Inhibition of IL-2 inducible T-cell kinase alleviates T-cell activation and murine myocardial inflammation associated with CVB3 infection

Molecular Immunology

Volumn 59, Issue 1, 2014, Pages 30-38

  He, Feng ^a   Yao, Hailan ^a   Xiao, Zonghui ^a   Han, Jisheng ^b   Zou, Jizhen ^a   Liu, Zhewei ^a  

^a CAPITAL INSTITUTE OF PEDIATRICS   (China)

^b Aerospace 731 Hospital   (China)

Author keywords

Coxsackievirus B3; ITK; Myocarditis; RNAi

Indexed keywords

CYTOKINE; IL 2 INDUCIBLE T CELL KINASE; PHOSPHOTRANSFERASE; PLASMID VECTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR GENE THERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; ENZYME INHIBITION; GENETIC TRANSFECTION; HEART INJURY; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL LINE; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPLEEN CELL; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION; VIRUS MYOCARDITIS;

COXSACKIEVIRUS B3; ITK; MYOCARDITIS; RNAI;

ANIMALS; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; COXSACKIEVIRUS INFECTIONS; CYTOKINES; ENTEROVIRUS B, HUMAN; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; HUMANS; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MYOCARDITIS; PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; SPLEEN; SURVIVAL ANALYSIS; T-LYMPHOCYTES;

EID: 84892850462     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.12.004     Document Type: Article

References (33)

1. Bachmann M.F., Littman D.R., Liao X.C. Antiviral immune responses in Itk-deficient mice. J. Virol. 1997, 71:7253-7257.
2. Berg L.J., Finkelstein L.D., Lucas J.A., Schwartzberg P.L. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 2005, 23:549-600.
3. Esfandiarei M., McManus B.M. Molecular biology and pathogenesis of viral myocarditis. Annu. Rev. Pathol. 2008, 3:127-155.
4. Fan K., Jia Y., Wang S., Li H., Wu D., Wang G., Chen J.L. Role of Itk signalling in the interaction between influenza A virus and T-cells. J. Gen. Virol. 2012, 93:987-997.
5. Ferrara T.J., Mueller C., Sahu N., Ben-Jebria A., August A. Reduced airway hyperresponsiveness and tracheal responses during allergic asthma in mice lacking tyrosine kinase inducible T-cell kinase. J. Allergy Clin. Immunol. 2006, 117:780-786.
6. Gibson S., August A., Kawakami Y., Kawakami T., Dupont B., Mills G.B. The EMT/ITK/TSK (EMT) tyrosine kinase is activated during TCR signaling: LCK is required for optimal activation of EMT. J. Immunol. 1996, 156:2716-2722.
7. Grasis J.A., Browne C.D., Tsoukas C.D. Inducible T cell tyrosine kinase regulates actin-dependent cytoskeletal events induced by the T cell antigen receptor. J. Immunol. 2003, 170:3971-3976.
8. Han T., Zhao K., Wu C., Lu H., Song D., He W., Gao F. Viral kinetics are associated with changes in cytokines and chemokines in serum and target organs of SSM-CVB3-infected macaques. Exp. Mol. Pathol. 2013, 94:174-181.
9. Heim A., Weiss S. Interferons in enteroviral heart disease: modulation of cytokine expression and antiviral activity. Med. Microbiol. Immunol. 2004, 193:149-154.
10. Huber S. T cells in coxsackievirus-induced myocarditis. Viral Immunol. 2004, 17:152-164.
11. Huber S., Shi C., Budd R.C. Gammadelta T cells promote a Th1 response during coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J. Virol. 2002, 76:6487-6494.
12. Khurana D., Arneson L.N., Schoon R.A., Dick C.J., Leibson P.J. Differential regulation of human NK cell-mediated cytotoxicity by the tyrosine kinase Itk. J. Immunol. 2007, 178:3575-3582.
13. Li X., Zheng L., Peng F., Qi C., Zhang X., Zhou A., Liu Z., Wu S. Recombinant thymosin beta 4 can promote full-thickness cutaneous wound healing. Protein Exp. Purif. 2007, 56:229-236.
14. Liao X.C., Fournier S., Killeen N., Weiss A., Allison J.P., Littman D.R. Itk negatively regulates induction of T cell proliferation by CD28 costimulation. J. Exp. Med. 1997, 186:221-228.
15. Lin T.A., McIntyre K.W., Das J., Liu C., O'Day K.D., Penhallow B., Hung C.Y., Whitney G.S., Shuster D.J., Yang X., Townsend R., Postelnek J., Spergel S.H., Lin J., Moquin R.V., Furch J.A., Kamath A.V., Zhang H., Marathe P.H., Perez-Villar J.J., Doweyko A., Killar L., Dodd J.H., Barrish J.C., Wityak J., Kanner S.B. Selective Itk inhibitors block T-cell activation and murine lung inflammation. Biochemistry 2004, 43:11056-11062.
16. Lodge P.A., Herzum M., Olszewski J., Huber S.A. Coxsackievirus B-3 myocarditis. Acute and chronic forms of the disease caused by different immunopathogenic mechanisms. Am. J. Pathol. 1987, 128:455-463.
17. Lundgren M., Darnerud P.O., Blomberg J., Friman G., Ilback N.G. Sequential changes in serum cytokines reflect viral RNA kinetics in target organs of a Coxsackievirus B infection in mice. J. Clin. Immunol. 2009, 29:611-619.
18. Luppi P., Rudert W., Licata A., Riboni S., Betters D., Cotrufo M., Frati G., Condorelli G., Trucco M. Expansion of specific alphabeta+ T-cell subsets in the myocardium of patients with myocarditis and idiopathic dilated cardiomyopathy associated with Coxsackievirus B infection. Hum. Immunol. 2003, 64:194-210.
19. Miller A.T., Wilcox H.M., Lai Z., Berg L.J. Signaling through Itk promotes T helper 2 differentiation via negative regulation of T-bet. Immunity 2004, 21:67-80.
20. Mueller C., August A. Attenuation of immunological symptoms of allergic asthma in mice lacking the tyrosine kinase ITK. J. Immunol. 2003, 170:5056-5063.
21. Readinger J.A., Schiralli G.M., Jiang J.K., Thomas C.J., August A., Henderson A.J., Schwartzberg P.L. Selective targeting of ITK blocks multiple steps of HIV replication. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6684-6689.
22. Robert V., Triffaux E., Savignac M., Pelletier L. Calcium signaling in T lymphocytes. Med. Sci. (Paris) 2012, 28:773-779.
23. Schaeffer E.M., Debnath J., Yap G., McVicar D., Liao X.C., Littman D.R., Sher A., Varmus H.E., Lenardo M.J., Schwartzberg P.L. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 1999, 284:638-641.
24. Schaeffer E.M., Yap G.S., Lewis C.M., Czar M.J., McVicar D.W., Cheever A.W., Sher A., Schwartzberg P.L. Mutation of Tec family kinases alters T helper cell differentiation. Nat. Immunol. 2001, 2:1183-1188.
25. Seko Y., Takahashi N., Yagita H., Okumura K., Yazaki Y. Expression of cytokine mRNAs in murine hearts with acute myocarditis caused by coxsackievirus b3. J. Pathol. 1997, 183:105-108.
26. Tam P.E. Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol. 2006, 19:133-146.
27. Van Houten N., Huber S.A. Genetics of Coxsackie B3 (CVB3) myocarditis. Eur. Heart J. 1991, 12(Suppl. D):108-112.
28. van Oers N.S., Killeen N., Weiss A. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 1996, 183:1053-1062.
29. von Bonin A., Rausch A., Mengel A., Hitchcock M., Kruger M., von Ahsen O., Merz C., Rose L., Stock C., Martin S.F., Leder G., Docke W.D., Asadullah K., Zugel U. Inhibition of the IL-2-inducible tyrosine kinase (Itk) activity: a new concept for the therapy of inflammatory skin diseases. Exp. Dermatol. 2011, 20:41-47.
30. Yao H., Zhang Y., He F., Wang C., Xiao Z., Zou J., Wang F., Liu Z. Short hairpin RNA targeting 2B gene of coxsackievirus B3 exhibits potential antiviral effects both in vitro and in vivo. BMC Infect. Dis. 2012, 12:177.
31. Yuan J., Cheung P.K., Zhang H.M., Chau D., Yang D. Inhibition of coxsackievirus B3 replication by small interfering RNAs requires perfect sequence match in the central region of the viral positive strand. J. Virol. 2005, 79:2151-2159.
32. Yue Y., Gui J., Xu W., Xiong S. Gene therapy with CCL2 (MCP-1) mutant protects CVB3-induced myocarditis by compromising Th1 polarization. Mol. Immunol. 2011, 48:706-713.
33. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., Samelson L.E. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998, 92:83-92.