Characterization of a novel interaction between transcription factor TFII-I and the inducible tyrosine kinase in T cells

European Journal of Immunology

Volumn 39, Issue 9, 2009, Pages 2584-2595

  Sacristán, Catarina ^a,d   Schattgen, Stefan A ^b   Berg, Leslie J ^b   Bunnell, Stephen C ^c   Roy, Ananda L ^c   Rosenstein, Yvonne ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Co stimulation; Inducible tyrosine kinase; T cell receptors; T cell signaling; Transcription factor TFII I

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; INDUCIBLE TYROSINE KINASE; LEUKOSIALIN; PLECKSTRIN; PROLINE; PROTEIN C FOS; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR II 1; UNCLASSIFIED DRUG; EMT PROTEIN TYROSINE KINASE; EMT PROTEIN-TYROSINE KINASE; GTF2I PROTEIN, HUMAN; SPN PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION; ANIMAL; B LYMPHOCYTE; GENETICS; IMMUNOLOGY; LEUKEMIA CELL LINE; METABOLISM; ONCOGENE; PHOSPHORYLATION; PROMOTER REGION; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD28; ANTIGENS, CD3; ANTIGENS, CD43; B-LYMPHOCYTES; GENES, FOS; HUMANS; JURKAT CELLS; MICE; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN-TYROSINE KINASES; T-LYMPHOCYTES; TRANSCRIPTION FACTORS, TFII;

EID: 70349232884     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200839031     Document Type: Article

References (48)

1. Berg, L. J., Finkelstein, L. D., Lucas, J. A. and Schwartzberg, P. L., Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 2005. 23: 549-600.
2. + T-cell development. Nat. Rev. Immunol. 2007. 7: 479-485.
3. Felices, M., Berg, L. J., The Tec kinases Itk and Rlk regulate NKT cell maturation, cytokine production, and survival. J. Immunol. 2008. 180: 3007-3018.
4. Tsukada, S., Saffran, D. C., Rawlings, D. J., Parolini, O., Allen, R. C., Klisak, I., Sparkes, R. S. et al., Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell 1993. 72: 279-290. (Pubitemid 23044942)
5. Vetrie, D., Vorechovsky, I., Sideras, P., Holland, J., Davies, A., Flinter, F., Hammarstrom, L. et al., The gene involved in X-linked agammaglobulinemia is a member of the src family of protein-tyrosine kinases. Nature 1993. 361: 226-233. (Pubitemid 23034471)
6. Rawlings, D. J., Saffran, D. C., Tsukada, S., Largaespada, D. A., Grimaldi, J. C., Cohen, L., Mohr, R. N. et al., Mutation of the unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 1993. 261: 358-361. (Pubitemid 23281007)
7. Thomas, J. D., Sideras, P., Smith, C. I. E., Vorechovsky, I., Chapman, V. and Paul,W. E., Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science 1993. 261: 355-358. (Pubitemid 23281006)
8. Yang, W. and Desiderio, S., BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl. Acad. Sci. USA 1997. 94: 604-609.
9. Novina, C. D., Kumar, S., Bajpai, U., Cheriyath, V., Zhang, K., Pillai, S., Wortis, H. H. and Roy, A. L., Regulation of nuclear localization and transcriptional activity of TFII-I by Bruton's tyrosine kinase. Mol. Cell. Biol. 1999. 19: 5014-5024.
10. Egloff, A. M. and Desiderio, S., Identification of phosphorylation sites for Bruton's tyrosine kinase within the transcriptional regulator BAP/TFII-I. J. Biol. Chem. 2001. 276: 27806-27815.
11. Sacristán, C., Tussié-Luna, M. I., Logan, S. M., Roy, A. L., Mechanism of Btk-mediated recruitment and regulation of TFII-I. J. Biol. Chem. 2004. 279: 7147-7158.
12. Cheriyath, V., Desgranges, Z. P. and Roy, A. L., c-Src dependent transcriptional activation of TFII-I. J. Biol. Chem. 2002. 277: 22798-22805.
13. Roy, A. L., Meisterernst, M., Pognonec, P. and Roeder, R. G., Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature 1991. 354: 245-248. (Pubitemid 21896825)
14. Roy, A. L., Carruthers, C., Gutjahr, T. and Roeder, R. G., Direct role for Myc in transcription initiation mediated by interactions with TFII-I. Nature 1993. 365: 359-361. (Pubitemid 23288980)
15. Cheriyath, V., Novina, C. D. and Roy, A. L., TFII-I regulates Vbeta promoter activity through an initiator element. Mol. Cell. Biol. 1998. 18: 4444-4454.
16. Hakre, S., Tussie-Luna, M. I., Ashworth, T., Novina, C. D., Settleman, J., Sharp, P. A. and Roy, A. L., Opposing functions of TFII-I spliced Isoforms in growth factor-induced gene expression. Mol. Cell 2006. 24: 301-308. (Pubitemid 44557127)
17. Caraveo, G., van Rossum, D. B., Patterson, R. L., Snyder, S. H. and Desiderio, S., Action of TFII-I outside the nucleus as an inhibitor of agonist-induced calcium entry. Science 2006. 314: 122-125. (Pubitemid 44547755)
18. Ashworth, T. and Roy, A. L., TFII-I controls B cell proliferation via regulating NF-kappaB. J. Immunol. 2007. 178: 2631-2635.
19. Kim, D.-W., Cheriyath, V., Roy, A. L. and Cochran, B. H., TFII-I enhances activation of the c-fos promoter through interactions with upstream elements. Mol. Cell. Biol. 1998. 18: 3310-3320.
20. Kim, D.-W. and Cochran, B. H., JAK2 activates TFII-I and regulates its interaction with extracellular signal-regulated kinase. Mol. Cell. Biol. 2001. 21: 3387-3397.
21. Crusselle-Davis, V. J., Vieira, K. F., Zhou, Z., Anantharaman, A. and Bungert, J., Antagonistic regulation of beta-globin gene expression by helix-loop-helix proteins USF and TFII-I. Mol. Cell. Biol. 2006. 26: 6832-6843.
22. Ogura, Y., Azuma, M., Tsuboi, Y., Kabe, Y., Yamaguchi, Y., Wada, T., Watanabe, H. and Handa, H., TFII-I down-regulates a subset of estrogen-responsive genes through its interaction with an initiator element and estrogen receptor alpha. Genes Cells 2006. 11: 373-381.
23. Wen, Y. D., Cress, W. D., Roy, A. L. and Seto, E., Histone deacetylase 3 binds to and regulates the multifunctional transcription factor TFII-I. J. Biol. Chem. 2003. 278: 1841-1847.
24. Novina, C. D., Cheriyath, V. and Roy, A. L., Regulation of TFII-I activity by phosphorylation. J. Biol. Chem. 1998. 273: 33443-33448.
25. Cyster, J. G., Shotton, D. M. and Williams, A. F., The dimensions of the T lymphocyte glycoprotein leukosialin and identification of linear protein epitopes that can be modified by glycosylation. EMBO J. 1991. 10: 893-902.
26. Cruz-Munoz, M. E., Salas-Vidal, E., Salaiza-Suazo, N., Becker, I., Pedraza-Alva, G. and Rosenstein, Y., The CD43 coreceptor molecule recruits the zeta-chain as part of its signaling pathway. J. Immunol. 2003. 171: 1901-1908. (Pubitemid 36966473)
27. Pedraza-Alva, G., Merida, L. B., Burakoff, S. J. and Rosenstein, Y., CD43-specific activation of T cells induces association of CD43 to Fyn kinase. J. Biol. Chem. 1996. 271: 27564-27568.
28. Pedraza-Alva, G., Merida, L. B., Burakoff, S. J. and Rosenstein, Y., T cell activation through the CD43 molecule leads to Vav tyrosine phosphorylation and mitogen-activated protein kinase pathway activation. J. Biol. Chem. 1998. 273: 14218-14224.
29. Pedraza-Alva, G., Sawasdikosol, S., Liu, Y. C., Merida, L. B., Cruz-Munoz, M. E., Oceguera-Yanez, F., Burakoff, S. J. and Rosenstein, Y., Regulation of Cbl molecular interactions by the co-receptor molecule CD43 in human T cells. J. Biol. Chem. 2001. 276: 729-737.
30. Santana, M. A., Pedraza-Alva, G., Olivares-Zavaleta, N., Madrid-Marina, V., Horejsi, V., Burakoff, S. J. and Rosenstein, Y., CD43-mediated signals induce DNA binding activity of AP-1, NF-AT, and NFkappa B transcription factors in human T lymphocytes. J. Biol. Chem. 2000. 275: 31460-31468.
31. Fierro, N. A., Pedraza-Alva, G. and Rosenstein, Y., TCR-dependent cell response is modulated by the timing of CD43 engagement. J. Immunol. 2006. 176: 7346-7353. (Pubitemid 43849035)
32. Ji, H. B., Gupta, A., Okamoto, S., Blum, M. D., Tan, L., Goldring, M. B., Lacy, E. et al., T cell-specific expression of the murine CD3delta promoter. J. Biol. Chem. 2002. 277: 47898-47906.
33. Chen, J., Malcolm, T., Estable, M. C., Roeder, R. G. and Sadowski, I., TFII-I regulates induction of chromosomally integrated human immunodeficiency virus type 1 long terminal repeat in cooperation with USF. J. Virol. 2005. 79: 4396-4406. (Pubitemid 40388376)
34. Sadowski, I. and Mitchell, D. A., TFII-I and USF (RBF-2) regulate Ras/ MAPK-responsive HIV-1 transcription in T cells. Eur. J. Cancer 2005. 41: 2528-2536. (Pubitemid 41540628)
35. Malcolm, T., Chen, J., Chang, C. and Sadowski, I., Induction of chromosomally integrated HIV-1 LTR requires RBF-2 (USF/TFII-I) and Ras/MAPK signaling. Virus Genes 2007. 35: 215-223. (Pubitemid 47087561)
36. Park, J. K., Rosenstein, Y. J., Remold-O'Donnell, E., Bierer, B. E., Rosen, F. S. and Burakoff, S. J., Enhancement of T-cell activation by the CD43 molecule whose expression is defective in Wiskott-Aldrich syndrome. Nature 1991. 350: 706-709. (Pubitemid 21912302)
37. Bagriacik, E. U., Tang, M., Wang, H. C. and Klein, J. R., CD43 potentiates CD3-induced proliferation of murine intestinal intraepithelial lymphocytes. Immunol. Cell. Biol. 2001. 79: 303-307.
38. Mao, C., Zhou, M. and Uckun, F. M., Crystal structure of Bruton's tyrosine kinase domain suggests a novel pathway for activation and provides insights into the molecular basis of X-linked agammaglobulinemia. J. Biol. Chem. 2001. 276: 41435-41443.
39. Brown, K., Long, J. M., Vial, S. C., Dedi, N., Dunster, N. J., Renwick, S. B., Tanner, A. J. et al., Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. J. Biol. Chem. 2004. 279: 18727-18732.
40. Pérez-Jurado, L. A., Wang, Y-K., Peoples, R., Coloma, A., Cruces, J. and Franke, U., A duplicated gene in the breakpoint regions of the 7q11.23 Williams-Beuren syndrome deletion encodes the initiator binding protein TFII-I and BAP-135, a phosphorylation target of Btk. Hum. Mol. Genet. 1998. 7: 325-334.
41. Wang, Y.-K., Pérez-Jurado, L. A. and Francke, U., A mouse single-copy gene, Gtf2i, the homolog of human GTF2I, that is duplicated in the Williams-Beuren Syndrome deletion region. Genomics 1998. 48: 163-170. (Pubitemid 28164495)
42. Bunnell, S. C., Diehn, M., Yaffe, M. B., Findell, P. R., Cantley, L. C. and Berg, L. J., Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 2000. 275: 2219-2230.
43. Cheriyath, V. and Roy, A. L., Alternatively spliced isoforms of TFII-I. J. Biol. Chem. 2000. 275: 26300-26308.
44. Cheriyath, V. and Roy, A. L., Structure-function analysis of TFII-I. Roles of the N-terminal end, basic region, and I-repeats. J. Biol. Chem. 2001. 276: 8377-8383.
45. Mizushima, S. and Nagata, S., pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 1990. 18: 5322. (Pubitemid 20270119)
46. Heyeck, S. D.,Wilcox, H. M., Bunnell, S. C. and Berg, L. J., Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 1997. 272: 25401-25408.
47. Acuto, O. and Michel, F., CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat. Rev. Immunol. 2003. 3: 939-951.
48. Remold-O'Donnell, E., Davis,A. E., III, Kenney, D., Bhaskar, K. R. and Rosen, F. S., Purification and chemical composition of gpL115, the human lymphocyte surface sialoglycoprotein that is defective in Wiskott-Aldrich syndrome. J. Biol. Chem. 1986. 261: 7526-7530.