The adaptor protein SAP directly associates with PECAM-1 and regulates PECAM-1-mediated-cell adhesion in T-like cell lines

Molecular Immunology

Volumn 58, Issue 2, 2014, Pages 206-213

  Proust, Richard ^a,d   Crouin, Catherine ^e   Gandji, Leslie Yewakon ^a,b,c,d   Bertoglio, Jacques ^e   Gesbert, Franck ^a,b,c,d  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b INSTITUT CURIE   (France)

^c Centre National de la Recherche Scientifique   (France)

^d INSERM   (France)

^e INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

PECAM 1; SH2 domain; SLAM associated protein; T cell adhesion

Indexed keywords

CD150 ANTIGEN; CD31 ANTIGEN; IMMUNOGLOBULIN; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL LINE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HYBRID; LEUKOCYTE; MEDIATOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; T LYMPHOCYTE; YEAST;

CAM; CELL-ADHESION-MOLECULE; FCS; FETAL CALF SERUM; IMMUNORECEPTOR TYROSINE-BASED INHIBITION MOTIF; IMMUNORECEPTOR TYROSINE-BASED SWITCH MOTIF; ITIM; ITSM; PECAM-1; PLATELET-ENDOTHELIAL CELL ADHESION MOLECULE-1; SAP; SH2; SH2-CONTAINING TYROSINE PHOSPHATASE-2; SH2-DOMAIN; SHP-2; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE; SLAM; SLAM-ASSOCIATED PROTEIN; SRC HOMOLOGY 2; T CELL ADHESION; TEM; TRANSENDOTHELIAL MIGRATION; X-LINKED LYMPHOPROLIFERATIVE SYNDROME-1; XLP-1;

AMINO ACID SEQUENCE; ANTIGENS, CD31; BASE SEQUENCE; CELL ADHESION; CELL LINE; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; T-LYMPHOCYTES;

EID: 84891444685     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.12.002     Document Type: Article

References (41)

1. Cannons J.L., Qi H., Lu K.T., Dutta M., Gomez-Rodriguez J., Cheng J., Wakeland E.K., Germain R.N., Schwartzberg P.L. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010, 32:253-265.
2. Cannons J.L., Tangye S.G., Schwartzberg P.L. SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 2011, 29:665-705.
3. Chan B., Lanyi A., Song H.K., Griesbach J., Simarro-Grande M., Poy F., Howie D., Sumegi J., Terhorst C., Eck M.J. SAP couples Fyn to SLAM immune receptors. Nat. Cell Biol. 2003, 5:155-160.
4. Coffey A.J., Brooksbank R.A., Brandau O., Oohashi T., Howell G.R., Bye J.M., Cahn A.P., Durham J., Heath P., Wray P., Pavitt R., Wilkinson J., Leversha M., Huckle E., Shaw-Smith C.J., Dunham A., Rhodes S., Schuster V., Porta G., Yin L., Serafini P., Sylla B., Zollo M., Franco B., Bolino A., Seri M., Lanyi A., Davis J.R., Webster D., Harris A., Lenoir G., de Saint-Basile G., Jones A., Behloradsky B.H., Achatz H., Murken J., Fassler R., Sumegi J., Romeo G., Vaudin M., Ross M.T., Meindl A., Bentley D.R. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 1998, 20:129-135.
5. Crouin C., Arnaud M., Gesbert F., Camonis J., Bertoglio J. A yeast two-hybrid study of human p97/Gab2 interactions with its SH2 domain-containing binding partners. FEBS Lett. 2001, 495:148-153.
6. Czar M.J., Kersh E.N., Mijares L.A., Lanier G., Lewis J., Yap G., Chen A., Sher A., Duckett C.S., Ahmed R., Schwartzberg P.L. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:7449-7454.
7. Elias C.G., Spellberg J.P., Karan-Tamir B., Lin C.H., Wang Y.J., McKenna P.J., Muller W.A., Zukowski M.M., Andrew D.P. Ligation of CD31/PECAM-1 modulates the function of lymphocytes, monocytes and neutrophils. Eur. J. Immunol. 1998, 28:1948-1958.
8. Gu C., Tangye S.G., Sun X., Luo Y., Lin Z., Wu J. The X-linked lymphoproliferative disease gene product SAP associates with PAK-interacting exchange factor and participates in T cell activation. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14447-14452.
9. Henshall T.L., Jones K.L., Wilkinson R., Jackson D.E. Src homology 2 domain-containing protein-tyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J. Immunol. 2001, 166:3098-3106.
10. Jackson D.E., Ward C.M., Wang R., Newman P.J. The protein-tyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1- and integrin-mediated cellular signaling. J. Biol. Chem. 1997, 272:6986-6993.
11. Latour S., Roncagalli R., Chen R., Bakinowski M., Shi X., Schwartzberg P.L., Davidson D., Veillette A. Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat. Cell Biol. 2003, 5:149-154.
12. Li C., Schibli D., Li S.S. The XLP syndrome protein SAP interacts with SH3 proteins to regulate T cell signaling and proliferation. Cell Signal. 2009, 21:111-119.
13. Li S.C., Gish G., Yang D., Coffey A.J., Forman-Kay J.D., Ernberg I., Kay L.E., Pawson T. Novel mode of ligand binding by the SH2 domain of the human XLP disease gene product SAP/SH2D1A. Curr. Biol. 1999, 9:1355-1362.
14. Lu T.T., Barreuther M., Davis S., Madri J.A. Platelet endothelial cell adhesion molecule-1 is phosphorylatable by c-Src, binds Src-Src homology 2 domain, and exhibits immunoreceptor tyrosine-based activation motif-like properties. J. Biol. Chem. 1997, 272:14442-14446.
15. Masuda M., Osawa M., Shigematsu H., Harada N., Fujiwara K. Platelet endothelial cell adhesion molecule-1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett. 1997, 408:331-336.
16. Morra M., Howie D., Grande M.S., Sayos J., Wang N., Wu C., Engel P., Terhorst C. X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu. Rev. Immunol. 2001, 19:657-682.
17. Muller W.A. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 2003, 24:327-334.
18. Muller W.A., Ratti C.M., McDonnell S.L., Cohn Z.A. A human endothelial cell-restricted, externally disposed plasmalemmal protein enriched in intercellular junctions. J. Exp. Med. 1989, 170:399-414.
19. Muller W.A., Weigl S.A., Deng X., Phillips D.M. PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 1993, 178:449-460.
20. Newman D.K., Hamilton C., Newman P.J. Inhibition of antigen-receptor signaling by platelet endothelial cell adhesion molecule-1 (CD31) requires functional ITIMs, SHP-2, and p56(lck). Blood 2001, 97:2351-2357.
21. Newman P.J., Newman D.K. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vasc. Biol. 2003, 23:953-964.
22. Newton-Nash D.K., Newman P.J. A new role for platelet-endothelial cell adhesion molecule-1 (CD31): inhibition of TCR-mediated signal transduction. J. Immunol. 1999, 163:682-688.
23. Nichols K.E., Harkin D.P., Levitz S., Krainer M., Kolquist K.A., Genovese C., Bernard A., Ferguson M., Zuo L., Snyder E., Buckler A.J., Wise C., Ashley J., Lovett M., Valentine M.B., Look A.T., Gerald W., Housman D.E., Haber D.A. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13765-13770.
24. Nichols K.E., Hom J., Gong S.Y., Ganguly A., Ma C.S., Cannons J.L., Tangye S.G., Schwartzberg P.L., Koretzky G.A., Stein P.L. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 2005, 11:340-345.
25. Nichols K.E., Ma C.S., Cannons J.L., Schwartzberg P.L., Tangye S.G. Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol. Rev. 2005, 203:180-199.
26. Pasquier B., Yin L., Fondaneche M.C., Relouzat F., Bloch-Queyrat C., Lambert N., Fischer A., de Saint-Basile G., Latour S. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J. Exp. Med. 2005, 201:695-701.
27. Poy F., Yaffe M.B., Sayos J., Saxena K., Morra M., Sumegi J., Cantley L.C., Terhorst C., Eck M.J. Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol. Cell 1999, 4:555-561.
28. Privratsky J.R., Newman D.K., Newman P.J. PECAM-1: conflicts of interest in inflammation. Life Sci. 2010, 87:69-82.
29. Proust R., Bertoglio J., Gesbert F. The adaptor protein SAP directly associates with CD3zeta chain and regulates T cell receptor signaling. PLoS ONE 2012, 7:e43200.
30. Pumphrey N.J., Taylor V., Freeman S., Douglas M.R., Bradfield P.F., Young S.P., Lord J.M., Wakelam M.J., Bird I.N., Salmon M., Buckley C.D. Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett. 1999, 450:77-83.
31. Quiroga M.F., Jurado J.O., Martinez G.J., Pasquinelli V., Musella R.M., Abbate E., Issekutz A.C., Bracco M.M., Malbran A., Sieling P.A., Chuluyan E., Garcia V.E. Cross-talk between CD31 and the signaling lymphocytic activation molecule-associated protein during interferon-gamma production against Mycobacterium tuberculosis. J. Infect. Dis. 2007, 196:1369-1378.
32. Reedquist K.A., Ross E., Koop E.A., Wolthuis R.M., Zwartkruis F.J., van Kooyk Y., Salmon M., Buckley C.D., Bos J.L. The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 2000, 148:1151-1158.
33. Sagawa K., Kimura T., Swieter M., Siraganian R.P. The protein-tyrosine phosphatase SHP-2 associates with tyrosine-phosphorylated adhesion molecule PECAM-1 (CD31). J. Biol. Chem. 1997, 272:31086-31091.
34. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., van Schaik S., Notarangelo L., Geha R., Roncarolo M.G., Oettgen H., De Vries J.E., Aversa G., Terhorst C. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 1998, 395:462-469.
35. Snow A.L., Marsh R.A., Krummey S.M., Roehrs P., Young L.R., Zhang K., van Hoff J., Dhar D., Nichols K.E., Filipovich A.H., Su H.C., Bleesing J.J., Lenardo M.J. Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency. J. Clin. Invest. 2009, 119:2976-2989.
36. Sumegi J., Huang D., Lanyi A., Davis J.D., Seemayer T.A., Maeda A., Klein G., Seri M., Wakiguchi H., Purtilo D.T., Gross T.G. Correlation of mutations of the SH2D1A gene and Epstein-Barr virus infection with clinical phenotype and outcome in X-linked lymphoproliferative disease. Blood 2000, 96:3118-3125.
37. Tanaka Y., Albelda S.M., Horgan K.J., van Seventer G.A., Shimizu Y., Newman W., Hallam J., Newman P.J., Buck C.A., Shaw S. CD31 expressed on distinctive T cell subsets is a preferential amplifier of beta 1 integrin-mediated adhesion. J. Exp. Med. 1992, 176:245-253.
38. Tangye S.G., Lazetic S., Woollatt E., Sutherland G.R., Lanier L.L., Phillips J.H. Cutting edge: human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J. Immunol. 1999, 162:6981-6985.
39. Thompson R.D., Noble K.E., Larbi K.Y., Dewar A., Duncan G.S., Mak T.W., Nourshargh S. Platelet-endothelial cell adhesion molecule-1 (PECAM-1)-deficient mice demonstrate a transient and cytokine-specific role for PECAM-1 in leukocyte migration through the perivascular basement membrane. Blood 2001, 97:1854-1860.
40. Vaporciyan A.A., DeLisser H.M., Yan H.C., Mendiguren I.I., Thom S.R., Jones M.L., Ward P.A., Albelda S.M. Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 1993, 262:1580-1582.
41. Wu C., Nguyen K.B., Pien G.C., Wang N., Gullo C., Howie D., Sosa M.R., Edwards M.J., Borrow P., Satoskar A.R., Sharpe A.H., Biron C.A., Terhorst C. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2001, 2:410-414.