Mach, B. (1986). Alternative splicing and alternative initiation of translation explain the four forms of the la-antigen associated invariant chain. EMBO J. 5, 3483-3488.
80. Sudhof, T.C. (1995). The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
81. Teyton, L., O'Sullivan, D., Dickson, P.W., Lotteau, V., Sette, A., Fink, P., and Peterson, P.A. (1990). Invariant chain distinguishes between the exogenous and endogenous antigen presentation pathways. Nature 348, 39-44.
82. Thomas-Reetz, A.C., and De Camilli, P. (1994). A role for synaptic vesicles in non-neuronal cells: clues from pancreatic beta cells and from chromaffin cells. Faseb. J. 8, 209-216.
83. Thorens, B. (1993). Facilitated glucose transporters in epithelial cells. Annu. Rev. Physiol. 55, 591-608.
84. Townsend, A., and Bodmer, H. (1989). Antigen recognition by class I-restricted T lymphocytes. Ann. Rev. Immunol. 7, 601-624.
85. Townsend, A., Ohlen, C., Bastin, J., Ljunggren, H.-G., Foster, L., and Karre, K. (1989). Association of class I major histocompatibility heavy and light chains induced by viral peptides. Nature 340, 443-448.
86. Townsend, A.R M., Gotch, F.M., and Davey, J. (1985). Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42, 457-467.
87. 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.
88. Warmerdam, P.A., 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. 133, 281-291.
89. 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.
90. 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.
91. Zinkernagel, R.M., and Doherty, P.C. (1974a). Immunological surveillance against altered self components by sensitised T lymphocytes in lymphocytic choriomeningitis. Nature 251, 547-548.
92. Zinkernagel, R.M., and Doherty, P.C. (1974b). Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701-702.