Intracellular pathway for the generation of functional MHC class II peptide complexes in immature human dendritic cells

Journal of Immunology

Volumn 160, Issue 6, 1998, Pages 2597-2607

  Saudrais, Cédric ^a   Spehner, Danièle ^b   De La Salle, Henri ^b   Bohbot, Alain ^b   Cazenave, Jean Pierre ^b   Goud, Bruno ^a   Hanau, Daniel ^b   Salamero, Jean ^a,c  

^a CNRS   (France)

^b HÔPITAL DE HAUTEPIERRE   (France)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL COMPARTMENTALIZATION; CELL STIMULATION; COMPLEX FORMATION; DENDRITIC CELL; ENDOCYTOSIS; ENDOSOME; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; INTERNALIZATION; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN DEGRADATION; VIRUS TRANSFORMATION;

CELL MEMBRANE; CELLS, CULTURED; DENDRITIC CELLS; DIMERIZATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MICROTUBULES;

EID: 0032521508     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Cresswell, P. 1994. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:259.
2. Riberdy, J. M., R. R. Avva, H. J. Geuze, and P. Cresswell. 1994. Transport and intracellular distribution of MHC class II molecules and associated invariant chain in normal and antigen-processing mutant cell lines. J. Cell Biol. 125:1225.
3. 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.
4. 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.
5. 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.
6. Kleijmeer, M. J., M. A. Ossevoort, C. J. van Veen, J. J. van Hellemond, J. J. Neefjes, W. M. Kast, C. J. 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.
7. 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.
8. Denzin, L. K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82:155.
9. 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.
10. Glickman, J. N., P. A. Morton, J. W. Slot, S. Kornfeld, and H. J. Geuze. 1996. The biogenesis of the MHC class II compartment in human I-cell disease B lymphoblasts. J. Cell Biol. 132:769.
11. 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.
12. 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.
13. Schuler, G., and R. M. Steinman. 1985. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161:526.
14. Witmer-Pack, M. D., J. Valinsky, W. Olivier, and R. M. Steinman. 1988. Quantitation of surface antigens on cultured murine epidermal Langerhans cells: rapid and selective increase in the level of surface MHC products. J. Invest. Dermatol. 90:387.
15. Jiang, W., W. J. Swiggard, C. Heufler, M. Peng, A. Mirza, R. M. Steinman, and M. C. Nussenzweig. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375:151.
16. Sallusto, F., M. Cella, C. Danieli, and A. Lanzavecchia. 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.
17. Guery, J. C., F. Ria, and L. Adorini. 1996. Dendritic cells but not B cells present antigenic complexes to class II-restricted T cells after administration of protein in adjuvant. J. Exp. Med. 183:751.
18. Inaba, K., J. P. Metlay, M. T. Crowley, and R. M. Steinman. 1990. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J. Exp. Med. 172:631.
19. Sallusto, F., and A. Lanzavecchia. 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.
20. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271.
21. Austyn, J. M. 1996. New insights into the mobilization and phagocytic activity of dendritic cells. J. Exp. Med. 183:1287.
22. Thirdborough, S. M., N. J. London, R. F. James, and P. R. Bell. 1993. A method for the isolation of human lymphoid dendritic cells from the spleen. Transplant lmmunol. 1:143.
23. Lenz, A., M. Heine, G. Schuler, and N. Romani. 1993. Human and murine dermis contain dendritic cells: isolation by means of a novel method and phenotypical and functional characterization. J. Clin. Invest. 92:2587.
24. Winzler, C., P. Rovere, M. Rescigno, F. Granucci, G. Penna, L. Adorini, V. S. Zimmermann, J. Davoust, and P. Ricciardi-Castagnoli. 1997. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185:317.
25. Xu, S., P. R. Bergstresser, and A. Takashima. 1995. Phenotypic and functional heterogeneity among murine epidermal-derived dendritic cell clones. J. Invest. Dermatol. 105:831.
26. Peters, J. H., R. Gieseler, B. Thiele, and F. Steinbach. 1996. Dendritic cells: from ontogenetic orphans to myelomonocytic descendants. Immunol. Today 17:273.
27. O'Doherty, U., M. Peng, S. Gezelter, W. J. Swiggard, M. Betjes, N. Bhardwaj, and R. M. Steinman. 1994. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 82:487.
28. Weissman, D., Y. Li, J. Ananworanich, L. J. Zhou, J. Adelsberger, T. F. Tedder, M. Baseler, and A. S. Fauci. 1995. Three populations of cells with dendritic morphology exist in peripheral blood, only one of which is infectable with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 92:826.
29. + precursors. J. Immunol. 158: 2134.
30. 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.
31. + dendritic cells and tartrate-resistant acid phosphatase-positive osteoclast-like multinucleated giant cells from human monocytes. Blood 88:4029.
32. 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.
33. Faradji, A., A. Bohbot, M. Schmitt-Goguel, J. C. Siffert, S. Dumont, M. L. Wiesel, Y. Piemont, A. Eischen, J. P. Bergerat, J. Bartholeyns, P. Poindron, J. P. Witz, and F. Oberling. 1994. Large scale isolation of human blood monocytes by continuous flow centrifugation leukapheresis and counterflow centrifugation elutriation for adoptive cellular immunotherapy in cancer patients. J. Immunol. Methods 174:297.
34. de la Salle, H., D. Hanau, D. Fricker, A. Urlacher, A. Kelly, J. Salamero, S. H. Powis, L. Donato, H. Bausinger, M. Laforet, M. Jeras, D. Spehner, T. Bieber, A. Falkenrodt, J. P. Cazenave, J. Trowsdale, and M. M. Tongio. 1994. Homozygous human TAP peptide transporter mutation in HLA class I deficiency. Science 265:237.
35. Lampson, L. A., and R. Levy. 1980. Two populations of Ia-like molecules on a human B cell line. J. Immunol. 125:293.
36. Guy, K., V. Van Heyningen, B. B. Cohen, D. L. Deane, and C. M. Steel. 1982. Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to Ia alpha and beta chains. Eur. J. Immunol. 12:942.
37. Salamero, J., R. Le Borgne, C. Saudrais, B. Goud, and B. Hoflack. 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.
38. Hanau, D., M. Fabre, D. A. Schmitt, J. L. Stampf, J. C. Garaud, T. Bieber, E. Grosshans, C. Benezra, and J. P. Cazenave. 1987. Human epidermal Langerhans cells internalize by receptor-mediated endocytosis T6 (CD1 "NA1/34") surface antigen: birbeck granules are involved in the intracellular traffic of the T6 antigen. J. Invest. Dermatol. 89:172.
39. Humbert, M., G. Raposo, P. Cosson, H. Reggio, J. Davoust, and J. Salamero. 1993. The invariant chain induces compact forms of class II molecules localized in late endosomal compartments. Eur. J. Immunol. 23:3158.
40. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680.
41. Salamero, J., E. S. Sztul, and K. E. Howell. 1990. Exocytic transport vesicles generated in vitro from the trans-Golgi network carry secretory and plasma membrane proteins. Proc. Natl. Acad. Sci. USA 87:7717.
42. 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 J. 14:37.
43. Bijlmakers, M. J., P. Benaroch, and H. L. Ploegh. 1994. Assembly of HLA DR1 molecules translated in vitro: binding of peptide in the endoplasmic reticulum precludes association with invariant chain. EMBO J. 13:2699.
44. Gachet, C., D. Hanau, D. Spehner, C. Brisson, J. C. Garaud, D. A. Schmitt, P. Ohlmann, and J. P. Cazenave. 1993. Alpha IIb beta 3 integrin dissociation induced by EDTA results in morphological changes of the platelet surface-connected canalicular system with differential location of the two separate subunits. J. Cell Biol. 120:1021.
45. 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 354:392.
46. Strubin, M., C. Berte, and B. Mach. 1986. Alternative splicing and alternative initiation of translation explain the four forms of the Ia antigen-associated invariant chain. EMBO J. 5:3483.
47. 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.
48. 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.
49. Lindner, R., and E. R. Unanue. 1996. Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J. 15:6910.
50. Bonnerot, C., D. Lankar, D. Hanau, D. Spehner, J. Davoust, J. Salamero, and W. H. Fridman. 1995. Role of B cell receptor Ig alpha and Ig beta subunits in MHC class II-restricted antigen presentation. Immunity 3:335.
51. Salzman, N. H., and F. R. Maxfield. 1989. Fusion accessibility of endocytic compartments along the recycling and lysosomal endocytic pathways in intact cells. J. Cell Biol. 109:2097.
52. Brown, K. D., M. Friedkin, and E. Rozengurt. 1980. Colchicine inhibits epidermal growth factor degradation in 3T3 cells. Proc. Natl. Acad. Sci. USA 77:480.
53. Durrbach, A., D. Louvard, and E. Coudrier. 1996. Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109:457.
54. Oka, J. A., and P. H. Weigel. 1983. Microtubule-depolymerizing agents inhibit asialo-orosomucoid delivery to lysosomes but not its endocytosis or degradation in isolated rat hepatocytes. Biochim. Biophys. Acta 763:368.
55. Bera, T., G. M. Kindberg, T. Ford, and R. Blomhoff. 1985. Intracellular transport of asialoglycoproteins in rat hepatocytes: evidence for two subpopulations of lysosomes. Exp. Cell Res. 161:285.
56. Sugita, M., R. M. Jackman, E. van Donselaar, S. M. Behar, R. A. Rogers, P. J. Peters, M. B. Brenner, and S. A. Porcelli. 1996. Cytoplasmic tail-dependent localization of CD1b antigen-presenting molecules to MIICs. Science 273:349.
57. 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.
58. Futter, C. E., C. N. Connolly, D. F. Cutler, and C. R. Hopkins. 1995. Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface. J. Biol. Chem. 270:10999.
59. 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.
60. Maric, 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.
61. Wubbolts, R., M. Fernandez-Borja, L. Oomen, D. Verwoerd, H. Janssen, J. Calafat, A. Tulp, S. Dusseljee, and J. Neefjes. 1996. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135:611.
62. Escola, J. M., F. Deleuil, E. Stang, J. Boretto, P. Chavrier, and J. P. Gorvel. 1996. Characterization of a lysozyme-major histocompatibility complex class II molecule-loading compartment as a specialized recycling endosome in murine B lymphocytes. J. Biol. Chem. 271:27360.
63. Bremnes, B., T. Madsen, M. Gedde-Dahl, and O. Bakke. 1994. An LI and ML motif in the cytoplasmic tail of the MHC-associated invariant chain mediate rapid internalization. J. Cell Sci. 107:2021.
64. 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.
65. Kampgen, E., N. Koch, F. Koch, P. Stoger, C. Heufler, G. Schuler, and N. Romani. 1991. Class II major histocompatibility complex molecules of murine dendritic cells: synthesis, sialylation of invariant chain, and antigen processing capacity are down-regulated upon culture. Proc. Natl. Acad. Sci. USA 88:3014.
66. Becker, D., A. B. Reske-Kunz, J. Knop, and K. Reske. 1991. Biochemical properties of MHC class II molecules endogenously synthesized and expressed by mouse Langerhans cells. Eur. J. Immunol. 21:1213.
67. Peterson, M., and J. Miller. 1992. Antigen presentation enhanced by the alternatively spliced invariant chain gene product p41. Nature 357:596.
68. Fineschi, B., L. S. Arneson, M. F. Naujokas, and J. Miller. 1995. Proteolysis of major histocompatibility complex class II-associated invariant chain is regulated by the alternatively spliced gene product, p41. Proc. Natl. Acad. Sci. USA 92: 10257.