Disrupting the intermolecular self-association of Itk enhances T cell signaling

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4228-4235

  Min, Lie ^a   Wu, Wenfang ^b   Joseph, Raji E ^a   Fulton, D Bruce ^a   Berg, Leslie ^b   Andreotti, Amy H ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRUTON TYROSINE KINASE; CALCIUM ION; ENZYME VARIANT; INTERLEUKIN 2 TYROSINE KINASE; PHOSPHOLIPASE C GAMMA1; PROTEIN SH2; PROTEIN SH3; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; EMT PROTEIN TYROSINE KINASE; EMT PROTEIN-TYROSINE KINASE; LYMPHOCYTE ANTIGEN RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME BINDING; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; INSECT CELL; LIGAND BINDING; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; WILD TYPE; ANIMAL; ARMYWORM; BACULOVIRUS; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRAIN 3T3; DOWN REGULATION; DRUG ANTAGONISM; ENZYMOLOGY; GENE VECTOR; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; POINT MUTATION;

ANIMALS; BACULOVIRIDAE; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; DOWN-REGULATION; ENZYME ACTIVATION; GENETIC VECTORS; MICE; MODELS, IMMUNOLOGICAL; NIH 3T3 CELLS; POINT MUTATION; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SPODOPTERA;

EID: 77952784916     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901908     Document Type: Article

References (54)

1. Gibson, S., B. Leung, J. A. Squire, M. Hill, N. Arima, P. Goss, D. Hogg, and G. B. Mills. 1993. Identification, cloning, and characterization of a novel human T-cell-specific tyrosine kinase located at the hematopoietin complex on chromosome 5q. Blood 82: 1561-1572. (Pubitemid 23263974)
2. Heyeck, S. D., and L. J. Berg. 1993. Developmental regulation of a murine T-cell-specific tyrosine kinase gene, Tsk. Proc. Natl. Acad. Sci. USA 90: 669-673.
3. Siliciano, J. D., T. A. Morrow, and S. V. Desiderio. 1992. itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc. Natl. Acad. Sci. USA 89: 11194-11198.
4. Tanaka, N., H. Asao, K. Ohtani, M. Nakamura, and K. Sugamura. 1993. A novel human tyrosine kinase gene inducible in T cells by interleukin 2. FEBS Lett. 324: 1-5. (Pubitemid 23165025)
5. Yamada, N., Y. Kawakami, H. Kimura, H. Fukamachi, G. Baier, A. Altman, T. Kato, Y. Inagaki, and T. Kawakami. 1993. Structure and expression of novel protein-tyrosine kinases, EMB and EMT, in hematopoietic cells. Biochem. Biophys. Res. Commun. 192: 231-240.
6. Liu, K. Q., S. C. Bunnell, C. B. Gurniak, and L. J. Berg. 1998. T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itkdeficient T cells. J. Exp. Med. 187: 1721-1727.
7. Perez-Villar, J. J., and S. B. Kanner. 1999. Regulated association between the tyrosine kinase Emt/Itk/Tsk and phospholipase-C gamma 1 in human T lymphocytes. J. Immunol. 163: 6435-6441.
8. Schaeffer, E. M., J. Debnath, G. Yap, D. McVicar, X. C. Liao, D. R. Littman, A. Sher, H. E. Varmus, M. J. Lenardo, and P. L. Schwartzberg. 1999. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 284: 638-641.
9. Wilcox, H. M., and L. J. Berg. 2003. Itk phosphorylation sites are required for functional activity in primary T cells. J. Biol. Chem. 278: 37112-37121.
10. Palacios, E. H., and A. Weiss. 2004. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23: 7990-8000.
11. Berg, L. J., L. D. Finkelstein, J. A. Lucas, and P. L. Schwartzberg. 2005. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 23: 549-600.
12. Cooper, J. A., and B. Howell. 1993. The when and how of Src regulation. Cell 73: 1051-1054.
13. Roskoski, R., Jr. 2004. Src protein-tyrosine kinase structure and regulation. Biochem. Biophys. Res. Commun. 324: 1155-1164.
14. Xu, W., A. Doshi, M. Lei, M. J. Eck, and S. C. Harrison. 1999. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3: 629-638. (Pubitemid 29268446)
15. Xu, W., S. C. Harrison, and M. J. Eck. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595-602. (Pubitemid 27087566)
16. Severin, A., R. E. Joseph, S. Boyken, D. B. Fulton, and A. H. Andreotti. 2009. Proline isomerization preorganizes the Itk SH2 domain for binding to the Itk SH3 domain. J. Mol. Biol. 387: 726-743.
17. Andreotti, A. H., S. C. Bunnell, S. Feng, L. J. Berg, and S. L. Schreiber. 1997. Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature 385: 93-97.
18. Brazin, K. N., D. B. Fulton, and A. H. Andreotti. 2000. A specific intermolecular association between the regulatory domains of a Tec family kinase. J. Mol. Biol. 302: 607-623.
19. Mallis, R. J., K. N. Brazin, D. B. Fulton, and A. H. Andreotti. 2002. Structural characterization of a proline-driven conformational switch within the Itk SH2 domain. Nat. Struct. Biol. 9: 900-905.
20. Laederach, A., K. W. Cradic, K. N. Brazin, J. Zamoon, D. B. Fulton, X. Y. Huang, and A. H. Andreotti. 2002. Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: intramolecular contact versus asymmetric homodimerization. Protein Sci. 11: 36-45. (Pubitemid 34024755)
21. Laederach, A., K. W. Cradic, D. B. Fulton, and A. H. Andreotti. 2003. Determinants of intra versus intermolecular self-association within the regulatory domains of Rlk and Itk. J. Mol. Biol. 329: 1011-1020.
22. Morrogh, L. M., S. Hinshelwood, P. Costello, G. O. Cory, and C. Kinnon. 1999. The SH3 domain of Bruton's tyrosine kinase displays altered ligand binding properties when auto-phosphorylated in vitro. Eur. J. Immunol. 29: 2269-2279.
23. Okoh, M. P., and M. Vihinen. 2002. Interaction between Btk TH and SH3 domain. Biopolymers 63: 325-334.
24. Pursglove, S. E., T. D. Mulhern, J. P. Mackay, M. G. Hinds, and G. W. Booker. 2002. The solution structure and intramolecular associations of the Tec kinase SRC homology 3 domain. J. Biol. Chem. 277: 755-762.
25. Hansson, H., M. P. Okoh, C. I. Smith, M. Vihinen, and T. Härd. 2001. Intermolecular interactions between the SH3 domain and the proline-rich TH region of Bruton's tyrosine kinase. FEBS Lett. 489: 67-70. (Pubitemid 32176007)
26. 4. Science 316: 886-889.
27. Qi, Q., N. Sahu, and A. August. 2006. Tec kinase Itk forms membrane clusters specifically in the vicinity of recruiting receptors. J. Biol. Chem. 281: 38529-38534.
28. Joseph, R. E., L. Min, and A. H. Andreotti. 2007. The linker between SH2 and kinase domains positively regulates catalysis of the Tec family kinases. Biochemistry 46: 5455-5462.
29. Brown, K., J. M. Long, S. C. Vial, N. Dedi, N. J. Dunster, S. B. Renwick, A. J. Tanner, J. D. Frantz, M. A. Fleming, and G. M. Cheetham. 2004. Crystal structures of interleukin-2 tyrosine kinase and their implications for the design of selective inhibitors. J. Biol. Chem. 279: 18727-18732.
30. Hawkins, J., and A. Marcy. 2001. Characterization of Itk tyrosine kinase: contribution of noncatalytic domains to enzymatic activity. Protein Expr. Purif. 22: 211-219.
31. Heyeck, S. D., H. M. Wilcox, S. C. Bunnell, and L. J. Berg. 1997. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 272: 25401-25408.
32. Ouyang, W., S. H. Ranganath, K. Weindel, D. Bhattacharya, T. L. Murphy, W. C. Sha, and K. M. Murphy. 1998. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity 9: 745-755. (Pubitemid 28557602)
33. Masuyama, N., K. Oishi, Y. Mori, T. Ueno, Y. Takahama, and Y. Gotoh. 2001. Akt inhibits the orphan nuclear receptor Nur77 and T-cell apoptosis. J. Biol. Chem. 276: 32799-32805.
34. Weng, Z., R. J. Rickles, S. Feng, S. Richard, A. S. Shaw, S. L. Schreiber, and J. S. Brugge. 1995. Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol. Cell. Biol. 15: 5627-5634.
35. Yu, H., J. K. Chen, S. Feng, D. C. Dalgarno, A. W. Brauer, and S. L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76: 933-945.
36. Bunnell, S. C., M. Diehn, M. B. Yaffe, P. R. Findell, L. C. Cantley, and L. J. Berg. 2000. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 275: 2219-2230.
37. Miller, A. T., and L. J. Berg. 2002. New insights into the regulation and functions of Tec family tyrosine kinases in the immune system. Curr. Opin. Immunol. 14: 331-340.
38. + T-cell development. Nat. Rev. Immunol. 7: 479-485.
39. Nika, K., L. Tautz, Y. Arimura, T. Vang, S. Williams, and T. Mustelin. 2007. A weak Lck tail bite is necessary for Lck function in T cell antigen receptor signaling. J. Biol. Chem. 282: 36000-36009.
40. August, A., A. Sadra, B. Dupont, and H. Hanafusa. 1997. Src-induced activation of inducible T cell kinase (ITK) requires phosphatidylinositol 3-kinase activity and the Pleckstrin homology domain of inducible T cell kinase. Proc. Natl. Acad. Sci. USA 94: 11227-11232.
41. Kojima, T., M. Fukuda, Y. Watanabe, F. Hamazato, and K. Mikoshiba. 1997. Characterization of the pleckstrin homology domain of Btk as an inositol polyphosphate and phosphoinositide binding domain. Biochem. Biophys. Res. Commun. 236: 333-339.
42. Rameh, L. E., A. Arvidsson, K. L. Carraway, III, A. D. Couvillon, G. Rathbun, A. Crompton, B. VanRenterghem, M. P. Czech, K. S. Ravichandran, S. J. Burakoff, et al. 1997. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272: 22059-22066.
43. Salim, K., M. J. Bottomley, E. Querfurth, M. J. Zvelebil, I. Gout, R. Scaife, R. L. Margolis, R. Gigg, C. I. Smith, P. C. Driscoll, et al. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15: 6241-6250.
44. Klemm, J. D., S. L. Schreiber, and G. R. Crabtree. 1998. Dimerization as a regulatory mechanism in signal transduction. Annu. Rev. Immunol. 16: 569-592.
45. Lemmon, M. A., and J. Schlessinger. 1998. Transmembrane signaling by receptor oligomerization. Methods Mol. Biol. 84: 49-71.
46. Su, Q., S. Wang, D. Baltzis, L. K. Qu, A. H. Wong, and A. E. Koromilas. 2006. Tyrosine phosphorylation acts as a molecular switch to full-scale activation of the eIF2alpha RNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 103: 63-68.
47. Lemaire, P. A., J. Lary, and J. L. Cole. 2005. Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA. J. Mol. Biol. 345: 81-90.
48. Jiang, G., J. den Hertog, J. Su, J. Noel, J. Sap, and T. Hunter. 1999. Dimerization inhibits the activity of receptor-like protein-tyrosine phosphatase-alpha. Nature 401: 606-610. (Pubitemid 129517077)
49. Nayak, V., K. Zhao, A. Wyce, M. F. Schwartz, W. S. Lo, S. L. Berger, and R. Marmorstein. 2006. Structure and dimerization of the kinase domain from yeast Snf1, a member of the Snf1/AMPK protein family. Structure 14: 477-485. (Pubitemid 43363481)
50. Rosenberg, O. S., S. Deindl, R. J. Sung, A. C. Nairn, and J. Kuriyan. 2005. Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme. Cell 123: 849-860.
51. Ogawa, A., Y. Takayama, H. Sakai, K. T. Chong, S. Takeuchi, A. Nakagawa, S. Nada, M. Okada, and T. Tsukihara. 2002. Structure of the carboxyl-terminal Src kinase, Csk. J. Biol. Chem. 277: 14351-14354.
52. Ching, K. A., J. A. Grasis, P. Tailor, Y. Kawakami, T. Kawakami, and C. D. Tsoukas. 2000. TCR/CD3-induced activation and binding of Emt/Itk to linker of activated T cell complexes: requirement for the Src homology 2 domain. J. Immunol. 165: 256-262.
53. 2+ events and cytoskeletal reorganization. Trends Immunol. 22: 17-20.
54. Joseph, R. E., D. B. Fulton, and A. H. Andreotti. 2007. Mechanism and functional significance of Itk autophosphorylation. J. Mol. Biol. 373: 1281-1292.