Early Endosomes and a Late Endocytic Compartment Generate Different Peptide-Class II MHC Complexes via Distinct Processing Mechanisms

Journal of Immunology

Volumn 158, Issue 4, 1997, Pages 1523-1532

  Griffin, John P ^a   Chu, Rose ^a   Harding, Clifford V ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

H2 M ANTIGENS; H2-M ANTIGENS; HLA ANTIGEN CLASS 2; HLA D ANTIGEN; HLA DMB; HLA-DMB; LYSOZYME; PEPTIDE; RIBONUCLEASE;

ANIMAL; ANTIGEN PRESENTATION; ARTICLE; BIOSYNTHESIS; CBA MOUSE; CELL FRACTIONATION; CHEMISTRY; CHICKEN; ENDOCYTOSIS; ENDOSOME; IMMUNOLOGY; METABOLISM; MOUSE; PEPTIDE SYNTHESIS;

ANIMALS; ANTIGEN PRESENTATION; CHICKENS; ENDOCYTOSIS; ENDOSOMES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-D ANTIGENS; MICE; MICE, INBRED CBA; MURAMIDASE; PEPTIDE BIOSYNTHESIS; PEPTIDES; RIBONUCLEASES; SUBCELLULAR FRACTIONS;

EID: 0031568395     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Germain, R. N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76:287.
2. Cresswell, P. 1994. Assembly, transport and function of MHC class II molecules. Annu. Rev. Immunol. 12:259.
3. Harding, C. V., and H. J. Geuze. 1993. Antigen processing and intracellular traffic of antigens and MHC molecules. Curr. Opin. Cell Biol. 5:596.
4. 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.
5. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
6. i from class II MHC α- and β-chains. J. Immunol. 146:3877.
7. Nguyen, Q. V., and R. E. Humphreys. 1989. Time course of intracellular associations, processing, and cleavages of Ii forms and class II major histocompatibility complex molecules. J. Biol. Chem. 264:1631.
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.
9. Ziegler, H. K., and E. R. Unanue. 1982. Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc. Natl. Acad. Sci. USA 79:175.
10. Harding, C. V., and E. R. Unanue. 1989. Antigen processing and intracellular Ia: possible roles of endocytosis and protein synthesis in Ia function. J. Immunol. 142:12.
11. Harding, C. V., and E. R. Unanue. 1990. Low-temperature inhibition of antigen processing and iron uptake from transferrin: deficits in endosome functions at 18°C. Eur. J. Immunol. 20:323.
12. 125I-asialofetuin by the perfused rat liver. J. Biol. Chem. 255:5971.
13. Weigel, P. H., and J. A. Oka. 1982. Endocytosis and degradation mediated by the asialoglycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 257:1201.
14. Weigel, P. H., and J. A. Oka. 1981. Temperature dependence of endocytosis mediated by the asialogiycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 256:2615.
15. Harding, C. V., D. S. Collins, J. W. Slot, H. J. Geuze, and E. R. Unanue. 1991. Liposome-encapsulated antigens are processed in lysosomes, recycled and presented to T cells. Cell 64:393.
16. Harding, C. V., D. S. Collins, O. Kanagawa, and E. R. Unanue. 1991. Liposome-encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J. Immunol. 147:2860.
17. Jensen, P. E. 1991. Reduction of disulfide bonds during antigen processing: evidence from a thiol-dependent insulin determinant. J. Exp. Med. 174:1121.
18. Hampl, J., G. Gradehandt, H. Kalbacher, and E. Rude. 1992. In vitro processing of insulin for recognition by murine T cells results in the generation of A chains with free CysSH. J. Immunol. 148:2664.
19. Collins, D. S., E. R. Unanue, and C. V. Harding. 1991. Reduction of disulfide bonds within lysosomes is a key step in antigen processing. J. Immunol. 147: 4054.
20. 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.
21. Harding, C. V., and H. J. Geuze. 1992. Class II MHC molecules are present in macrophage lysosomes and phagolysosomes that function in the phagocytic processing of Listeria monocytogenes for presentation to T cells. J. Cell Biol. 119: 531.
22. Harding, C. V., and H. J. Geuze. 1993. Immunogenic peptides bind to class II MHC molecules in an early lysosomal compartment. J. Immunol. 151:3988.
23. Kleijmeer, M. J., M. A. Ossevoort, C. J. H. Van Veen, J. J. Van Hellemond, J. J. Neefjes, W. M. Kast, C. J. M. Melief, and H. J. Geuze. 1995. MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J. Immunol. 154:5715.
24. Nijman, H. W., M. J. Kleijmeer, M. A. Ossevoort, V. M. J. Oorschot, M. P. M. Vierboom, M. Van de Keur, P. Kenemans, W. M. Kast, H. J. Geuze, and C. J. M. Melief. 1995. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J. Exp. Med. 182:163.
25. Kleijmeer, M. J., V. M. Oorschot, and H. J. Geuze. 1994. Human resident Langerhans cells display a lysosomal compartment enriched in MHC class II. J. Invest. Dermatol. 103:516.
26. Mommaas, A. M., A. A. Mulder, C. J. Out, G. Girolomoni, H. K. Koerten, B. J. Vermeer, and F. Koning. 1995. Distribution of HLA class II molecules in epidermal Langerhans cells in situ. Eur. J. Immunol. 25:520.
27. 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.
28. Sanderson, F., C. Thomas, J. Neefjes, and J. Trowsdale. 1996. Association between HLA-DM and HLA-DR in vivo. Immunity 4:87.
29. 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 peptides. Immunity 3:197.
30. 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.
31. 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.
32. Monji, T., A. L. McCormack, J. R. I. Yates, and D. Pious. 1994. Invariant-cognate peptide exchange restores class II dimer stability in HLA-DM mutants. J. Immunol 153:4468.
33. Denzin, L. K., N. F. Robbins, C. Carboy-Newcomb, and P. Cresswell. 1994. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1:595.
34. Fling, S. P., B. Arp, and D. Pious. 1994. HLA-DMA and -DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells. Nature 368:554.
35. Morris, P., J. Shaman, M. Attaya, M. Amaya, S. Goodman, C. Bergman, J. J. Monaco, and E. Mellins. 1994. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368:551.
36. 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.
37. Amigorena, S., J. R. Drake, P. Webster, and I. Mellman. 1994. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369:113.
38. Guagliardi, L. E., B. Koppelman, J. S. Blum, M. S. Marks, P. Cresswell, and F. M. Brodsky. 1990. Co-localization of molecules involved in antigen processing and presentation in an early endocytic compartment. Nature 343:133.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. Rudensky, A. Y., M. Maric, S. Eastmen, L. Shoemaker, P. C. DeRoos, and J. S. Blum. 1994. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity 1:585.
46. 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.
47. Diment, S., and P. Stahl. 1985. Macrophage endosomes contain proteases which degrade endocytosed protein ligands. J. Biol. Chem. 260:15311.
48. Pinet, V., M. Vergelli, R. Martin, O. Bakke, and E. O. Long. 1995. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 375: 603.
49. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21:235.
50. Diment, S., and S. Shinde. 1995. Selective processing of exogenous antigens by antigen-presenting cells with deleted MHC genes. J. Immunol 154:530.
51. Stebbins, C. C., G. E. Loss, Jr., C. G. Elias, A. Chervonsky, and A. J. Sant. 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.
52. k class II molecules in human APC containing deleted or mutated HLA-DM genes. J. Immunol. 153: 5382.
53. Allen, P. M., D. J. Strydom, and E. R. Unanue. 1984. Processing of lysozyme by macrophages: identification of the determinant recognized by two T-cell hybridomas. Proc. Natl. Acad. Sci. USA 81:2489.
54. k molecule. J. Immunol. 143:802.
55. k molecule. J. Immunol. 141:4124.
56. Chen, J. S., R. G. Lorenz, J. Goldberg, and P. M. Allen. 1991. Identification and characterization of a T cell-inducing epitope of bovine ribonuclease that can be restricted by multiple class II molecules. J. Immunol 147:3672.
57. Harding, C. V. 1994. Techniques for studying phagocytic processing of bacteria for class I or II MHC-restricted antigen recognition by T lymphocytes. Methods Cell Biol. 45:307.
58. Pinet, V., M. S. Malnati, and E. O. Long. 1994. Two processing pathways tor the MHC class II-restricted presentation of exogenous influenza virus antigen. J. Immunol. 152:4852.
59. Rudensky, A. Y., S. Rath, P. Preston-Hurlbut, D. B. Murphy, and C. A. Janeway. 1991. On the complexity of self. Nature 353:660.
60. d. Proc. Natl. Acad. Sci. USA 81:7564.
61. Lanzavecchia, A., P. A. Reid, and C. Watts. 1992. Irreversible association of peptides with class II MHC molecules in living cells. Nature 357:249.
62. 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.
63. 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.
64. Reid, P. A., and C. Watts. 1990. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 346:655.
65. Machy, P., J.-P. Bizozzero, H. Reggio, and L. Leserman. 1990. Endocytosis and recycling of MHC-encoded class II molecules by mouse B lymphocytes. J. Immunol. 145:1350.
66. Salamero, J., M. Humbert, P. Cosson, and J. Davoust. 1990. Mouse B lymphocyte specific endocytosis and recycling of MHC class II molecules. EMBO J. 9:3489.
67. Harding, C. V., R. W. Roof, and E. R. Unanue. 1989. Turnover of Ia-peptide complexes is facilitated in viable antigen-presenting cells: biosynthetic turnover of Ia vs. peptide exchange. Proc. Natl. Acad. Sci. USA 86:4230.
68. Adorini, L., E. Appella, G. Doria, F. Cardinaux, and Z. A. Nagy. 1989. Competition for antigen presentation in living cells involves exchange of peptides bound by class II MHC molecules. Nature 342:800.
69. Escola, J.-M., J.-C. Grivel, P. Chavrier, and J.-P. Gorvel. 1995. Different endocytic compartments are involved in the tight association of class II molecules with processed hen egg lysozyme and ribonuclease A in B cells. J. Cell Sci. 108:2337.
70. Viville, S., J. Neefjes, V. Lotteau, A. Dierich, M. Lemeur, H Ploegh, C. Benoist, and D. Mathis. 1993. Mice lacking the MHC class II-associated invariant chain. Cell 72:635.
71. Nadimi, F., J. Moreno, F. Momburg, A. Heuser, S. Fuchs, L. Adorini, and G. J. Hämmerling. 1991. Antigen presentation of egg-white lysozyme but not of ribonuclease A is augmented by the major histocompatibility complex class II-associated invariant chain. Eur. J. Immunol 21:1255.
72. Peterson, M., and J. Miller. 1992. Antigen presentation enhanced by the alternatively spliced invariant chain gene product p41. Nature 357:596.