SAP modulates B cell functions in a genetic background-dependent manner

Immunology Letters

Volumn 153, Issue 1-2, 2013, Pages 15-21

  Detre, Cynthia ^a   Yigit, Burcu ^a   Keszei, Marton ^a   Castro, Wilson ^a   Magelky, Erica M ^a   Terhorst, Cox ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

SAP; SLAM family receptors; XLP

Indexed keywords

IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; HUMORAL IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

SAP; SLAM-FAMILY RECEPTORS; XLP;

ANIMALS; ANTIGENS, CD40; ANTIGENS, CD43; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; HOMEODOMAIN PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE ACTIVATION; LYMPHOPROLIFERATIVE DISORDERS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84880352833     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2013.06.003     Document Type: Article

References (32)

1. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 1998, 395:462-469.
2. Coffey A.J., Brooksbank R.A., Brandau O., Oohashi T., Howell G.R., Bye J.M., et al. 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.
3. Calpe S., Wang N., Romero X., Berger S.B., Lanyi A., Engel P., et al. The SLAM and SAP gene families control innate and adaptive immune responses. Adv Immunol 2008, 97:177-250.
4. Detre C., Keszei M., Romero X., Tsokos G.C., Terhorst C. SLAM family receptors and the SLAM-associated protein (SAP) modulate T cell functions. Semin Immunopathol 2010, 32:157-171.
5. Cannons J.L., Tangye S.G., Schwartzberg P.L. SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol 2011, 29:665-705.
6. Morra M., Howie D., Grande M.S., Sayos J., Wang N., Wu C., et al. X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu Rev Immunol 2001, 19:657-682.
7. Morra M., Silander O., Calpe S., Choi M., Oettgen H., Myers L., et al. Alterations of the X-linked lymphoproliferative disease gene SH2D1A in common variable immunodeficiency syndrome. Blood 2001, 98:1321-1325.
8. Parolini O., Kagerbauer B., Simonitsch-Klupp I., Ambros P., Jaeger U., Mann G., et al. Analysis of SH2D1A mutations in patients with severe Epstein-Barr virus infections, Burkitt's lymphoma, and Hodgkin's lymphoma. Ann Hematol 2002, 81:441-447.
9. Crotty S., Kersh E.N., Cannons J., Schwartzberg P.L., Ahmed R. SAP is required for generating long-term humoral immunity. Nature 2003, 421:282-287.
10. Morra M., Barrington R.A., Abadia-Molina A.C., Okamoto S., Julien A., Gullo C., et al. Defective B cell responses in the absence of SH2D1A. Proc Natl Acad Sci U S A 2005, 102:4819-4823.
11. Cannons J.L., Yu L.J., Jankovic D., Crotty S., Horai R., Kirby M., et al. SAP regulates T cell-mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J Exp Med 2006, 203:1551-1565.
12. Qi H., Cannons J.L., Klauschen F., Schwartzberg P.L., Germain R.N. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008, 455:764-769.
13. Cannons J.L., Qi H., Lu K.T., Dutta M., Gomez-Rodriguez J., Cheng J., et al. 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.
14. Qi H. From SAP-less T cells to helpless B cells and back: dynamic T-B cell interactions underlie germinal center development and function. Immunol Rev 2012, 247:24-35.
15. Kageyama R., Cannons J.L., Zhao F., Yusuf I., Lao C., Locci M., et al. The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 2012, 36:986-1002.
16. Poy F., Yaffe M.B., Sayos J., Saxena K., Morra M., Sumegi J., et al. 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.
17. Morra M., Lu J., Poy F., Martin M., Sayos J., Calpe S., et al. Structural basis for the interaction of the free SH2 domain EAT-2 with SLAM receptors in hematopoietic cells. EMBO J 2001, 20:5840-5852.
18. Cao E., Ramagopal U.A., Fedorov A., Fedorov E., Yan Q., Lary J.W., et al. NTB-A receptor crystal structure: insights into homophilic interactions in the signaling lymphocytic activation molecule receptor family. Immunity 2006, 25:559-570.
19. Yan Q., Malashkevich V.N., Fedorov A., Fedorov E., Cao E., Lary J.W., et al. Structure of CD84 provides insight into SLAM family function. Proc Natl Acad Sci U S A 2007, 104:10583-10588.
20. Chan B., Lanyi A., Song H.K., Griesbach J., Simarro-Grande M., Poy F., et al. SAP couples Fyn to SLAM immune receptors. Nat Cell Biol 2003, 5:155-160.
21. Hwang P.M., Li C., Morra M., Lillywhite J., Muhandiram D.R., Gertler F., et al. A "three-pronged" binding mechanism for the SAP/SH2D1A SH2 domain: structural basis and relevance to the XLP syndrome. EMBO J 2002, 21:314-323.
22. Latour S., Roncagalli R., Chen R., Bakinowski M., Shi X., Schwartzberg P.L., et al. 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.
23. Berger S.B., Romero X., Ma C., Wang G., Faubion W.A., Liao G., et al. SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages. Nat Immunol 2010, 11:920-927.
24. Detre C., Keszei M., Garrido-Mesa N., Kis-Toth K., Castro W., Agyemang A.F., et al. SAP expression in invariant NKT cells is required for cognate help to support B-cell responses. Blood 2012, 120:122-129.
25. King I.L., Fortier A., Tighe M., Dibble J., Watts G.F., Veerapen N., et al. Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat Immunol 2011, 13:44-50.
26. Chang P.P., Barral P., Fitch J., Pratama A., Ma C.S., Kallies A., et al. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat Immunol 2011, 13:35-43.
27. Veillette A., Zhang S., Shi X., Dong Z., Davidson D., Zhong M.C. SAP expression in T cells, not in B cells, is required for humoral immunity. Proc Natl Acad Sci U S A 2008, 105:1273-1278.
28. Al-Alem U., Li C., Forey N., Relouzat F., Fondanèche M.C., Tavtigian S.V., et al. Impaired Ig class switch in mice deficient for the X-linked lymphoproliferative disease gene Sap. Blood 2005, 106:2069-2075.
29. Shlapatska L.M., Mikhalap S.V., Berdova A.G., Zelensky O.M., Yun T.J., Nichols K.E., et al. CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J Immunol 2001, 166:5480-5487.
30. Springer T.A., Dustin M.L. Integrin inside-out signaling and the immunological synapse. Curr Opin Cell Biol 2012, 24:107-115.
31. Wu C., Nguyen K.B., Pien G.C., Wang N., Gullo C., Howie D., et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat Immunol 2001, 2:410-414.
32. Rolink A., Melchers F., Andersson J. The SCID but not the RAG-2 gene product is required for S mu-S epsilon heavy chain class switching. Immunity 1996, 5:319-330.