Linker for activation of T cells is displaced from lipid rafts and decreases in lupus T cells after activation via the TCR/CD3 pathway

Clinical Immunology

Volumn 142, Issue 3, 2012, Pages 243-251

  Abdoel, Nursamaa ^a   Brun, Susana ^a,c   Bracho, Carmen ^b   Rodríguez, Martín A ^a   Blasini, Ana M ^a  

^a HOSPITAL UNIVERSITARIO DE CARACAS   (Venezuela)

^b INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Immunological synapse; Linker for activation of t cells; Membrane microdomains; Systemic lupus erithematosus; T cell signaling

Indexed keywords

ANTIMALARIAL AGENT; AZATHIOPRINE; CD3 ANTIGEN; CYCLOPHOSPHAMIDE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; LAT PROTEIN; NONSTEROID ANTIINFLAMMATORY AGENT; PREDNISONE; T LYMPHOCYTE RECEPTOR;

ADOLESCENT; ADULT; ARTICLE; CHILD; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID RAFT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SCHOOL CHILD; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADOLESCENT; ADULT; CHILD; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MEMBRANE MICRODOMAINS; MIDDLE AGED; PHOSPHORYLATION; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84857363737     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2011.12.010     Document Type: Article

References (50)

1. Crispin J.C., Liossis S.N., Kis-Toth K., Lieberman L.A., Kyttaris V.C., Juang Y.T., Tsokos G.C. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol. Med. 2010, 16(2):47-57.
2. Fields P.E., Gajewski T.F., Fitch F.W. Blocked Ras activation in anergic CD4+ T cells. Science 1996, 271(5253):1276-1278.
3. Li W., Whaley C.D., Mondino A., Mueller D.L. Blocked signal transduction to the ERK and JNK protein kinases in anergic CD4+ T cells. Science 1996, 271(5253):1272-1276.
4. Deng C., Kaplan M.J., Yang J., Ray D., Zhang Z., McCune W.J., Hanash S.M., Richardson B.C. Decreased Ras-mitogen-activated protein kinase signaling may cause DNA hypomethylation in T lymphocytes from lupus patients. Arthritis Rheum. 2001, 44:397-407.
5. Yi Y., McNerney M., Datta S.K. Regulatory defects in Cbl and mitogen-activated protein kinase (extracellular signal-related kinase) pathways cause persistent hyperexpression of CD40 ligand in human lupus T cells. J. Immunol. 2000, 165(11):6627-6634.
6. Perl A., Jr Gergely P., Banki K. Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int. Rev. Immunol. 2004, 23(3-4):293-313.
7. Liossis S.N., Ding X.Z., Dennis G.J., Tsokos G.C. Altered pattern of TCR/CD3-mediated protein-tyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor zeta chain. J. Clin. Invest. 1998, 101(7):1448-1457.
8. Brundula V., Rivas L.J., Blasini A.M., París M., Salazar S., Stekman I.L., Rodríguez M.A. Diminished levels of T cell receptor zeta chains in peripheral blood T lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 1999, 42(9):1908-1916.
9. Kammer G.M., Laxminarayana D., Khan I.U. Mechanisms of deficient type I protein kinase A activity in lupus T lymphocytes. Int. Rev. Immunol. 2004, 23:225-244.
10. Blasini A.M., Brundula V., París M., Rivas L., Salazar S., Stekman I.L., Rodriguez M.A. Protein tyrosine kinase activity in T lymphocytes from patients with systemic lupus erythematosus. J. Autoimmun. 1998, 11(5):387-393.
11. Vassilopoulos D., Kovacs B., Tsokos G.C. TCR/CD3 complex-mediated signal transduction pathway in T cells and T cell lines from patients with systemic lupus erythematosus. J. Immunol. 1995, 155(4):2269-2281.
12. Cedeño S., Cifarelli D.F., Blasini A.M., París M., Placeres F., Alonso G., Rodriguez M.A. Defective activity of ERK-1 and ERK-2 mitogen activated protein kinases in peripheral blood T lymphocytes from patients with systemic lupus erythematosus: potential role of altered coupling of Ras guanine nucleotide exchange factor hSos to adapter protein Grb2 in lupus T cells. Clin. Immunol. 2003, 106(1):41-49.
13. Solomou E.E., Yuang Y.T., Gourley M.F., Kammer G.M., Tsokos G.C. Molecular basis of deficient IL-2 production in T cells from patients with systemic lupus erythematosus. J. Immunol. 2001, 166:4216-4222.
14. Graninger W.B., Steiner C.W., Graninger M.T., Aringer M., Smolen J.S. Cytokine regulation of apoptosis and Bcl-2 expression in lymphocytes of patients with systemic lupus erythematosus. Cell Death Differ. 2000, 7(10):966-972.
15. Blasini A.M., Rodríguez M.A. Altered signaling triggered by ligation of the TCR/CD3 receptor in T lymphocytes from patients with systemic lupus erythematosus: the road from anergy to autoimmunity. Int. Rev. Immunol. 2004, 23(3-4):265-272.
16. Balagopalan L., Coussens N.P., Sherman E., Samelson L.E., Sommers C.L. The LAT story: a tale of cooperativity, coordination, and choreography. Cold Spring Harb. Perspect. Biol. 2010, 2(8):a005512.
17. Zhang W., Trible R.P., Samelson L.E. LAT palmitoylation: its essential role in membrane microdomains targeting and tyrosine phosphorylation during the T cell activation. Immunity 1998, 9:239-246.
18. Zhang W., Irvin B.J., Trible R.P., Abraham R.T., Samelson L.E. Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int. Immunol. 1999, 11(6):943-950.
19. Xavier R., Brennan T., Li Q., McCormack C., Seed B. Membrane compartmentation is required for efficient T cell activation. Immunity 1998, 8(6):723-732.
20. Kabouridis P.S., Janzen J., Magee A.L., Ley S.C. Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur. J. Immunol. 2000, 30(3):954-963.
21. Drevot P., Langlet C., Guo X.J., Bernard A.M., Colard O., Chauvin J.P., Lasserre R., He H.T. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 2002, 21(8):1899-1908.
22. Janes P.W., Ley S.C., Magee A.I., Kabouridis P.S. The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin. Immunol. 2000, 12(1):23-34.
23. Deng G.M., Tsokos G.C. Cholera toxin B accelerates disease progression in lupus-prone mice by promoting lipid raft aggregation. J. Immunol. 2008, 181(6):4019-4026.
24. Fukumoto R., Dundr M., Nicot C., Adams A., Valeri V.W., Samelson L.E., Franchini G. Inhibition of T-cell receptor signal transduction and viral expression by the linker for activation of T cells-interacting p12(I) protein of human T-cell leukemia/lymphoma virus type 1. J. Virol. 2007, 81(17):9088-9099.
25. Jury E.C., Isenberg D.A., Mauri C., Ehrenstein M.R. Atorvastatin restores Lck expression and lipid raft-associated signaling in T cells from patients with systemic lupus erythematosus. J. Immunol. 2006, 177(10):7416-7422.
26. Dykstra M., Cherukuri A., Sohn H.W., Tzeng S.J., Pierce S.K. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 2003, 21:457-481.
27. Paz P.E., Wang S., Clarke H., Lu X., Stokoe D., Abo A. Mapping the Zap-70 phosphorylation sites on LAT (linker for activation of T cells) required for recruitment and activation of signalling proteins in T cells. Biochem. J. 2001, 356(Pt 2):461-471.
28. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J., Rothfield N.F., Schaller J.G., Talal N., Winchester R.J. The 1982 revised criteria for the classification of systemic lupus erythemathosus. Arthritis Rheum. 1998, 25(11):1271-1277.
29. Zhu M., Janssen E., Zhang W. Minimal requirement of tyrosine residues of linker for activation of T cells in TCR signaling and thymocyte development. J. Immunol. 2003, 170(1):325-333.
30. Jiang Y., Cheng H. Evidence of LAT as a dual substrate for Lck and Syk in T lymphocytes. Leuk. Res. 2007, 31(4):541-545.
31. Dustin M.L. Membrane domains and the immunological synapse: keeping T cells resting and ready. J. Clin. Invest. 2002, 109(2):155-160.
32. Jordan S., Rodgers W. T cell glycolipid-enriched membrane domains are constitutively assembled as membrane patches that translocate to immune synapses. J. Immunol. 2003, 171(1):78-87.
33. Nicolaou S.A., Szigligeti P., Neumeier L., Lee S.M., Duncan H.J., Kant S.K., Mongey A.B., Filipovich A.H., Conforti L. Altered dynamics of Kv1.3 channel compartmentalization in the immunological synapse in systemic lupus erythematosus. J. Immunol. 2007, 179(1):346-356.
34. Flores-Borja F., Jury E.C., Mauri C., Ehrenstein M.R. Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(49):19396-19401.
35. Dong S., Corre B., Foulon E., Dufour E., Veillette A., Acuto O., Michel F. T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2. J. Exp. Med. 2006, 203(11):2509-2518.
36. Sommers C.L., Park C.S., Lee J., Feng C., Fuller C.L., Grinberg A., Hildebrand J.A., Lacaná E., Menon R.K., Shores E.W., Samelson L.E., Love P.E. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 2002, 296(5575):2040-2043.
37. Clarke R.L., Thiemann S., Refaeli Y., Werlen G., Potter T.A. A new function for LAT and CD8 during CD8-mediated apoptosis that is independent of TCR signal transduction. Eur. J. Immunol. 2009, 39(6):1619-1631.
38. Tanimura N., Nagafuku M., Minaki Y., Umeda Y., Hayashi F., Sakakura J., Kato A., Liddicoat D.R., Ogata M., Hamaoka T., Kosugi A. Dynamic changes in the mobility of LAT in aggregated lipid rafts upon T cell activation. J. Cell Biol. 2003, 160(1):125-135.
39. Krishnan S., Nambiar M.P., Warke V.G., Fisher C.U., Mitchell J., Delaney N., Tsokos G.C. Alterations in lipid raft composition and dynamics contribute to abnormal T cell responses in systemic lupus erythematosus. J. Immunol. 2004, 172(12):7821-7831.
40. Jury E.C., Kabouridis P.S., Flores-Borja F., Mageed R.A., Isenberg D.A. Altered lipid raft-associated signaling and ganglioside expression in T lymphocytes from patients with systemic lupus erythematosus. J. Clin. Invest. 2004, 113(8):1176-1187.
41. Flores-Borja F., Kabouridis P.S., Jury E.C., Isenberg D.A., Mageed R.A. Decreased Lyn expression and translocation to lipid raft signaling domains in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 2005, 52(12):3955-3965.
42. Zeyda M., Staffler G., Horejsi V., Waldhausl W., Stulnig T.M. LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J. Biol. Chem. 2002, 277(32):28418-28423.
43. Bonello G., Blanchard N., Montoya M.C., Aguado E., Langlet C., He H.T., Nunez-Cruz S., Malissen M., Sanchez-Madrid F., Olive D., Hivroz C., Collette Y. Dynamic recruitment of the adaptor protein LAT: LAT exists in two distinct intracellular pools and controls its own recruitmentm. J. Cell Sci. 2004, 117(7):1009-1016.
44. Balagopalan L., Barr V.A., Sommers C.L., Barda-Saad M., Goyal A., Isakowitz M.S., Samelson L.E. c-Cbl-Mediated regulation of LAT-nucleated signaling complexes. Mol. Cell. Biol. 2007, 27(24):8622-8636.
45. Kuhné M.R., Lin J., Yablonski D., Mollenauer M.N., Ehrlich L.I., Huppa J., Davis M.M., Weiss A. Linker for activation of T cells, zeta-associated protein-70, and Src homology 2 domain-containing leukocyte protein-76 are required for TCR-induced microtubule-organizing center polarization. J. Immunol. 2003, 171(2):860-866.
46. Brignatz C., Restouin A., Bonello G., Olive D., Collette Y. Evidences for ubiquitination and intracellular trafficking of LAT, the linker of activated T cells. Biochim. Biophys. Acta 2005, 1746(2):108-115.
47. Balagopalan L., Barr V.A., Samelson L.E. Endocytic events in TCR signaling: focus on adapters in microclusters. Immunol. Rev. 2009, 232(1):84-98.
48. Fernandez D.R., Telarico T., Bonilla E., Li Q., Banerjee S., Middleton F.A., Phillips P.E., Crow M.K., Oess S., Muller-Esterl W., Perl A. Activation of mammalian target of rapamycin controls the loss of TCRzeta in lupus T cells through HRES-1/Rab4-regulated lysosomal degradation. J. Immunol. 2009, 182(4):2063-2073.
49. Finco T.S., Justice-Healy G.E., Patel S.J., Hamilton V.E. Regulation of the human LAT gene by the Elf-1 transcription factor. BMC Mol. Biol. 2006, 7:4.
50. Juang Y.T., Tenbrock K., Nambiar M.P., Gourley M.F., Tsokos G.C. Defective production of functional 98-kDa form of Elf-1 is responsible for the decreased expression of TCR zeta-chain in patients with systemic lupus erythematosus. J. Immunol. 2002, 169(10):6048-6055.