Actin microfilaments control the MHC class II antigen presentation pathway in B cells

Journal of Cell Science

Volumn 111, Issue 13, 1998, Pages 1791-1800

  Barois, Nicolas ^a   Forquet, Frédérique ^a   Davoust, Jean ^a  

^a INSERM   (France)

Author keywords

Antigen processing; Cytoskeleton; H2 M molecule; Invariant chain; Lysosome

Indexed keywords

ACTIN; CYTOCHALASIN D; LEUPEPTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ACTIN FILAMENT; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CYTOSKELETON; ENDOSOME; MICROFILAMENT; PRIORITY JOURNAL;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CYTOCHALASIN D; HISTOCOMPATIBILITY ANTIGENS CLASS II; LYSOSOMES; MACROMOLECULAR SUBSTANCES; MICE; MICROFILAMENTS; MOLECULAR SEQUENCE DATA; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 0031822775     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Adorini, L., Ullrich, S. J., Appella, E. and Fuchs, S. (1990). Inhibition by brefeldin A of presentation of exogenous protein antigens to MHC class II-restricted T cells. Nature 346, 63-66.
2. Allen, P. M. and Unanue, F. R. (1984). Differential requirements for antigen processing by macrophages for lysozyme-specific T cell hybridomas. J. Immunol. 132, 1077-1079.
3. Amigorena, S., Webster, P., Drake, J., Newcomb, J., Cresswell, P. and Mellman, I. (1995). Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J. Exp. Med. 181, 1729-1741.
4. Arneson, L. S. and Miller, J. (1995). Efficient endosomal localisation of major histocompatibility complex class II-invariant chain complexes requires multimerization of the invariant chain targeting sequence. J. Cell Biol. 129, 1217-1228.
5. Barois, N., Forquet, F. and Davoust, J. (1997). Selective modulation of the major histocompatibility complex class II antigen presentation pathway following B cell receptor ligation and protein kinase C activation. J. Biol. Chem. 272, 3641-3647.
6. + T cells. Crit. Rev. Immunol. 16, 359-379.
7. Brachet, V., Raposo, G., Amigorena, S. and Mellman, I. (1997). Ii chain controls the transport of major histocompatibility complex class II molecules to and from lysosomes. J. Cell Biol. 137, 51-65.
8. Cella, M., Engering, A., Pinet, V., Pieters, J. and Lanzavecchia, A. (1997). Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388, 782-787.
9. Denzin, L. K. and Cresswell, P. (1995). HLA-DM induces CLIP dissociation from MHC: class II αβ dimers and facilitates peptide loading. Cell 82, 155-165.
10. Durrbach, A., Louvard, D. and Coudrier, E. (1996). Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109, 457-465.
11. Fernandez-Borja, M., Verwoerd, D., Sanderson, F., Aerts, H., Trowsdale, J., Tulp, A. and Neefjes, J. (1996). HLA-DM and MHC class II molecules co-distribute with peptidase-containing lysosomal subcompartments. Int. Immunol. 8, 625-640.
12. Germain, R. N. and Hendrix, L. R. (1991). MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 353, 134-139.
13. Germain, R. N. (1994). MHC-dependent antigen processing and peptide presentation: Providing ligands for T lymphocyte activation. Cell 76, 287-299.
14. Ghosh, P., Amaya, M., Mellins, E. and Wiley, D. C. (1995). The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature 378, 457-462.
15. Gottlieb, T. A., Ivanov, I. E., Adesnik, M. and Sabatini, D. D. (1993). Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120, 695-710.
16. Granger, B. L., Green, S. A., Gabel, C. A., Howe, C. L., Mellman, I. and Helenius, A. (1990). Characterization and cloning of Igp 110, a lysosomal membrane glycoprotein from mouse and rat cells. J. Biol. Chem. 265, 12036-12043.
17. Griffin, J. P., Chu, R. and Harding, C. V. (1997). Early endosomes and a late endocytic compartment generate different peptide-class II MHC complexes via distinct processing mechanisms. J. Immunol. 158, 1523-1532.
18. Griffiths, G., Hoflack, B., Simons, K., Mellman, I. and Kornfeld, S. (1988). The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329-341.
19. Harding, C. V., Roof, R. W. and Unanue, E. R. (1989). Turnover of lapeptide complexes is facilitated in viable antigen-presenting cells: Biosynthetic turnover of la vs. peptide exchange. Proc. Nat. Acad. Sci. USA 86, 4230-4234.
20. Liu, K.-J., Parikh, V. S., Tucker, P. W. and Kim, B. S. (1994). Surface immunoglobulins mediate efficient transport of antigen to lysosomal compartments resulting in enhanced specific antigen presentation by B cells. Eur. J. Immunol. 24, 2755-2760.
21. Long, E. O., LaVaute, T., Pinet, V. and Jaraquemada, D. (1994). Invariant chain prevents the HLA-DR-restricted presentation of a cytosolic peptide. J. Immunol. 153, 1487-1494.
22. Lorenz, R. G., Tyler, A. N. and Allen, P. M. (1988). T cell recognition of bovine ribonuclease: Self/non-self discrimination at the level of binding to the 1-Aλ molecule. J. Immunol. 141, 4124-4128.
23. MacLean-Fletcher, S. and Pollard, T. D. (1980). Mechanisms of action of cyto B on actin. Cell 20, 329-341.
24. Maric, M. A., Taylor, M. D. and Blum, J. S. (1994). Endosomal aspartic proteinases are required for invariant-chain processing. Proc. Vat. Acad. Sci. USA 91, 2171-2175.
25. Melamed, I., Downey, G. P., Aktories, K. and Roifman, C. M. (1991). Microfilament assembly is required for antigen-receptor-mcdiated activation of human B lymphocytes. J. Immunol. 147, 1139-1146.
26. Mitchell, R. N., Barnes, K. A., Grupp, S. A., Sanchez, M., Misulovin, Z., Nussenzweig, M. C. and Abbas, A. K. (1995). Intracellular targeting of antigens internalized by membrane immunoglobulin in B lymphocytes. J. Exp. Med. 181, 1705-1714.
27. Morkowski, S., Goldrath, A. W., Eastman, S., Ramachandra, L., Freed, D. C., Whiteley, P. and Rudensky, A. Y. (1995). T cell recognition of major histocompatibility complex class II complexes with invariant chain processing intermediates. J. Exp. Med. 182, 1403-1413.
28. Nadimi, F., Moreno, J., Momburg, F., Heuser, A., Fuchs, S., Adorini, L. and Hämmerling, G. J. (1991). Antigen presentation of hen egg-white lysozyme but not of ribonuclease A is augmented by the major histocompatibility complex class II-associated invariant chain. Eur. J. Immunol. 21, 1255-1263.
29. Neefjes, J. J. and Ploegh, H. L. (1992). Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistant αβ heterodimers in endosomes. EMBO J. 11, 411-416.
30. Newell, M. K., Justement, L. B., Miles, C. R. and Freed, J. H. (1988). Biochemical characterization of proteins that co-purify with class II antigens of the murine MHC. J. Immunol. 140, 1930-1938.
31. Nguyen, Q. V., Knapp, W. and Humphreys, R. E. (1989). Inhibition by leupeptin and antipain of the intracellular proteolysis of li. Hum. Immunol. 24, 153-163.
32. Odorizzi, C. G., Trowbridge, I. S., Xue, L., Hopkins, C. R., Davis, C. D. and Collawn, J. F. (1994). Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment. J. Cell Biol. 126, 317-330.
33. 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.
34. Pieters, J., Bakke, O. and Dobberstein, B. (1993). The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 106, 831-846.
35. 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.
36. Pond, L. and Watts, C. (1997). Characterization of transport of newly assembled. T cell-stimolatory MHC class II-peptide complexes from MHC class II compartments to the cell surface. J. Immunol. 159, 543-553.
37. Qiu, Y., Xu, X., Wandinger-Ness, A., Dalke, D. P. and Pierce, S. K. (1994). Separation of subcellular compartments containing distinct functional forms of MHC class II. J. Cell Biol. 125, 595-605.
38. Riese, R. J., Wolf, P. R., Brömme, 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.
39. Roche, P. A. and Cresswell, P. (1991). Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Nat. Acad. Sci. USA 88, 3150-3154.
40. 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.
41. Romagnoli, P. and Germain, R. N. (1994). The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy. J. Exp. Med. 180, 1107-1113.
42. Salamero, J., Humbert, M., Cosson, P. and Davoust, J. (1990). Mouse B lymphocyte specific endocytosis and recycling of MHC class II molecules. EMBO J. 9, 3489-3496.
43. 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.
44. Sanderson, F., Thomas, C., Neefjes, J. and Trowsdale, J. (1996). Association between HLA-DM and HLA-DR in vivo. Immunity 4, 87-96.
45. Soreng, K. M., Moore, J. C., Sherman, M. A. and Jensen, P. E. (1994). Requirement for protein synthesis in antigen processing by B cells. Cell. Immunol. 157, 277-290.
46. Soreng, K. M., Weber, D. A., joshi, H., Moore, J. C. and Jensen, P. E. (1995). A role for microfilaments but not microtubules in processing soluble antigens. Cell. Immunol. 166, 25-34.
47. St-Pierre, Y. and Watts, T. H. (1990). MHC class II-restricted presentation of native protein antigen by B cells is inhibitable by cycloheximide and brefeldin A. J. Immunol. 145, 812-818.
48. 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.
49. k protein. Proc. Nat. Acad. Sci. USA 86, 6297-6301.
50. Wade, W. F., Freed, J. H. and Edidin, M. (1989b). Translational diffusion of class II major histocompatibility complex molecules is constrained by their cytoplasmic domains. J. Cell Biol. 109, 3325-3331.
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.
52. Winzler, C., Rovere, P., Rescigno, M., Granucci, F., Penna, G., Adorini, L., Zimmermann, V. S., Davoust, J. and Ricciardi-Castagnoli, P. (1997). Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185, 317-328.
53. Wubbolts, R., Fernandez-Borja, M., Oomen, L., Verwoerd, D., Janssen, H., Cafafat, J., Tulp, A., Dusseljee, S. and Neefjes, J. (1996). Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135, 611-622.
54. Xu, M., Capraro, G. A., Daibata, M., Reyes, V. K. and Humphreys, R. E. (1994). Cathepsin B cleavage and release of invariant chain from MHC class II molecules follow a staged pattern. Mol. Immunol. 31, 723-731.