Complement regulatory protein Crry/p65-mediated signaling in T lymphocytes: Role of its cytoplasmic domain and partitioning into lipid rafts

Journal of Leukocyte Biology

Volumn 78, Issue 6, 2005, Pages 1386-1396

  Jiménez Periañez, Arturo ^a   Ojeda, Gloria ^a   Criado, Gabriel ^a,b   Sánchez, Alejandra ^c   Pini, Eliana ^a   Madrenas, Joaquín ^b   Rojo, Jose Maria ^c   Portolés, Pilar ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Cell surface molecule; Costimulation; Signal transduction

Indexed keywords

ACTIN; CD3 ANTIGEN; CD4 ANTIGEN; COMPLEMENT; CRRY PROTEIN; GLYCOPROTEIN; INTERLEUKIN 4; INTERLEUKIN 5; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE ZAP 70; PROTEIN P56; STRESS ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; VAV PROTEIN; WORTMANNIN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL PROTECTION; COMPLEMENT ACTIVATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; CYTOSKELETON; IMMUNOPRECIPITATION; INNATE IMMUNITY; LIPID RAFT; LYMPHOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL;

ANIMALS; ANTIGENS, CD3; CELL LINE; CYTOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; IMMUNITY, NATURAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE MICRODOMAINS; MICE; ONCOGENE PROTEIN V-AKT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-VAV; RECEPTORS, COMPLEMENT; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TH1 CELLS; ZAP-70 PROTEIN-TYROSINE KINASE;

ANIMALIA;

EID: 28844503929     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1104642     Document Type: Article

References (69)

1. Acuto, O., Cantrell, D. (2000) T cell activation and the cytoskeleton. Annu. Rev. Immunol. 18, 165-184.
2. Samelson, L. (2002) Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20, 371-394.
3. Su, B., Jacinto, E., Hibi, M., Kallunki, T., Karin, M., Ben-Neriah, Y. (1994) JNK is involved in signal integration during costimulation of T lymphocytes. Cell 77, 727-736.
4. Janeway Jr., C. A., Bottomly, K. (1994) Signals and signs for lymphocyte responses. Cell 76, 275-285.
5. Rudd, C. E., Schneider, H. (2003) Unifying concepts in CD28, ICOS and CTLA4 coreceptor signaling. Nat. Rev. Immunol. 3, 544-556.
6. Rudd, C. E. (1996) Upstream-downstream: CD28 cosignaling pathways and T cell function. Immunity 4, 527-534.
7. Watts, T. H., DeBenedette, M. A. (1999) T cell co-stimulatory molecules other than CD28. Curr. Opin. Immunol. 11, 286-293.
8. Zhou, X. Y., Yashiro-Ohtani, Y., Toyo-Oka, K., Park, C. S., Tai, X. G., Hamaoka, T., Fujiwara, H. (2000) CD5 costimulation up-regulates the signaling to extracellular signal-regulated kinase activation in CD4+ CD8+ thymocytes and supports their differentiation to the CD4 lineage. J. Immunol. 164, 1260-1268.
9. Fernandez-Centeno, E., de Ojeda, G., Rojo, J. M., Portoles, P. (2000) Crry/p65, a membrane complement regulatory protein, has costimulatory properties on mouse T cells. J. Immunol. 164, 4533-4542.
10. Fearon, D. T., Carter, R. H. (1995) The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu. Rev. Immunol. 13, 127-149.
11. Carroll, M. C. (1998) The role of complement and complement receptors in induction and regulation of immunity. Annu. Rev. Immunol. 16, 545-568.
12. Lindahl, G., Sjöbring, U., Johnson, E. (2000) Human complement regulators: a major target for pathogenic microorganisms. Curr. Opin. Immunol. 12, 44-51.
13. Davis, L. S., Patel, S. S., Atkinson, J. P., Lipsky, P. E. (1988) Decay-accelerating factor functions as a signal transducing molecule for human T cells. J. Immunol. 141, 2246-2252.
14. Cerny, J., Stockinger, H., Horejsi, V. (1996) Noncovalent associations of T lymphocyte surface proteins. Eur. J. Immunol. 26, 2335-2343.
15. Millan, J., Qaidi, M., Alonso, M. A. (2001) Segregation of co-stimulatory components into specific T cell surface lipid rafts. Eur. J. Immunol. 31, 467-473.
16. CBL and LAT phosphorylation. J. Immunol. 164, 6091-6095.
17. Kemper, C., Chan, A. A., Green, J. M., Brett, K. A., Murphy, K. M., Atkinson, J. P. (2003) Activation of human CD4+ cells with CD3 and CD46 induces T-regulatory cell 1 phenotype. Nature 421, 388-392.
18. Zaffran, Y., Destaing, O., Roux, A., Ory, S., Nheu, T., Jurdic, P., Rabourdin-Combe, C., Astier, A. L. (2001) CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signal-regulated kinase mitogen-activated protein kinase. J. Immunol. 167, 6780-6785.
19. Sánchez, A., Feito, M. J., Rojo, J. M. (2004) CD46-mediated costimulation induces Th1-biased response and enhances early TCR/CD3 signaling in human CD4+ T lymphocytes. Eur. J. Immunol. 34, 2439-2448.
20. Kinoshita, T., Takeda, J., Hong, K., Kozono, H., Sakai, H., Inoue, K. (1988) Monoclonal antibodies to mouse complement receptor type 1 (CR1). Their use in a distribution study showing that mouse erythrocytes and platelets are CR1-negative. J. Immunol. 140, 3066-3072.
21. Kinoshita, T., Thyphronitis, G., Tsokos, G. C., Finkelman, F. D., Hong, K., Sakai, H., Inoue, K. (1990) Characterization of murine complement receptor type 2 and its immunological cross-reactivity with type 1 receptor, Int. Immunol. 2, 651-659.
22. Li, B., Sallee, C., Dehoff, M., Foley, S., Molina, H., Holers, V. M. (1993) Mouse Crry/p65. Characterization of monoclonal antibodies and the tissue distribution of a functional homologue of human MCP and DAF. J. Immunol. 151, 4295-4305.
23. Kameyoshi, Y., Matsushita, M., Okada, H. (1989) Murine membrane inhibitor of complement which accelerates decay of human C3 convertase. Immunology 68, 439-444.
24. Portolés, P., Rojo, J., Golby, A., Bonneville, M., Gromkowski, S., Greenbaum, L., Janeway Jr., C. A., Murphy, D. B., Bottomly, K. (1989) Monoclonal antibodies to murine CD3ε define distinct epitopes, one of which may interact with CD4 during T cell activation. J. Immunol. 142, 4169-4175.
25. Dialynas, D. P., Wilde, D. B., Marrack, P., Pierres, A., Wall, K., Harran, W., Otten, G., Liken, M., Pierres, M., Kappler, J., Fitch, F. (1983) Characterization of the murine antigenic determinant, designated L3T4a, by functional T cell clones appears to correlate primarily with class II MHC antigen-reactivity. Immunol. Rev. 74, 29-56.
26. Ledbetter, J. A., Herzenberg, L. A. (1979) Xenogeneic monoclonal antibodies to mouse lymphoid differenctiation antigens. Immunol. Rev. 47, 63-90.
27. Springer, T., Galfré, G., Secher, D. S., Milstein, C. (1979) Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur. J. Immunol. 9, 301-306.
28. Feito, M. J., Vaschetto, R., Criado, G., Sánchez, A., Chiocchetti, A., Jiménez-Periáñez, A., Dianzani, U., Portolés, M. P., Rojo, J. M. (2003) Mechanisms of ICOS costimulation: effects on proximal TCR signals and MAP kinase pathways. Eur. J. Immunol. 33, 204-214.
29. Karasuyama, H., Melchers, F. (1988) Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3 4, or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18, 97-104.
30. + T cell line is activated by syngeneic antigen presenting cells in the absence of antigen. Cell. Immunol. 164, 265-278.
31. Kaye, J., Porcelli, S., Tite, J., Jones, B., Janeway Jr., C. A. (1983) Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen-presenting cells in the activation of T cells. J. Exp. Med. 158, 836-856.
32. Yagi, J., Baron, J., Buxser, S., Janeway Jr., C. A. (1990) Bacterial proteins that mediate the association of a defined subset of T cell receptor:CD4 complexes with class II MHC. J. Immunol. 144, 892-901.
33. Parish, C. R., McKenzie, I. F. C. (1978) A sensitive rosetting method for detecting subpopulations of lymphocytes which react with alloantisera. J. Immunol. Methods 20, 173-183.
34. Darlington, P. J., Baroja, M. L., Chau, T. A., Siu, E., Ling, V., Carreno, B. M., Madrenas, J. (2002) Surface cytotoxic T lymphocyte-associated antigen 4 partitions within lipid rafts and relocates to the immunological synapse under conditions of inhibition of T cell activation. J. Exp. Med. 195, 1337-1347.
35. Tuosto, L., Acuto, O. (1998) CD28 affects the earliest signaling events generated by TCR engagement. Eur. J. Immunol. 28, 2131-2142.
36. Li, W., Whaley, C. D., Bonnevier, J. L., Mondino, A., Martin, M. E., Aagaard-Tillery, K. M., Mueller, D. L. (2001) CD28 signaling augments Elk-1-dependent transcription at c-fos gene during antigen stimulation. J. Immunol. 167, 827-835.
37. Foley, S., Li, B., Dehoff, M., Molina, H., Holers, V. M. (1993) Mouse Crry/p65 is a regulator of the alternative pathway of complement activation. Eur. J. Immunol. 23, 1381-1384.
38. Kim, Y-U., Kinoshita, T., Molina, H., Hourcade, D., Seya, T., Wagner, L. M., Holers, V. M. (1995) Mouse complement regulatory protein Crry/p65 uses the specific mechanisms of both human decay-accelerating factor and membrane cofactor protein. J. Exp. Med. 181, 151-159.
39. Quigg, R. J., He, C., Lim, A., Berthiaume, D., Alexander, J. J., Kraus, D., Holers, V. M. (1998) Transgenic mice overexpressing the complement inhibitor Crry as a soluble protein are protected from antibody-induced glomerular injury. J. Exp. Med. 188, 1321-1331.
40. Dykstra, M., Cherukuri, A., Sohn, H. W., Tzeng, S-J., Pierce, S. (2003) Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21, 457-481.
41. Viola, A., Schroeder, S., Sakakibara, Y., Lanzavecchia, A. (1999) T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283, 680-682.
42. lck) during T-cell activation. Mol. Cell. Biol. 8, 4353-4361.
43. Marth, J. D., Lewis, D. B., Cooke, M. P., Mellins, E. D., Gearn, M. E., Samelson, L. E., Wilson, C. B., Miller, A. D., Perlmutter, R. M. (1989) Lymphocyte activation provokes modification of a lymphocyte-specific protein tyrosine kinase (p56lck). J. Immunol. 142, 2430-2437.
44. Winkler, D. G., Park, I., Kim, T., Payne, N. S., Walsh, C. T., Strominger, J. L., Shin, J. (1993) Phosphorylation of Ser-42 and Ser-59 in the N-terminal region of tyrosine kinase p56lck. Proc. Natl. Acad. Sci. USA 90, 5176-5180.
45. Kesavan, K. P., Isaacson, C. C., Ashende, C. L., Geahlen, R. L., Harrison, M. L. (2002) Characterization of the in vivo sites of serine phosphorylation on Lck identifying serine 59 as a site of mitotic phosphorylation. J. Biol. Chem. 277, 14666-14673.
46. Cantley, L. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657.
47. Bustelo, X. R. (2000) Regulatory and signaling properties of the Vav family. Mol. Cell. Biol. 20, 1461-1477.
48. Penninger, J. M., Crabtree, G. R. (1999) The actin cytoskeleton and lymphocyte activation. Cell 96, 9-12.
49. Villalba, M., Bi, K., Rodriguez, F., Tanaka, Y., Schoenberger, S., Altman, A. (2001) Vav1/Rac-dependent actin cytoskeleton reorganization is required for lipid raft clustering in T cells. J. Cell Biol. 155, 331-338.
50. Montixi, C., Langlet, C., Bernard, A. M., Thimonier, J., Dubois, C., Wurbel, M. A., Chauvin, J. P., Pierres, M., He, H-T. (1998) Engagement of T cell receptor triggers its recruiment to low-density detergent-insoluble membrane domains. EMBO J. 17, 5334-5348.
51. Janes, P. W., Ley, S. C., Magee, A. I. (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461.
52. Yashiro-Ohtani, Y., Zhou, X. Y., Toyo-Oka, K., Tai, X. G., Park, C. S., Hamaoka, T., Abe, R., Miyake, K., Fujiwara, H. (2000) Non-CD28 costimulatory molecules present in T cell rafts induce T cell costimulation by enhancing the association of TCR with rafts. J. Immunol. 164, 1251-1259.
53. Cherukuri, A., Carter, R. H., Brooks, S., Bormann, W., Finn, R., Dowd, C. S., Pierce, S. (2004) B cell signaling is regulated by induced palmitoylation of CD81. J. Biol. Chem. 279, 31973-31982.
54. Yang, H., Reinherz, E. L. (2001) Dynamic recruitment of human CD2 into lipid rafts. Linkage to T cell signal transduction. J. Biol. Chem. 276, 18775-18785.
55. Mañes, S., del Real, G., Martínez-A, C. (2003) Pathogens: raft hijackers. Nat. Rev. Immunol. 3, 557-568.
56. Moran, M., Miceli, M. C. (1998) Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity 9, 787-796.
57. Shenoy-Scaria, A. M., Kwong, J., Fujita, T., Olszowy, M. W., Shaw, A., Lublin, D. M. (1992) Signal transduction through decay-accelerating factor: interaction of glycosyl-phosphatidylinositol anchor and protein tyrosine kinases p56lck and p59fyn. J. Immunol. 149, 3535-3541.
58. Crespo, P., Schuebel, K. E., Ostrom, A. A., Gutkind, J. S., Bustelo, X. R. (1997) Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogen product. Nature 385, 169-172.
59. Michel, F., Attal-Bonnefoy, G., Mangino, G., Mise-Omata, S., Acuto, O. (2001) CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 15, 935-945.
60. Brdickova, N., Brdicka, T., Angelisova, P., Horvath, O., Spicka, J., Hilgert, I., Paces, J., Simeoni, L., Kliche, S., Merten, C., Schraven, B., Horejsi, V. (2003) LIME: a new membrane raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J. Exp. Med. 198, 1453-1462.
61. Hur, E. M., Son, M., Lee, O. H., Choi, Y. B., Park, C., Lee, H., Yun, Y. (2003) LIME, a novel transmembrane adaptor protein, associates with p56lck and mediates T cell activation. J. Exp. Med. 198, 1463-1473.
62. Kang, H., Schneider H., Rudd, C. E. (2002) Phosphatidylinositol 3-kinase p85 adaptor function in T-cells. Co-stimulation and regulation of cytokine transcription independent of associated p110. J. Biol. Chem. 277, 912-921.
63. Lindstein, T., June, C. H., Ledbetter, J. A., Stella, G., Thompson, C. B. (1989) Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244, 339-343.
64. Chen, C-Y., Del Gatto-Konczak, F., Wu, Z., Karin, M. (1998) Stabilization of interleukin-2 by the c-Jun NH2-terminal kinase pathway. Science 280, 1945-1949.
65. Brint, E. K., Fitzgerald K. A., Smith, P., Coyle, A. J., Gutierrez-Ramos, J-C., Fallon, P. G., O'Neill, L. A. (2002) Characterization of signaling pathways activated by the interleukin 1 (IL-1) receptor homologue T1/ST2. J. Biol. Chem. 277, 49205-49211.
66. Blanchard, A. D., Page, K. R., Watkin, H., Hayward, P., Wong, T., Bartholomew, M., Quint, D. J., Daly, M., Garcia-Lopez, J., Champion, B. R. (2000) Identification and characterization of SKAT-2, a novel Th2-specific zinc finger gene. Eur. J. Immunol. 30, 3100-3110.
67. Ranganath, S., Ouyang, W., Bhattarcharya, D., Sha, W. C., Grupe, A., Peltz, G., Murphy, K. M. (1998) GATA-3-dependent enhancer activity in IL-4 gene regulation. J. Immunol. 161, 3822-3826.
68. Fearon, D. T., Carroll, M. C. (2000) Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu. Rev. Immunol. 18, 393-422.
69. Springall, T., Sheerin, N. S., Abe, K., Holers, V. M., Wan, H., Sacks, S. H. (2001) Epithelial secretion of C3 promotes colonization of the upper urinary tract by Escherichia coli. Nat. Med. 7, 801-806.