Structural analysis of the lymphocyte-specific kinase Lck in complex with non-selective and Src family selective kinase inhibitors

Structure

Volumn 7, Issue 6, 1999, Pages 651-661

  Zhu, Xiaotian ^a   Kim, Joseph L ^a   Newcomb, John R ^a   Rose, Paul E ^a   Stover, David R ^a   Toledo, Leticia M ^a   Zhao, Huilin ^a   Morgenstern, Kurt A ^a  

^a Kinetix Pharmaceuticals Inc   (United States)

Author keywords

AMP PNP; Kinase; Lck; PP2; Src family; Staurosporine; X ray structure

Indexed keywords

ADENOSINE TRIPHOSPHATE DERIVATIVE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; STAUROSPORINE; T LYMPHOCYTE RECEPTOR;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN PURIFICATION; STRUCTURE ANALYSIS;

EID: 0033152210     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(99)80086-0     Document Type: Article

References (63)

1. Alberola-lia, J., Takaki, S., Kerner, J.D. & Perlmutter, R.M. (1997). Differential signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 15, 125-154.
2. Berridge, M.J. (1997). Lymphocyte activation in health and disease. Crit. Rev. Immunol. 17, 155-178.
3. Qian, D. & Weiss, A. (1997). T cell antigen receptor signal transduction. Curr. Opin. Cell Biol. 9, 205-212.
4. Barber, EK., Dasgupta, J.D., Schlossman, S.F., Trevillyan, J.M. & Rudd, C.E. (1989), The CD4 and CD8 antigens are coupled to a protein-tyrosine kinase (p56lck) that phosphorylates the CD3 complex. Proc. Natl Acad. Sci. USA 86, 3277-3281.
5. Wong, J., Straus, D. & Chan, A.C. (1998). Genetic evidence of a role for Lck in T-cell receptor function independent or downstream of ZAP-70/Syk protein tyrosine kinases. Mol. Cell Biol. 18, 2855-2866.
6. Thome, M., Germain, V., DiSanto, J.P. & Acuto, O. (1996). The p56lck SH2 domain mediates recruitment of CD8/p56lck to the activated T cell receptor/CD3/zeta complex. Eur. J. Immunol. 26, 2093-2100.
7. Chu, K. & Littman, D.R. (1994). Requirement for kinase activity of CD4-associated p56lck in antibody-triggered T cell signal transduction. J. Biol. Chem. 269, 24095-24101.
8. Chalupny, N.J., Ledbetter, J.A. & Kavathas, P. (1991). Association of CD8 with p56lck is required for early T cell signaling events. EMBO J. 10, 1201-1207.
9. Van Oers, N.S., Killeen, N. & Weiss, A. (1996). Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. J. Exp. Med. 183, 1053-1062.
10. Kersh, E.N., Shaw, A.S. & Allen, P.M. (1998). Fidelity of T cell activation through multistep T cell receptor zeta phosphorylation. Science 281, 572-575.
11. Madrenas, J., Wange, R.L., Wang. J.L., Isakov, N., Samelson, L.E. & Germain, R.N. (1995). Zeta phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267, 515-518.
12. Straus, D.B. & Weiss, A. (1993). The CD3 chains of the T cell antigen receptor associate with the ZAP-70 tyrosine kinase and are tyrosine phosphorylated after receptor stimulation. J. Exp. Med. 178. 1523-1530.
13. Wange, R.L., Kong, A.N. & Samelson, L.E. (1992). A tyrosine-phosphorylated 70 kDa protein binds a photoaffinity analogue of ATP and associates with both the zeta chain and CD3 components of the activated T cell antigen receptor. J. Biol. Chem. 267, 11685-11688.
14. Chan, A.C., Irving, B.A., Fraser, J.D. & Weiss, A. (1991). The zeta chain is associated with a tyrosine kinase and upon T-cell antigen receptor stimulation associates with ZAP-70, a 70 kDa tyrosine phosphoprotein. Proc. Natl Acad. Sci. USA 88, 9166-9170.
15. Isakov, N., Wange, R.L., Burgess, W.H., Watts, J.D., Aebersold, R. & Samelson, L.E. (1995). ZAP-70 binding specificity to T cell receptor tyrosine-based activation motifs: The tandem SH2 domains of ZAP-70 bind distinct tyrosine-based activation motifs with varying affinity. J. Exp. Med. 181, 375-380.
16. Wange, R.L., Malek, S.N., Desiderio, S. & Samelson, L.E. (1993). Tandem SH2 domains of ZAP-70 bind to T cell antigen receptor zeta and CD3 epsilon from activated Jurkat T cells. J. Biol. Chem. 268, 19797-19801.
17. Chan, A.C., et al., & Kurosaki, T. (1995). Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J. 14, 24499-24508.
18. Neumeister, E.N., Zhu, Y., Richard, S., Terhorst, C., Chan, A.C. & Shaw, A.S. (1995). Binding of ZAP-70 to phosphorylated T-cell receptor zeta and eta enhances its autophosphorylation and generates specific binding sites for SH2 domain-containing proteins. Mol. Cell Biol. 15, 3171-3178.
19. Watts, J.D., Affolter, M., Krebs, D.L., Wange, R.L., Samelson, L.E. & Aebersold, R. (1994). Identification by electrospray ionization mass spectrometry of the sites of tyrosine phosphorylation induced in activated Jurkat T cells on the protein tyrosine kinase ZAP-70. J. Biol. Chem. 269, 29520-29529.
20. LoGrasso, P.V., Hawkins, J., Frank, L.J., Wisniewski, D. & Marcy, A. (1996). Mechanism of activation for Zap-70 catalytic activity. Proc. Natl Acad. Sci. USA 93, 12165-12170.
21. Wange, R.L., Guitian, R., Isakov, N., Watts, J.D., Aebersold, R. & Samelson, LE. (1995). Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of ZAP-70. J. Biol. Chem. 270, 18730-18733.
22. Rudd, C.E. (1999). Adaptors and molecular scaffolds in immune cell signaling. Cell 96, 5-8.
23. Straus, D.B. & Weiss, A. (1992). Genetic evidence for the involvement of the Lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70, 585-593.
24. Henning, S.W. & Cantrell, D.A. (1998). p56lck signals for regulating thymocyte development can be distinguished by their dependency on Rho function. J. Exp. Med. 188, 931-939.
25. Levin, S.D., Abraham, K.M., Anderson, S.J., Forbush, K.A. & Perlmutter, R.M. (1993). The protein tyrosine kinase p56lck regulates thymocyte development independently of its interaction with CD4 and CD8 coreceptors J. Exp. Med. 178, 245-255. Erratum appears in J. Exp. Med. (1993) 178 p.1135.
26. Molina, T.J., et al., & Veillette A. (1992). Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164.
27. Molina, T.J., Bachmann, M.F., Kundig T.M., Zinkernagel, R.M. & Mak, T.W. (1993). Peripheral T cells in mice lacking p56lck do not express significant antiviral effector functions. J. Immunol. 151, 699-706.
28. Lin, R.S., Rodriguez, C., Veillette, A. & Lodish, H.F. (1998). Zinc is essential for binding of p56(lck) to CD4 and CD8alpha. J. Biol. Chem. 273, 32878-32882.
29. 2+ ion links the cytoplasmic tail of CD4 and the N-terminal region of Lck. J. Biol. Chem. 273, 18729-18733.
30. Watts, J.D., et al., Aebersold, R. (1992). Purification and initial characterization of the lymphocyte-specific protein-tyrosyl kinase p56lck from a baculovirus expression system. J. Biol. Chem. 267, 901-907.
31. Gervais, F.G., Chow, L.M., Lee, J.M., Branton, P.E. & Veillette, A. (1993). The SH2 domain is required for stable phosphorylation of p56lck at tyrosine 505, the negative regulatory site. Mol. Cell Biol. 13, 7112-7121.
32. Bougeret, C., et al., & Fischer, S. (1996). Detection of a physical and functional interaction between Csk and Lck which involves the SH2 domain of Csk and is mediated by autophosphorylation of Lck on tyrosine 394. J. Biol. Chem. 271, 7465-7472.
33. Jullien, P., et al., & Benarous, R. (1994). Tyr394 and Tyr505 are autophosphorylated in recombinant Lck protein-tyrosine kinase expressed in Escherichia coli. Eur. J. Biochem. 224, 589-596.
34. Williams, J.C., et al., & Wierenga, R.K. (1997). The 2.35 Å crystal structure of the inactivated form of chicken Src: A dynamic molecule with multiple regulatory interactions. J. Mol. Biol. 274, 757-775.
35. Sicheri, F., Moarefi, I. & Kuriyan. J. (1997). Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602-609.
36. Xu, W., Harrison, S.C. & Eck, M.J. (1997). Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602.
37. Reynolds, P.J., Hurley, T.R. & Sefton, B.M. (1992). Functional analysis of the SH2 and SH3 domains of the Lck tyrosine protein kinase. Oncogene 7, 1949-1955.
38. Mustelin, T. & Altman, A. (1990). Dephosphorylation and activation of the T cell tyrosine kinase pp56lck by the leukocyte common antigen (CD45). Oncogene 5, 809-813.
39. Moarefi, I., et al., & Miller, W.T. (1997). Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385, 650-653.
40. Yamaguchi, H. & Hendrickson, W.A. (1996). Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384, 484-489.
41. Meggio, D., et al., & Furet, P. (1995). Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur. J. Biochem. 234, 317-322.
42. Prade, L., Engh, R.A., Girod, A., Kinzel, V., Huber, R. & Bossemeyer, D. (1997). Staurosporine-induced conformational changes of cAMP- Dependent protein kinase catalytic subunit explain inhibitory potential. Structure 5, 1627-1637.
43. Lawrie, A.M., Noble, M.E., Tunnah, P., Brown, N.R., Johnson, L.N. & Endicott, J.A. (1997). Protein kinase inhibition by staurosporine revealed in details of the molecular interaction with CDK2. Nat. Struct. Biol. 4, 796-801.
44. Toledo, L.M. & Lydon, N.B. (1997). Structures of staurosporine bound to CDK2 and cAPK - new tools for structure-based design of protein kinase inhibitors. Structure 5, 1551-1556.
45. Lamers, M.B., Antson, A.A., Hubbard, R.E., Scott, R.K. & Williams, D.H. (1999). Structure of the protein tyrosine kinase domain of C-terminal Src kinase (CSK) in complex with staurosporine. J. Mol. Biol. 285, 713-725.
46. Hanke, J.H., et al., & Connelly, P.A. (1996). Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck-and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701.
47. Knighton, D.R. et. al., & Sowadski, J.M. (1991). Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 407-414.
48. Knighton, D.R., et al., & Sowadski, J.M. (1991). Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 414-420.
49. Hubbard, S.R. (1997). Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16, 5572-5581.
50. Kuduva, S.S., Craig, D.C., Nangia, A. & Gautam, R. (1999). Cubanecarboxylic acids. Crystal engineering considerations and the role of C-H O hydrogen bonds in determining O-H O networks. J. Am. Chem. Soc. 121, 1936-1944.
51. Kim, Y.H., Buchholz, MA, Chrest, F.J. & Nordin, A.A. (1994). Upregulation of c-myc induces the gene expression of the murine homologues of p34cdc2 and cyclin-dependent kinase-2 in T lymphocytes. J. Immunol. 152, 4328-4333.
52. Traxler, P. (1998). Tyrosine kinase inhibitors in cancer treatment (Part II). Expert Opinion in Therapeutic Patents 8, 1599-1625.
53. Mohammadi, et al., & Hubbard, S.R. (1998). Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J. 17, 5896-5904.
54. Tong, L., et al., & Pargellis, C.A. (1997). A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket. Nat. Struct. Biol. 4, 311-316.
55. Wilson, K.P., et al., & Su, M.S.S. (1997). The structural basis for the specificity of pyridinylimidazole inhibitors of p38 MAP kinase. Chem. Biol. 4, 423-431.
56. Wang, Z., et al., & Goldsmith, E.J. (1998). Structural basis of inhibitor selectivity in MAP kinases. Structure 6, 1117-1128.
57. Morgenstern, K.A., et al., & Kisiel, W. (1994). Complementary DNA cloning and kinetic characterization of a novel intracellular serine proteinase inhibitor: Mechanism of action with trypsin and factor Xa as model proteinases. Biochemistry 33, 3432-3441.
58. Morgenstern, K.A., et al., & Thomson, J.A. (1997). Polynucleotide modulation of the protease, nucleoside triphosphatase, and helicase activities of a hepatitis C virus NS3-NS4A complex isolated from transfected COS cells. J. Virol. 71, 3767-3775.
59. Otwinowski, Z. (1993) Oscillation data reduction program. In Data Collection and Processing, Proceedings of the National Study Weekend. (Sawyer, L., Issacs, N. & Bailey, S.W., eds), pp.55-62, Daresbury Laboratory, Warrington, Uk.
60. Navaza, J. (1994). AmoRe: An automated package for molecular replacement. Acta Crystallogr. A 50, 157-163.
61. Brünger, AT., Krukowski, A. & Erickson, J.W. (1990). Slow-cooling protocols for crystallographic refinement by simulated annealing. Acta Crystallogr. A 46, 585-593.
62. Nicholls, A., Sharp, K.A. & Honig, B. (1991). Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.
63. Evans, S.V. (1993). SETOR: Hardware-lighted three-dimensional solid model representations of macromolecules. J. Mol. Graph. 11, 134-138.