A deficient translocation of CD3ζ, ZAP-70 and Grb2 to lipid raft, as a hallmark of defective adaptive immune response during chronic hepatitis B infection

Cellular Immunology

Volumn 284, Issue 1-2, 2013, Pages 9-19

  Barboza, Luisa ^a   Salmen, Siham ^a   Teran Angel, Guillermo ^a   Peterson, Darrell L ^b   Berrueta, Lisbeth ^a  

^a UNIVERSIDAD DE LOS ANDES   (Venezuela)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Cell signaling; Hepatitis B; Lipid rafts; Signalosome; T cell

Indexed keywords

CD3 ANTIGEN; CD3 ZETA ANTIGEN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; PROTEIN KINASE ZAP 70; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; HEPATITIS B; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIPID RAFT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

CELL SIGNALING; HEPATITIS B; LIPID RAFTS; SIGNALOSOME; T CELL;

ADAPTIVE IMMUNITY; ANTIGENS, CD3; FLOW CYTOMETRY; GRB2 ADAPTOR PROTEIN; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; LEUKOCYTES, MONONUCLEAR; MEMBRANE MICRODOMAINS; MICROSCOPY, FLUORESCENCE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, VIRAL; SPHINGOLIPID ACTIVATOR PROTEINS; T-LYMPHOCYTES; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84881293461     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2013.05.008     Document Type: Article

References (64)

1. MacLeod M.K., Kappler J.W., Marrack P. Memory CD4 T cells: generation, reactivation and re-assignment. Immunology 2010, 130:10-15.
2. Smith-Garvin J.E., Koretzky G.A., Jordan M.S. T cell activation. Annu. Rev. Immunol. 2009, 27:591-619.
3. Grakoui A., Bromley S.K., Sumen C., Davis M.M., Shaw A.S., Allen P.M., Dustin M.L. The immunological synapse: a molecular machine controlling T cell activation. Science 1999, 285:221-227.
4. Monks C.R., Freiberg B.A., Kupfer H., Sciaky N., Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998, 395:82-86.
5. 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, 12:23-34.
6. Schade A.E., Levine A.D. Lipid raft heterogeneity in human peripheral blood T lymphoblasts: a mechanism for regulating the initiation of TCR signal transduction. J. Immunol. 2002, 168:2233-2239.
7. Viola A., Schroeder S., Sakakibara Y., Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999, 283:680-682.
8. Clements J., Boerth N., Lee J., Koretzky G. Integration of T cell receptor-dependent signaling pathways by adapter proteins. Ann. Rev. Immunol. 1999, 17:89.
9. Asada H., Ishii N., Sasaki Y., Endo K., Kasai H., Tanaka N., Takeshita T., Tsuchiya S., Konno T., Sugamura K. Grf40, A novel Grb2 family member, is involved in T cell signaling through interaction with SLP-76 and LAT. J. Exp. Med. 1999, 189:1383-1390.
10. Shi Y.H., Shi C.H. Molecular characteristics and stages of chronic hepatitis B virus infection. World J. Gastroenterol. 2009, 15:3099-3105.
11. Lok A.S., McMahon B.J. Chronic hepatitis B. Hepatology 2007, 45:507-539.
12. Boni C., Fisicaro P., Valdatta C., Amadei B., Di Vincenzo P., Giuberti T., Laccabue D., Zerbini A., Cavalli A., Missale G., Bertoletti A., Ferrari C. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J. Virol. 2007, 81:4215-4225.
13. Lu Y.W., Tan T.L., Zhang J., Chen W.N. Cellular apoptosis induced by replication of hepatitis B virus: possible link between viral genotype and clinical outcome. Virol. J. 2007, 4:117.
14. Rehermann B., Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 2005, 5:215-229.
15. Bertoletti A., Costanzo A., Chisari F.V., Levrero M., Artini M., Sette A., Penna A., Giuberti T., Fiaccadori F., Ferrari C. Cytotoxic T lymphocyte response to a wild type hepatitis B virus epitope in patients chronically infected by variant viruses carrying substitutions within the epitope. J. Exp. Med. 1994, 180:933-943.
16. Ferrari C., Penna A., Bertoletti A., Valli A., Antoni A., Giuberti T., Cavalli A., Petit M., Fiaccadori F. Cellular immune response to Hepatitis B virus-encoded antigens in acute and chronic Hepatitis B virus infection. J. Immunol. 1990, 145:3442-3449.
17. Jung M., Hartmann B., Tilman J., Diepolder H., Gruber R., Schraut W., Gruner N., Zachoval R., Hoffmann R., Santantonio T., Wachtler M., Rudolf G. Virus-specific lymphokine production differs quantitatively but not qualitatively in acute and chronic hepatitis B infection. Virology 1999, 261:165-172.
18. Sobao Y., Tomiyama H., Sugi K., Tokunaga M., Ueno T., Saito S., Fujiyama S., Morimoto M., Tanaka K., Takiguchi M. The role of hepatitis B virus-specific memory CD8 T cells in the control of viral replication. J. Hepatol. 2002, 36:105-115.
19. Beckebaum S., Cicinnati V., Zhang X., Ferencik S., Frilling A., Grosse-Wilde H., Broelsch C., Gerken G. Hepatitis B virus-induced defect of monocyte-derived dendritic cells leads to impaired T helper type 1 response in vitro: mechanisms for viral immune escape. Immunology 2003, 109:487-495.
20. Chen S., Akbar S.M., Abe M., Hiasa Y., Onji M. Immunosuppressive functions of hepatic myeloid-derived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin. Exp. Immunol. 2011, 166:134-142.
21. Milich D.R. Influence of T-helper cell subsets and crossregulation in hepatitis B virus infection. J. Viral Hepat. 1997, 4(Suppl. 2):48-59.
22. Jiang Y., Ma Z., Xin G., Yan H., Li W., Xu H., Hao C., Niu J., Zhao P. Th1 and Th2 immune response in chronic hepatitis B patients during a long-term treatment with adefovir dipivoxil. Mediators Inflamm. 2010, 143026.
23. Sun H.Q., Zhang J.Y., Zhang H., Zou Z.S., Wang F.S., Jia J.H. Increased Th17 cells contribute to disease progression in patients with HBV-associated liver cirrhosis. J. Viral Hepat. 2012, 19:396-403.
24. Chen M., Sallberg M., Hughes J., Jones J., Guidotti L.G., Chisari F.V., Billaud J.N., Milich D.R. Immune tolerance split between hepatitis B virus precore and core proteins. J. Virol. 2005, 79:3016-3027.
25. Reignat S., Webster G., Brown D., Ogg G., King A., Seneviratne S., Dusheiko G., Williams R., Maini M., Bertoletti A. Escaping high viral load exhaustion: CD8 cells with altered tetramer binding in chronic hepatitis B virus infection. J. Exp. Med. 2002, 195:1089-1101.
26. Vahlenkamp T.W., Tompkins M.B., Tompkins W.A. The role of CD4+CD25+ regulatory T cells in viral infections. Vet. Immunol. Immunopathol. 2005, 108:219-225.
27. Barboza L., Salmen S., Goncalves L., Colmenares M., Peterson D., Montes H., Cartagirone R., Gutierrez M.D., Berrueta L. Antigen-induced regulatory T cells in HBV chronically infected patients. Virology 2007, 368:41-49.
28. Stoop J.N., van der Molen R.G., Baan C.C., van der Laan L.J., Kuipers E.J., Kusters J.G., Janssen H.L. Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. Hepatology 2005, 41:771-778.
29. Zhang M., Zhou J., Zhao T., Huang G., Tan Y., Tan S., Fu X., Niu W., Meng G., Chen X., Shang X., Liu D., Ni B., Wang L., Wu Y. Dissection of a circulating and intrahepatic CD4(+)Foxp3(+) T-cell subpopulation in chronic hepatitis B virus (HBV) infection: a highly informative strategy for distinguishing chronic HBV infection states. J. Infect. Dis. 2012, 205:1111-1120.
30. Velazquez D., Milano M., Petrosino P., Sotolongo A., Barboza L., Salmen S., Berrueta L. Características fenotípicas de células T linfocitarias de tipo regulador (Treg) presentes en el hígado de pacientes con infección crónica por VHB. Avan. Biomed. 2012, 1:60-67.
31. Barboza L., Salmen S., Peterson D.L., Montes H., Colmenares M., Hernandez M., Berrueta-Carrillo L.E., Berrueta L. Altered T cell costimulation during chronic hepatitis B infection. Cell. Immunol. 2009, 257:61-68.
32. Schodel F., Moriarty A.M., Peterson D.L., Zheng J.A., Hughes J.L., Will H., Leturcq D.J., McGee J.S., Milich D.R. The position of heterologous epitopes inserted in hepatitis B virus core particles determines their immunogenicity. J. Virol. 1992, 66:106-114.
33. Colligan J.E. Biochemistry of cell activation. Short Protocols in Immunology: A Compendium of Methods from Currents Protocols in Immunology 2005, John Wiley & Sons.
34. 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, 177:7416-7422.
35. Ren D., Wang F., He X., Jiang L., Li D., Ying H., Sun S. Construction of bioactive chimeric MHC class I tetramer by expression and purification of human-murine chimeric MHC heavy chain and beta(2)m as a fusion protein in Escherichia coli. Protein Expr. Purif. 2006, 50:171-178.
36. Tavano R., Gri G., Molon B., Marinari B., Rudd C.E., Tuosto L., Viola A. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J. Immunol. 2004, 173:5392-5397.
37. Xu S., Huo J., Tan J.E., Lam K.P. Cbp deficiency alters Csk localization in lipid rafts but does not affect T-cell development. Mol. Cell. Biol. 2005, 25:8486-8495.
38. Bunnell S.C., Hong D.I., Kardon J.R., Yamazaki T., McGlade C.J., Barr V.A., Samelson L.E. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 2002, 158:1263-1275.
39. Roncagalli R., Mingueneau M., Gregoire C., Langlet C., Malissen B., Malissen M. Lymphoproliferative disorders involving T helper effector cells with defective LAT signalosomes. Semin. Immunopathol. 2010, 32:117-125.
40. Muhlbauer M., Fleck M., Schutz C., Weiss T., Froh M., Blank C., Scholmerich J., Hellerbrand C. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J. Hepatol. 2006, 45:520-528.
41. Zhang Z., Jin B., Zhang J.Y., Xu B., Wang H., Shi M., Wherry E.J., Lau G.K., Wang F.S. Dynamic decrease in PD-1 expression correlates with HBV-specific memory CD8 T-cell development in acute self-limited hepatitis B patients. J. Hepatol. 2009, 50:1163-1173.
42. Sheppard K.A., Fitz L.J., Lee J.M., Benander C., George J.A., Wooters J., Qiu Y., Jussif J.M., Carter L.L., Wood C.R., Chaudhary D. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett. 2004, 574:37-41.
43. Gonzalez P.A., Prado C.E., Leiva E.D., Carreno L.J., Bueno S.M., Riedel C.A., Kalergis A.M. Respiratory syncytial virus impairs T cell activation by preventing synapse assembly with dendritic cells. Proc. Natl. Acad. Sci. USA 2008, 105:14999-15004.
44. Nyakeriga A.M., Fichtenbaum C.J., Goebel J., Nicolaou S.A., Conforti L., Chougnet C.A. Engagement of the CD4 receptor affects the redistribution of Lck to the immunological synapse in primary T cells: implications for T-cell activation during human immunodeficiency virus type 1 infection. J. Virol. 2009, 83:1193-1200.
45. Tran-Van H., Avota E., Bortlein C., Mueller N., Schneider-Schaulies S. Measles virus modulates dendritic cell/T-cell communication at the level of plexinA1/neuropilin-1 recruitment and activity. Eur. J. Immunol. 2011, 41:151-163.
46. Fackler O.T., Alcover A., Schwartz O. Modulation of the immunological synapse: a key to HIV-1 pathogenesis?. Nat. Rev. Immunol. 2007, 7:310-317.
47. Simons K., Ehehalt R. Cholesterol, lipid rafts, and disease. J. Clin. Invest. 2002, 110:597-603.
48. Kusumi A., Ike H., Nakada C., Murase K., Fujiwara T. Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules. Semin. Immunol. 2005, 17:3-21.
49. 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, 172:7821-7831.
50. Ise W., Nakamura K., Shimizu N., Goto H., Fujimoto K., Kaminogawa S., Hachimura S. Orally tolerized T cells can form conjugates with APCs but are defective in immunological synapse formation. J. Immunol. 2005, 175:829-838.
51. Zhang W., Trible R.P., Samelson L.E. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 1998, 9:239-246.
52. DeFord-Watts L.M., Dougall D.S., Belkaya S., Johnson B.A., Eitson J.L., Roybal K.T., Barylko B., Albanesi J.P., Wulfing C., van Oers N.S. The CD3 zeta subunit contains a phosphoinositide-binding motif that is required for the stable accumulation of TCR-CD3 complex at the immunological synapse. J. Immunol. 2011, 186:6839-6847.
53. Samelson L.E. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 2002, 20:371-394.
54. Yokosuka T., Sakata-Sogawa K., Kobayashi W., Hiroshima M., Hashimoto-Tane A., Tokunaga M., Dustin M.L., Saito T. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 2005, 6:1253-1262.
55. Saito T., Yokosuka T., Hashimoto-Tane A. Dynamic regulation of T cell activation and co-stimulation through TCR-microclusters. FEBS Lett. 2010, 584:4865-4871.
56. Chiodetti L., Choi S., Barber D.L., Schwartz R.H. Adaptive tolerance and clonal anergy are distinct biochemical states. J. Immunol. 2006, 176:2279-2291.
57. Chuck M.I., Zhu M., Shen S., Zhang W. The role of the LAT-PLC-gamma1 interaction in T regulatory cell function. J. Immunol. 2010, 184:2476-2486.
58. Koonpaew S., Shen S., Flowers L., Zhang W. LAT-mediated signaling in CD4+CD25+ regulatory T cell development. J. Exp. Med. 2006, 203:119-129.
59. Stoop J.N., van der Molen R.G., Kuipers E.J., Kusters J.G., Janssen H.L. Inhibition of viral replication reduces regulatory T cells and enhances the antiviral immune response in chronic hepatitis B. Virology 2007, 361:141-148.
60. Xu D., Fu J., Jin L., Zhang H., Zhou C., Zou Z., Zhao J.M., Zhang B., Shi M., Ding X., Tang Z., Fu Y.X., Wang F.S. Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J. Immunol. 2006, 177:739-747.
61. Kittlesen D.J., Chianese-Bullock K.A., Yao Z.Q., Braciale T.J., Hahn Y.S. Interaction between complement receptor gC1qR and hepatitis C virus core protein inhibits T-lymphocyte proliferation. J. Clin. Invest. 2000, 106:1239-1249.
62. Yao Z.Q., Eisen-Vandervelde A., Waggoner S.N., Cale E.M., Hahn Y.S. Direct binding of hepatitis C virus core to gC1qR on CD4+ and CD8+ T cells leads to impaired activation of Lck and Akt. J. Virol. 2004, 78:6409-6419.
63. Yao Z.Q., King E., Prayther D., Yin D., Moorman J. T cell dysfunction by hepatitis C virus core protein involves PD-1/PDL-1 signaling. Viral Immunol. 2007, 20:276-287.
64. Schweneker M., Favre D., Martin J.N., Deeks S.G., McCune J.M. HIV-induced changes in T cell signaling pathways. J. Immunol. 2008, 180:6490-6500.