CD6 Regulates T-Cell Responses through Activation-Dependent Recruitment of the Positive Regulator SLP-76

REFERENCES

• Alberola-Ila, J., L. Places, D. A. Cantrell, J. Vives, and F. Lozano. 1992. Intracellular events involved in CD5-induced human T cell activation and proliferation. J. Immunol. 148:1287–1293.
   PubMedGoogle Scholar
• Axtell, R. C., M. S. Webb, S. R. Barnum, and C. Raman. 2004. Cutting edge: critical role for CD5 in experimental autoimmune encephalomyelitis: inhibition of engagement reverses disease in mice. J. Immunol. 173:2928–2932.
   PubMedGoogle Scholar
• Azzam, H. S., A. Grinberg, K. Lui, H. Shen, E. W. Shores, and P. E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188:2301–2311.
   PubMed Web of Science ®Google Scholar
• Bhandoola, A., R. Bosselut, Q. Yu, M. L. Cowan, L. Feigenbaum, P. E. Love, and A. Singer. 2002. CD5-mediated inhibition of TCR signaling during intrathymic selection and development does not require the CD5 extracellular domain. Eur. J. Immunol. 32:1811–1817.
   PubMedGoogle Scholar
• Bikah, G., F. M. Lynd, A. A. Aruffo, J. A. Ledbetter, and S. Bondada. 1998. A role for CD5 in cognate interactions between T cells and B cells, and identification of a novel ligand for CD5. Int. Immunol. 10:1185–1196.
   PubMedGoogle Scholar
• Bowen, M. A., D. D. Patel, X. Li, B. Modrell, A. R. Malacko, W.-C. Wang, H. Marquardt, M. Neubauer, J. M. Pesando, U. Francke, B. F. Haynes, and A. Aruffo. 1995. Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand. J. Exp. Med. 181:2213–2220.
   PubMed Web of Science ®Google Scholar
• Bowen, M. A., G. S. Whitney, M. Neubauer, G. C. Starling, D. Palmer, J. Zhang, N. J. Nowak, T. B. Shows, and A. Aruffo. 1997. Structure and chromosomal location of the human CD6 gene: detection of five human CD6 isoforms. J. Immunol. 158:1149–1156.
   PubMed Web of Science ®Google Scholar
• Brossard, C., M. Semichon, A. Trautmann, and G. Bismuth. 2003. CD5 inhibits signaling at the immunological synapse without impairing its formation. J. Immunol. 170:4623–4629.
   PubMedGoogle Scholar
• Brown, M. H., K. Boles, P. A. van der Merwe, V. Kumar, P. A. Mathew, and A. N. Barclay. 1998. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J. Exp. Med. 188:2083–2090.
   PubMed Web of Science ®Google Scholar
• Bunnell, S. C., D. I. Hong, J. R. Kardon, T. Yamazaki, C. J. McGlade, V. A. Barr, and L. E. Samelson. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:1263–1275.
   PubMedGoogle Scholar
• Calvo, J., L. Places, O. Padilla, J. M. Vila, J. Vives, M. A. Bowen, and F. Lozano. 1999. Interaction of recombinant and natural soluble CD5 forms with an alternative cell surface ligand. Eur. J. Immunol. 29:2119–2129.
   PubMedGoogle Scholar
• Castro, M. A., R. J. Nunes, M. I. Oliveira, P. A. Tavares, C. Simoes, J. R. Parnes, A. Moreira, and A. M. Carmo. 2003. OX52 is the rat homologue of CD6: evidence for an effector function in the regulation of CD5 phosphorylation. J. Leukoc. Biol. 73:183–190.
   PubMedGoogle Scholar
• da Silva, A. J., Z. Li, C. de Vera, E. Canto, P. Findell, and C. E. Rudd. 1997. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA 94:7493–7498.
   PubMedGoogle Scholar
• Douglass, A. D., and R. D. Vale. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121:937–950.
   PubMed Web of Science ®Google Scholar
• Gimferrer, I., M. Calvo, M. Mittelbrunn, M. Farnos, M. R. Sarrias, C. Enrich, J. Vives, F. Sanchez-Madrid, and F. Lozano. 2004. Relevance of CD6-mediated interactions in T cell activation and proliferation. J. Immunol. 173:2262–2270.
   PubMed Web of Science ®Google Scholar
• Gimferrer, I., M. Farnos, M. Calvo, M. Mittelbrunn, C. Enrich, F. Sanchez-Madrid, J. Vives, and F. Lozano. 2003. The accessory molecules CD5 and CD6 associate on the membrane of lymphoid T cells. J. Biol. Chem. 278:8564–8571.
   PubMedGoogle Scholar
• Gimferrer, I., A. Ibanez, M. Farnos, M. R. Sarrias, R. Fenutria, S. Rosello, P. Zimmermann, G. David, J. Vives, C. Serra-Pages, and F. Lozano. 2005. The lymphocyte receptor CD6 interacts with syntenin-1, a scaffolding protein containing PDZ domains. J. Immunol. 175:1406–1414.
   PubMedGoogle Scholar
• Harkiolaki, M., M. Lewitzky, R. J. Gilbert, E. Y. Jones, R. P. Bourette, G. Mouchiroud, H. Sondermann, I. Moarefi, and S. M. Feller. 2003. Structural basis for SH3 domain-mediated high-affinity binding between Mona/Gads and SLP-76. EMBO J. 22:2571–2582.
   PubMedGoogle Scholar
• Hassan, N. J., A. N. Barclay, and M. H. Brown. 2004. Frontline: optimal T cell activation requires the engagement of CD6 and CD166. Eur. J. Immunol. 34:930–940.
   PubMed Web of Science ®Google Scholar
• Houtman, J. C., Y. Higashimoto, N. Dimasi, S. Cho, H. Yamaguchi, B. Bowden, C. Regan, E. L. Malchiodi, R. Mariuzza, P. Schuck, E. Appella, and L. E. Samelson. 2004. Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences. Biochemistry 43:4170–4178.
   PubMed Web of Science ®Google Scholar
• Hutchings, N. J., N. Clarkson, R. Chalkley, A. N. Barclay, and M. H. Brown. 2003. Linking the T cell surface protein CD2 to the actin-capping protein CAPZ via CMS and CIN85. J. Biol. Chem. 278:22396–22403.
   PubMedGoogle Scholar
• Kobarg, J., G. S. Whitney, D. Palmer, A. Aruffo, and M. A. Bowen. 1997. Analysis of the tyrosine phosphorylation and calcium fluxing of human CD6 isoforms with different cytoplasmatic domains. Eur. J. Immunol. 27:2971–2980.
   PubMed Web of Science ®Google Scholar
• Ladbury, J. E., M. A. Lemmon, M. Zhou, J. Green, M. C. Botfield, and J. Schlessinger. 1995. Measurement of the binding of tyrosyl phosphopeptides to SH2 domains: a reappraisal. Proc. Natl. Acad. Sci. USA 92:3199–3203.
   PubMed Web of Science ®Google Scholar
• Li, S. C., G. Gish, D. Yang, A. J. Coffey, J. D. Forman-Kay, I. Ernberg, L. E. Kay, and T. Pawson. 1999. Novel mode of ligand binding by the SH2 domain of the human XLP disease gene product SAP/SH2D1A. Curr. Biol. 9:1355–1362.
   PubMed Web of Science ®Google Scholar
• Melton, E., N. Sarner, M. Torkar, P. A. van der Merwe, J. Q. Russell, R. C. Budd, C. Mamalaki, M. Tolaini, D. Kioussis, and R. Zamoyska. 1996. Transgene-encoded human CD2 acts in a dominant negative fashion to modify thymocyte selection signals in mice. Eur. J. Immunol. 26:2952–2963.
   PubMedGoogle Scholar
• Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587–3596.
   PubMed Web of Science ®Google Scholar
• Musci, M. A., L. R. Hendricks-Taylor, D. G. Motto, M. Paskind, J. Kamens, C. W. Turck, and G. A. Koretzky. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674–11677.
   PubMed Web of Science ®Google Scholar
• Ohno, H., T. Nakamura, H. Yagita, K. Okumura, M. Taniguchi, and T. Saito. 1991. Induction of negative signal through CD2 during antigen-specific T cell activation. J. Immunol. 147:2100–2106.
   PubMedGoogle Scholar
• Ono, M., S. Bolland, P. Tempst, and J. V. Ravetch. 1996. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature 383:263–266.
   PubMed Web of Science ®Google Scholar
• Pena-Rossi, C., L. A. Zuckerman, J. Strong, J. Kwan, W. Ferris, S. Chan, A. Tarakhovsky, A. D. Beyers, and N. Killeen. 1999. Negative regulation of CD4 lineage development and responses by CD5. J. Immunol. 163:6494–6501.
   PubMedGoogle Scholar
• Poy, F., M. B. Yaffe, J. Sayos, K. Saxena, M. Morra, J. Sumegi, L. C. Cantley, C. Terhorst, and M. J. Eck. 1999. Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol. Cell 4:555–561.
   PubMed Web of Science ®Google Scholar
• Risueno, R. M., D. Gil, E. Fernandez, F. Sanchez-Madrid, and B. Alarcon. 2005. Ligand-induced conformational change in the T-cell receptor associated with productive immune synapses. Blood 106:601–608.
   PubMedGoogle Scholar
• Robinson, W. H., H. E. Neuman de Vegvar, S. S. Prohaska, J. W. Rhee, and J. R. Parnes. 1995. Human CD6 possesses a large, alternatively spliced cytoplasmic domain. Eur. J. Immunol. 25:2765–2769.
   PubMed Web of Science ®Google Scholar
• Saifullah, M. K., D. A. Fox, S. Sarkar, S. M. Abidi, J. Endres, J. Piktel, T. M. Haqqi, and N. G. Singer. 2004. Expression and characterization of a novel CD6 ligand in cells derived from joint and epithelial tissues. J. Immunol. 173:6125–6133.
   PubMedGoogle Scholar
• Sauer, K., J. Liou, S. B. Singh, D. Yablonski, A. Weiss, and R. M. Perlmutter. 2001. Hematopoietic progenitor kinase 1 associates physically and functionally with the adaptor proteins B cell linker protein and SLP-76 in lymphocytes. J. Biol. Chem. 276:45207–45216.
   PubMedGoogle Scholar
• Singer, N. G., D. A. Fox, T. M. Haqqi, L. Beretta, J. S. Endres, S. Prohaska, J. R. Parnes, J. Bromberg, and R. M. Sramkoski. 2002. CD6: expression during development, apoptosis and selection of human and mouse thymocytes. Int. Immunol. 14:585–597.
   PubMed Web of Science ®Google Scholar
• Sonnenburg, E. D., A. Bilwes, T. Hunter, and J. P. Noel. 2003. The structure of the membrane distal phosphatase domain of RPTPalpha reveals interdomain flexibility and an SH2 domain interaction region. Biochemistry 42:7904–7914.
   PubMedGoogle Scholar
• Starling, G. C., G. S. Whitney, A. W. Siadak, M. B. Llewellyn, M. A. Bowen, A. G. Farr, and A. A. Aruffo. 1996. Characterization of mouse CD6 with novel monoclonal antibodies which enhance the allogeneic mixed leukocyte reaction. Eur. J. Immunol. 26:738–746.
   PubMedGoogle Scholar
• Tarakhovsky, A., S. B. Kanner, J. Hombach, J. A. Ledbetter, W. Muller, N. Killeen, and K. Rajewsky. 1995. A role for CD5 in TCR-mediated signal transduction and thymocyte selection. Science 269:535–537.
   PubMed Web of Science ®Google Scholar
• Teh, S. J., N. Killeen, A. Tarakhovsky, D. R. Littman, and H. S. Teh. 1997. CD2 regulates the positive selection and function of antigen-specific CD4− CD8+ T cells. Blood 89:1308–1318.
   PubMedGoogle Scholar
• Vargo, M. A., L. Nguyen, and R. F. Colman. 2004. Subunit interface residues of glutathione S-transferase A1-1 that are important in the monomer-dimer equilibrium. Biochemistry 43:3327–3335.
   PubMedGoogle Scholar
• Wee, S., G. L. Schieven, J. M. Kirihara, T. T. Tsu, J. A. Ledbetter, and A. Aruffo. 1993. Tyrosine phosphorylation of CD6 by stimulation of CD3: augmentation by the CD4 and CD2 coreceptors. J. Exp. Med. 177:219–223.
   PubMedGoogle Scholar
• Whitney, G. S., G. C. Starling, M. A. Bowen, B. Modrell, A. W. Siadak, and A. Aruffo. 1995. The membrane-proximal scavenger receptor cysteine-rich domain of CD6 contains the activated leukocyte cell adhesion molecule binding site. J. Biol. Chem. 270:18187–18190.
   PubMed Web of Science ®Google Scholar
• Wild, M. K., A. Cambiaggi, M. H. Brown, E. A. Davies, H. Ohno, T. Saito, and P. A. van der Merwe. 1999. Dependence of T cell antigen recognition on the dimensions of an accessory receptor-ligand complex. J. Exp. Med. 190:31–41.
   PubMedGoogle Scholar
• Wu, J. N., and G. A. Koretzky. 2004. The SLP-76 family of adapter proteins. Semin. Immunol. 16:379–393.
   PubMedGoogle Scholar
• Wyer, J. R., B. E. Willcox, G. F. Gao, U. C. Gerth, S. J. Davis, J. I. Bell, P. A. van der Merwe, and B. K. Jakobsen. 1999. T cell receptor and coreceptor CD8αα bind peptide-MHC independently and with distinct kinetics. Immunity 10:219–225.
   PubMedGoogle Scholar
• Yokosuka, T., K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M. L. Dustin, and T. Saito. 2005. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6:1253–1262.
   PubMed Web of Science ®Google Scholar
• Yu, H., J. K. Chen, S. Feng, D. C. Dalgarno, A. W. Brauer, and S. L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76:933–945.
   PubMed Web of Science ®Google Scholar
• Zimmerman, A. W., B. Joosten, R. Torensma, J. R. Parnes, F. N. van Leeuwen, and C. G. Figdor. 2006. Long-term engagement of CD6 and ALCAM is essential for T-cell proliferation induced by dendritic cells. Blood 107:3212–3220.
   PubMed Web of Science ®Google Scholar