Protein kinase C delta stimulates antigen presentation by Class II MHC in murine dendritic cells

International Immunology

Volumn 19, Issue 6, 2007, Pages 719-732

  Majewski, Michael ^a   Bose, Tina O ^a   Sillé, Fenna C M ^a   Pollington, Annette M ^b   Fiebiger, Edda ^c   Boes, Marianne ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Antigen presentation processing; Antigens peptides epitopes; Dendritic cells; Rodent

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN KINASE C DELTA; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CELL STIMULATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVATION; ENZYME INHIBITION; IMMUNOSTIMULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

ACETOPHENONES; ANIMALS; ANTIGEN PRESENTATION; BENZOPYRANS; BLOTTING, WESTERN; CELL MEMBRANE; DENDRITIC CELLS; ENDOCYTOSIS; ENZYME INHIBITORS; FLOW CYTOMETRY; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; IONOMYCIN; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-DELTA; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE;

EID: 34447578931     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm034     Document Type: Article

References (85)

1. Vogt, A, B., Spindeldreher, S. and Kropshofer, H. 2002. Clustering of MHC-peptide complexes prior to their engagement in the immunological synapse: Lipid raft and tetraspan microdomains. Immunol. Rev. 189:136.
2. Krogsgaard, M., Huppa, J. B., Purbhoo, M. A. and Davis, M. M. 2003. Linking molecular and cellular events in T-cell activation and synapse formation. Semin. Immunol. 15:307.
3. Boes, M. and Ploegh, H. L. 2004. Translating cell biology in vitro to immunity in vivo. Nature 430:264.
4. Tortorella, D., Gewurz, B. E., Furman, M. H., Schust, D. J. and Ploegh, H. L. 2000. Viral subversion of the immune system. Annu. Rev. Immunol. 18:861.
5. 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.
6. Cresswell, P. 1994. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:259.
7. Germain, R. N. 1994. MHC-dependent antigen processing and peptide presentation: Providing ligands for T lymphocyte activation. Cell 76:287.
8. Pierre, P. and Mellman, I. 1998. Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93:1135.
9. Bryant, P. and Ploegh, H. 2004. Class II MHC peptide loading by the professionals. Curr. Opin. Immunol. 16:96.
10. Bijlmakers, M. J., Benaroch, P. and Ploegh, H. L. 1994. Mapping functional regions in the lumenal domain of the class II-associated invariant chain. J. Exp. Med. 180:623.
11. 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.
12. Bakke O. and Dobberstein, B. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
13. Akira, S., Takeda, K. and Kaisho, T. 2001. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat. Immunol. 2:675.
14. Boes, M., Cerny, J., Massol, R. et al. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418:983.
15. Chow, A., Toomre, D., Garrett, W. and Mellman, I. 2002. Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418:988.
16. Banchereau, J., Briere, F., Caux, C. et al. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767.
17. Keenan, C. and Kelleher, D. 1998. Protein kinase C and the cytoskeleton. Cell. Signal. 10:225.
18. Newton, A. C. 1997. Regulation of protein kinase C. Curr. Opin. Cell Biol. 9:161.
19. Hu, J., Jacinto, R., McCall, C. and Li, L. 2002. Regulation of IL-1 receptor-associated kinases by lipopolysaccharide. J. Immunol. 168:3910.
20. Noubir, S., Hmama, Z. and Reiner, N. E. 2004. Dual receptors and distinct pathways mediate interleukin-1 receptor-associated kinase degradation in response to lipopolysaccharide. Involvement of CD14/TLR4, CR3, and phosphatidylinositol 3-kinase. J. Biol. Chem. 279:25189.
21. Kadowaki, N., Ho, S., Antonenko, S. et al. 2001. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194:863.
22. Weinmann, A. S., Mitchell, D. M., Sanjabi, S. et al. 2001. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat. Immunol. 2:51.
23. Shinji, H., Akagawa, K. S. and Yoshida, T. 1994. LPS induces selective translocation of protein kinase C-beta in LPS-responsive mouse macrophages, but not in LPS-nonresponsive mouse macrophages. J. Immunol. 153:5760.
24. Dietrich, J., Hou, X., Wegener, A. M. and Geisler, C. 1994. CD3 gamma contains a phosphoserine-dependent di-leucine motif involved in down-regulation of the T cell receptor. EMBO J. 13:2156.
25. Pitcher, C., Honing, S., Fingerhut, A., Bowers, K. and Marsh, M. 1999. Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 10:677.
26. Guinamard, R., Signoret, N., Ishiai, M., Marsh, M., Kurosaki, T. and Ravetch, J. V. 1999. B cell antigen receptor engagement inhibits stromal cell-derived factor (SDF)-1alpha chemotaxis and promotes protein kinase C (PKC)-induced internalization of CXCR4. J. Exp. Med. 189:1461.
27. Bikoff, E. K., Huang, L. Y., Episkopou, V., van Meerwijk, J., Germain, R. N. and Robertson, E. J. 1993. Defective major histocompatibility complex class II assembly, transport, peptide acquisition, and CD4+ T cell selection in mice lacking invariant chain expression. J. Exp. Med. 177:1699.
28. Shi, G. P., Villadangos, J. A., Dranoff, G. et al. 1999. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10:197.
29. Madsen, L., Labrecque, N., Engberg, J. et al. 1999. Mice lacking all conventional MHC class II genes. Proc. Natl Acad. Sci. USA 96:10338.
30. Li, W., Zhang, J., Bottaro, D. P. and Pierce, J. H. 1997. Identification of serine 643 of protein kinase C-delta as an important autophosphorylation site for its enzymatic activity. J. Biol. Chem. 272:24550.
31. Inaba, K., Inaba, M., Romani, N. et al. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176:1693.
32. Villadangos, J. A., Riese, R. J., Peters, C., Chapman, H. A. and Ploegh, H. L. 1997. Degradation of mouse invariant chain: Roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med. 186:549.
33. Metlay, J. P., Witmer-Pack, M. D., Agger, R., Crowley, M. T., Lawless, D. and Steinman, R. M. 1990. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 171:1753.
34. Gangeswaran, R. and Jones, K. T. 1997. Unique protein kinase C profile in mouse oocytes: Lack of calcium-dependent conventional isoforms suggested by rtPCR and Western blotting. FEBS Lett. 412:309.
35. Bertho, N., Cerny, J., Kim, Y. M., Fiebiger, E., Ploegh, H. and Boes, M. 2003. Requirements for T cell-polarized tubulation of class II+ compartments in dendritic cells. J. Immunol. 171:5689.
36. Boes, M., Bertho, N., Cerny, J., Op Den Brouw, M., Kirchhausen, T. and Ploegh, H. 2003. T cells induce extended class II MHC compartments in dendritic cells in a Toll-like receptor-dependent manner. J. Immunol. 171:4081.
37. Kleijmeer, M., Ramm, G., Schuurhuis, D. et al. 2001. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155:53.
38. Wilson, N. S., El-Sukkari, D., Belz, G. T. et al. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102:2187.
39. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev Immunol. 9:271.
40. Jaksits, S., Bauer, W., Kriehuber, E. et al. 2004. Lipid raft-associated GTPase signaling controls morphology and CD8+ T cell stimulatory capacity of human dendritic cells. J. Immunol. 173:1628.
41. Newton, A. C. 1995. Protein kinase C: Structure, function, and regulation. J. Biol. Chem. 270:28495.
42. Mellor, H. and Parker, P. J. 1998. The extended protein kinase C superfamily. Biochem. J. 332(Pt 2):281.
43. Nishizuka, Y. 1992. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607.
44. Steinberg, S. F. 2004. Distinctive activation mechanisms and functions for protein kinase Cdelta. Biochem. J. 384:449.
45. Harder, T., Scheiffele, P., Verkade, P. and Simons, K. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929.
46. Nishizuka, Y. 1995. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9:484.
47. Villadangos, J. A., Cardoso, M., Steptoe, R. J. et al. 2001. MHC class II expression is regulated in dendritic cells independently of invariant chain degradation. Immunity 14:739.
48. Delamarre, L., Holcombe, H. and Mellman, I. 2003. Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation. J. Exp. Med. 198:111.
49. Holm, P. K., Eker, P., Sandvig, K. and van Deurs, B. 1995. Phorbol myristate acetate selectively stimulates apical endocytosis via protein kinase C in polarized MDCK cells. Exp. Cell Res. 217:157.
50. Cardone, M. H., Smith, B. L., Song, W., Mochly-Rosen, D. and Mostov, K. E. 1994. Phorbol myristate acetate-mediated stimulation of transcytosis and apical recycling in MDCK cells. J. Cell Biol. 124:717.
51. Garcia-Garcia, E. and Rosales, C. 2002. Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72:1092.
52. Chimini, G. and Chavrier, P. 2000. Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nat. Cell Biol. 2:E191.
53. Garrett, W. S., Chen, L. M., Kroschewski, R. et al. 2000. Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102:325.
54. Gschwendt, M., Muller, H. J., Kielbassa, K. et al. 1994. Rottlerin, a novel protein kinase inhibitor. Biochem. Biophys. Res. Commun. 199:93.
55. Kontny, E., Kurowska, M., Szczepanska, K. and Maslinski, W. 2000. Rottlerin, a PKC isozyme-selective inhibitor, affects signaling events and cytokine production in human monocytes. J. Leukoc. Biol. 67:249.
56. Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95.
57. McKee, A. S., Dzierszinski, F., Boes, M., Roos, D. S. and Pearce, E. J. 2004. Functional inactivation of immature dendritic cells by the intracellular parasite Toxoplasma gondii. J. Immunol. 173:2632.
58. Haverstick, D. M., Engelhard, V. H. and Gray, L. S. 1991. Three intracellular signals for cytotoxic T lymphocyte-mediated killing. Independent roles for protein kinase C, Ca2+ influx, and Ca2+ release from internal stores. J. Immunol. 146:3306.
59. Pardo, J., Buferne, M., Martinez-Lorenzo, M. J. et al. 2003. Differential implication of protein kinase C isoforms in cytotoxic T lymphocyte degranulation and TCR-induced Fas ligand expression. Int. Immunol. 15:1441.
60. Chen, Z. Z., Coggeshall, K. M. and Cambier, J. C. 1986. Translocation of protein kinase C during membrane immunoglobulin-mediated transmembrane signaling in B lymphocytes. J. Immunol. 136:2300.
61. DeFranco, A. L. 1993. Structure and function of the B cell antigen receptor. Annu. Rev. Cell Biol. 9:377.
62. Pleiman, C. M., D'Ambrosio, D. and Cambier, J. C. 1994. The B-cell antigen receptor complex: Structure and signal transduction. Immunol. Today 15:393.
63. 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.
64. Anderson, H. A.. Bergstralh, D. T., Kawamura, T., Blauvelt, A. and Roche, P. A. 1999. Phosphorylation of the invariant chain by protein kinase C regulates MHC class II trafficking to antigen-processing compartments. J. Immunol. 163:5435.
65. Schechtman, D. and Mochly-Rosen, D. 2001. Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene 20:6339.
66. Caux, C., Dezutter-Dambuyant, C., Schmitt, D. and Banchereau, J. 1992. GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature 360:258.
67. Davis, T. A., Saini, A. A., Blair, P. J. et al. 1998. Phorbol esters induce differentiation of human CD34+ hemopoietic progenitors to dendritic cells: Evidence for protein kinase C-mediated signaling. J. Immunol. 160:3689.
68. St Louis, D. C., Woodcock, J. B., Franzoso, G. et al. 1999. Evidence for distinct intracellular signaling pathways in CD34+ progenitor to dendritic cell differentiation from a human cell line model. J. Immunol. 162:3237.
69. Lindner, I., Kharfan-Dabaia, M. A., Ayala, E. et al. 2003. Induced dendritic cell differentiation of chronic myeloid leukemia blasts is associated with down-regulation of BCR-ABL. J. Immunol. 171:1780.
70. Cejas, P. J., Carlson, L. M., Zhang, J. et al. 2005. Protein kinase C betall plays an essential role in dendritic cell differentiation and autoregulates its own expression. J. Biol. Chem. 280:28412.
71. Leitges, M., Mayr, M., Braun, U. et al. 2001. Exacerbated vein graft arteriosclerosis in protein kinase Cdelta-null mice. J. Clin. Invest. 108:1505.
72. Liu, H., Keefer, J. R., Wang, Q. F. and Friedman, A. D. 2003. Reciprocal effects of C/EBPalpha and PKCdelta on JunB expression and monocytic differentiation depend upon the C/EBPalpha basic region. Blood 101:3885.
73. Cejas, P. J., Carlson, L. M., Kolonias, D. et al. 2005. Regulation of RelB expression during the initiation of dendritic cell differentiation. Mol. Cell. Biol. 25:7900.
74. Bertho, N., Blancheteau, V. M., Setterblad, N. et al. 2002. MHC class II-mediated apoptosis of mature dendritic cells proceeds by activation of the protein kinase C-delta isoenzyme. Int. Immunol. 14:935.
75. Setterblad, N., Roucard, C., Bocaccio, C., Abastado, J. P., Charron, D. and Mooney, N. 2003. Composition of MHC class II-enriched lipid microdomains is modified during maturation of primary dendritic cells. J. Leukoc. Biol. 74:40.
76. Do, Y., Hegde, V. L., Nagarkatti, P. S. and Nagarkatti, M. 2004. Bryostatin-1 enhances the maturation and antigen-presenting ability of murine and human dendritic cells. Cancer Res. 64:6756.
77. Schnare, M., Barton, G. M., Holt, A. C., Takeda, K., Akira, S. and Medzhitov, R. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2:947.
78. West, M. A., Wallin, R. P., Matthews. S. P. et al. 2004. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305:1153.
79. Sallusto, F., Celia, 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.
80. Pierre, P., Turley, S. J., Gatti, E. et al. 1997. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388:787.
81. Kleijmeer, M. J., Morkowski, S., Griffith, J. M., Rudensky, A. Y. and Geuze, H. J. 1997. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J. Cell Biol. 139:639.
82. Kabir, N., Schaefer, A. W., Nakhost, A., Sossin, W. S. and Forscher, P. 2001. Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152:1033.
83. Vermassen, E., Van Acker, K., Annaert, W. G. et al. 2003. Microtubule-dependent redistribution of the type-1 inositol 1,4,5-trisphosphate receptor in A7r5 smooth muscle cells. J. Cell Sci. 116:1269.
84. Wubbolts, R., Fernandez-Borja, M., Oomen, L. et al. 1996. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135:611.
85. Jordens, I., Fernandez-Borja, M., Marsman, M. et al. 2001. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11:1680.