394
Views
27
CrossRef citations to date
0
Altmetric
Articles

Structural elements and allosteric mechanisms governing regulation and catalysis of CSK-family kinases and their inhibition of Src-family kinases

, , , , , & show all
Pages 329-350 | Received 20 Jan 2010, Accepted 07 Apr 2010, Published online: 17 May 2010

References

  • Adams JA. 2001. Kinetic and catalytic mechanisms of protein kinases. Chem Rev. 101:2271–2290.
  • Azam M, Seelinger MA, Gray NS, Kuriyan J, Daley GQ. 2008. Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat Struct Mol Biol. 15:1109–1118.
  • Bennett BD, Cowley S, Jiang S, London R, Deng B, Grabarek J, Groopman JE, Goeddel DV, Avraham H. 1994. Identification and characterization of a novel tyrosine kinase from megakaryocytes. J Biol Chem. 269:1068–1074.
  • Brinkworth RI, Breinl RA, Kobe B. 2003. Structural basis and prediction of substrate specificity in protein serine/threonine kinases. Proc Natl Acad Sci USA. 100:74–79.
  • Campbell KS, Buder A, Deuschle U. 1995. Interactions between the amino-terminal domain of p56lck and cytoplasmic domains of CD4 and CD8 alpha in yeast. Eur J Immunol. 25:2408–2412.
  • Cheng H-C, Chong YP, Ia KK, Tan Oa, Mulhern TD. 2006. Csk homologous kinase. UCSD-Nature Molecule Pages. doi:10.1038/mp.a000705.01.
  • Cheng HC, Johnson TM, Mills RD, Chong YP, Chan KC, Culvenor JG. 2010. Allosteric networks governing regulation and catalysis of src-family protein tyrosine kinases—implications for disease-associated kinases. Clin Exp Pharmacol Physiol. 37:93–101.
  • Chong YP, Chan AS, Chan KC, Williamson NA, Lerner EC, Smithgall TE, Bjorge JD, Fujita DJ, Purcell AW, Scholz G, Mulhern TD, Cheng HC. 2006. C-terminal Src kinase-homologous kinase (CHK), a unique inhibitor inactivating multiple active conformations of Src family tyrosine kinases. J Biol Chem. 281:32988–32999.
  • Chong YP, Mulhern TD, Cheng HC. C-terminal Src kinase (CSK) and CSK-homologous kinase (CHK)–endogenous negative regulators of Src-family protein kinases. Growth Factors. 2005a; 23:233–244.
  • Chong YP, Ia KK, Mulhern TD, Cheng HC. Endogenous and synthetic inhibitors of the Src-family protein tyrosine kinases. Biochim Biophys Acta. 2005b; 1754:210–220.
  • Chong YP, Mulhern TD, Zhu HJ, Fujita DJ, Bjorge JD, Tantiongco JP, Sotirellis N, Lio DS, Scholz G, Cheng HC. 2004. A novel non-catalytic mechanism employed by the C-terminal Src-homologous kinase to inhibit Src-family kinase activity. J Biol Chem. 279:20752–20766.
  • Cohen P, Knebel A. 2006. KESTREL: A powerful method for identifying the physiological substrates of protein kinases. Biochem J. 393:1–6.
  • Cole PA, Shen K, Qiao Y, Wang D. 2003. Protein tyrosine kinases Src and Csk: A tail's tale. Curr Opin Chem Biol. 7:580–585.
  • Cooper JA, Gould KL, Cartwright CA, Hunter T. 1986. Tyr527 is phosphorylated in pp60c-src: Implications for regulation. Science. 231:1431–1434.
  • Cowan-Jacob SW, Fendrich G, Manley PW, Jahnke W, Fabbro D, Liebetanz J, Meyer T. 2005. The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure. 13:861–871.
  • Cowan-Jacob SW. 2006. Structural biology of protein tyrosine kinases. Cell Mol Life Sci. 63:2608–2625.
  • D'Arco M, Giniatullin R, Leone V, Carloni P, Birsa N, Nair A, Nistri A, Fabbretti E. 2009. The C-terminal Src inhibitory kinase (Csk)-mediated tyrosine phosphorylation is a novel molecular mechanism to limit P2X3 receptor function in mouse sensory neurons. J Biol Chem. 284:21393–21401.
  • DeLano WL. 2002. The PyMOL molecular graphics system, http://www.pymol.org.
  • Filippakopoulos P, Muller S, Knapp S. 2009. SH2 domains: Modulators of nonreceptor tyrosine kinase activity. Curr Opin Struct Biol. 19:643–649.
  • Gingrich JR, Pelkey KA, Fam SR, Huang Y, Petralia RS, Wenthold RJ, Salter MW. 2004. Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc Natl Acad Sci USA. 101:6237–6242.
  • Hantschel O, Rix U, Superti-Furga G. 2008. Target spectrum of the BCR-ABL inhibitors imatinib, nilotinib and dasatinib. Leuk Lymphoma. 49:615–619.
  • Huang K, Wang YH, Brown A, Sun G. 2009. Identification of N-terminal lobe motifs that determine the kinase activity of the catalytic domains and regulatory strategies of Src and Csk protein tyrosine kinases. J Mol Biol. 386:1066–1077.
  • Hunter T, Sefton BM. 1980. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci USA. 77:1311–1315.
  • Ingley E. 2008. Src family kinases: Regulation of their activities, levels and identification of new pathways. Biochim Biophys Acta. 1784:56–65.
  • Johnson TM, Williamson NA, Scholz G, Jaworowski A, Wettenhall RE, Dunn AR, Cheng HC. 2000. Modulation of the catalytic activity of the Src family tyrosine kinase Hck by autophosphorylation at a novel site in the unique domain. J Biol Chem. 275:33353–33364.
  • Johnson LN. 2009. Protein kinase inhibitors: Contributions from structure to clinical compounds. Q Rev Biophys. 42:1–40.
  • Kamps MP, Buss JE, Sefton BM. 1985. Mutation of NH2-terminal glycine of p60src prevents both myristoylation and morphological transformation. Proc Natl Acad Sci USA. 82:4625–4628.
  • Kaplan W, Littlejohn TG. 2001. Swiss-PDB viewer (deep view). Brief Bioinform. 2:195–197.
  • Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K, Tarakhovsky A, Okada M. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 404:999–1003.
  • Kim LC, Song L, Haura EB. 2009. Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol. 6:587–595.
  • Klages S, Adam D, Class K, Fargnoli J, Bolen JB, Penhallow RC. 1994. Ctk: A protein-tyrosine kinase related to Csk that defines an enzyme family. Proc Natl Acad Sci USA. 91:2597–2601.
  • Kobe B, Kampmann T, Forwood JK, Listwan P, Brinkworth RI. 2005. Substrate specificity of protein kinases and computational prediction of substrates. Biochim Biophys Acta. 1754:200–209.
  • Kornev AP, Haste NM, Taylor SS, Eyck LF. 2006. Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc Natl Acad Sci USA. 103:17783–17788.
  • Kornev AP, Taylor SS. 2010. Defining the conserved internal architecture of a protein kinase. Biochim Biophys Acta. 1804:440–444.
  • Kornev AP, Taylor SS, Ten Eyck LF. 2008. A helix scaffold for the assembly of active protein kinases. Proc Natl Acad Sci USA. 105:14377–14382.
  • Kuo SS, Moran P, Gripp J, Armanini M, Phillips HS, Goddard A, Caras IW. 1994. Identification and characterization of Batk, a predominantly brain-specific non-receptor protein tyrosine kinase related to Csk. J Neurosci Res. 38:705–715.
  • Lamers MB, Antson AA, Hubbard RE, Scott RK, Williams DH. 1999. Structure of the protein tyrosine kinase domain of C-terminal Src kinase (CSK) in complex with staurosporine. J Mol Biol. 285:713–725.
  • Lee S, Ayrapetov MK, Kemble DJ, Parang K, Sun G. 2006. Docking-based substrate recognition by the catalytic domain of a protein tyrosine kinase, C-terminal Src kinase (Csk). J Biol Chem. 281:8183–8189.
  • Lee S, Lin X, Nam NH, Parang K, Sun G. 2003. Determination of the substrate-docking site of protein tyrosine kinase C-terminal Src kinase. Proc Natl Acad Sci USA. 100:14707–14712.
  • Levinson NM, Seeliger MA, Cole PA, Kuriyan J. 2008. Structural basis for the recognition of c-Src by its inactivator Csk. Cell. 134:124–134.
  • Levinson NM, Visperas PR, Kuriyan J. 2009. The tyrosine kinase Csk dimerizes through Its SH3 domain. PLoS One. 4:e7683.
  • Lieser SA, Aubol BE, Wong L, Jennings PA, Adams JA. Coupling phosphoryl transfer and substrate interactions in protein kinases. Biochim Biophys Acta. 2005a; 1754:191–199.
  • Lieser SA, Shindler C, Aubol BE, Lee S, Sun G, Adams JA. Phosphoryl transfer step in the C-terminal Src kinase controls Src recognition. J Biol Chem. 2005b; 280:7769–7776.
  • Lieser SA, Shaffer J, Adams JA. 2006. SRC tail phosphorylation is limited by structural changes in the regulatory tyrosine kinase Csk. J Biol Chem. 281:38004–38012.
  • Lin X, Ayrapetov MK, Lee S, Parang K, Sun G. 2005. Probing the communication between the regulatory and catalytic domains of a protein tyrosine kinase, Csk. Biochemistry. 44:1561–1567.
  • Lin X, Lee S, Sun G. 2003. Functions of the activation loop in Csk protein-tyrosine kinase. J Biol Chem. 278:24072–24077.
  • Lin X, Wang Y, Ahmadibeni Y, Parang K, Sun G. 2006. Structural basis for domain-domain communication in a protein tyrosine kinase, the C-terminal Src kinase. J Mol Biol. 357:1263–1273.
  • Li W, Young SL, King N, Miller WT. 2008. Signaling properties of a non-metazoan Src kinase and the evolutionary history of Src negative regulation. J Biol Chem. 283:15491–15501.
  • Martin GS. 2001. The hunting of the Src. Nat Rev Mol Cell Biol. 2:467–475.
  • Martin GS. 2004. The road to Src. Oncogene. 23:7910–7917.
  • Masterson LR, Mascioni A, Traaseth NJ, Taylor SS, Veglia G. 2008. Allosteric cooperativity in protein kinase A. Proc Natl Acad Sci USA. 105:506–511.
  • McVicar DW, Lal BK, Lloyd A, Kawamura M, Chen YQ, Zhang X, Staples JE, Ortaldo JR, O'Shea JJ. 1994. Molecular cloning of lsk, a carboxyl-terminal src kinase (csk) related gene, expressed in leukocytes. Oncogene. 9:2037–2044.
  • Mills JE, Whitford PC, Shaffer J, Onuchic JN, Adams JA, Jennings PA. 2007. A novel disulfide bond in the SH2 Domain of the C-terminal Src kinase controls catalytic activity. J Mol Biol. 365:1460–1468.
  • Mitsuhashi H, Futai E, Sasagawa N, Hayashi Y, Nishino I, Ishiura S. 2008. Csk-homologous kinase interacts with SHPS-1 and enhances neurite outgrowth of PC12 cells. J Neurochem. 105:101–112.
  • Moran MF, Koch CA, Anderson D, Ellis C, England L, Martin GS, Pawson T. 1990. Src homology region 2 domains direct protein-protein interactions in signal transduction. Proc Natl Acad Sci USA. 87:8622–8626.
  • Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H. 1991. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature. 351:69–72.
  • Nolen B, Taylor S, Ghosh G. 2004. Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell. 15:661–675.
  • Ogawa A, Takayama Y, Sakai H, Chong KT, Takeuchi S, Nakagawa A, Nada S, Okada M, Tsukihara T. 2002. Structure of the carboxyl-terminal Src kinase, Csk. J Biol Chem. 277:14351–14354.
  • Okada M, Nada S, Yamanashi Y, Yamamoto T, Nakagawa H. 1991. CSK: A protein-tyrosine kinase involved in regulation of src family kinases. J Biol Chem. 266:24249–24252.
  • Okada M, Nakagawa H. Protein tyrosine kinase in rat brain: Neonatal rat brain expresses two types of pp60c-src and a novel protein tyrosine kinase. J Biochem. 1988a; 104:297–305.
  • Okada M, Nakagawa H. Identification of a novel protein tyrosine kinase that phosphorylates pp60c-src and regulates its activity in neonatal rat brain. Biochem Biophys Res Commun. 1988b; 154:796–802.
  • Okada M, Nakagawa H. 1989. A protein tyrosine kinase involved in regulation of pp60c-src function. J Biol Chem. 264:20886–20893.
  • Parsons SJ, Parsons JT. 2004. Src family kinases, key regulators of signal transduction. Oncogene. 23:7906–7909.
  • Pellicena P, Miller WT. 2001. Processive phosphorylation of p130Cas by Src depends on SH3-polyproline interactions. J Biol Chem. 276:28190–28196.
  • Pincus D, Letunic I, Bork P, Lim WA. 2008. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc Natl Acad Sci USA. 105:9680–9684.
  • Ren R, Mayer BJ, Cicchetti P, Baltimore D. 1993. Identification of a ten-amino acid proline-rich SH3 binding site. Science. 259:1157–1161.
  • Resh MD. 1993. Interaction of tyrosine kinase oncoproteins with cellular membranes. Biochim Biophys Acta. 1155:307–322.
  • Ruzzene M, Songyang Z, Marin O, Donella-Deana A, Brunati AM, Guerra B, Agostinis P, Cantley LC, Pinna LA. 1997. Sequence specificity of C-terminal Src kinase (CSK)–a comparison with Src-related kinases c-Fgr and Lyn. Eur J Biochem. 246:433–439.
  • Sadowski I, Stone JC, Pawson T. 1986. A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps. Mol Cell Biol. 6:4396–4408.
  • Sakano S, Iwama A, Inazawa J, Ariyama T, Ohno M, Suda T. 1994. Molecular cloning of a novel non-receptor tyrosine kinase, HYL (hematopoietic consensus tyrosine-lacking kinase). Oncogene. 9:1155–1161.
  • Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 234:779–815.
  • Saunders NF, Brinkworth RI, Huber T, Kemp BE, Kobe B. 2008. Predikin and PredikinDB: A computational framework for the prediction of protein kinase peptide specificity and an associated database of phosphorylation sites. BMC Bioinformatics. 9:245.
  • Saunders NF, Kobe B. 2008. The Predikin webserver: Improved prediction of protein kinase peptide specificity using structural information. Nucleic Acids Res. 36:W286–W290.
  • Schmidt H, Hoffmann S, Tran T, Stoldt M, Stangler T, Wiesehan K, Willbold D. 2007. Solution structure of a Hck SH3 domain ligand complex reveals novel interaction modes. J Mol Biol. 365:1517–1532.
  • Segawa Y, Suga H, Iwabe N, Oneyama C, Akagi T, Miyata T, Okada M. 2006. Functional development of Src tyrosine kinases during evolution from a unicellular ancestor to multicellular animals. Proc Natl Acad Sci USA. 103:12021–12026.
  • Shekhtman A, Ghose R, Wang D, Cole PA, Cowburn D. 2001. Novel mechanism of regulation of the non-receptor protein tyrosine kinase Csk: Insights from NMR mapping studies and site-directed mutagenesis. J Mol Biol. 314:129–138.
  • Shenoy S, Chackalaparampil I, Bagrodia S, Lin PH, Shalloway D. 1992. Role of p34cdc2-mediated phosphorylations in two-step activation of pp60c-src during mitosis. Proc Natl Acad Sci USA. 89:7237–7241.
  • Sicheri F, Moarefi I, Kuriyan J. 1997. Crystal structure of the Src family tyrosine kinase Hck. Nature. 385:602–609.
  • Sondhi D, Cole PA. 1999. Domain interactions in protein tyrosine kinase Csk. Biochemistry. 38:11147–11155.
  • Sondhi D, Xu W, Songyang Z, Eck MJ, Cole PA. 1998. Peptide and protein phosphorylation by protein tyrosine kinase Csk: Insights into specificity and mechanism. Biochemistry. 37:165–172.
  • Songyang Z, Shoelson SE, McGlade J, Olivier P, Pawson T, Bustelo XR, Barbacid M, Sabe H, Hanafusa H, Yi T, Ren R, Baltinmore D, Ratnafsky S, Feldman RA, Cantley LC. 1994. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol Cell Biol. 14:2777–2785.
  • Sotirellis N, Johnson TM, Hibbs ML, Stanley IJ, Stanley E, Dunn AR, Cheng HC. 1995. Autophosphorylation induces autoactivation and a decrease in the Src homology 2 domain accessibility of the Lyn protein kinase. J Biol Chem. 270:29773–29780.
  • Takeuchi S, Takayama Y, Ogawa A, Tamura K, Okada M. 2000. Transmembrane phosphoprotein Cbp positively regulates the activity of the carboxyl-terminal Src kinase, Csk. J Biol Chem. 275:29183–29186.
  • Tarrant MK, Cole PA. 2009. The chemical biology of protein phosphorylation. Annu Rev Biochem. 78:797–825.
  • Taylor SS, Knighton DR, Zheng J, Ten Eyck LF, Sowadski JM. 1992. Structural framework for the protein kinase family. Annu Rev Cell Biol. 8:429–462.
  • Turk BE, Hutti JE, Cantley LC. 2006. Determining protein kinase substrate specificity by parallel solution-phase assay of large numbers of peptide substrates. Nat Protoc. 1:375–379.
  • Wang D, Huang XY, Cole PA. 2001. Molecular determinants for Csk-catalyzed tyrosine phosphorylation of the Src tail. Biochemistry. 40:2004–2010.
  • Weijland A, Neubauer G, Courtneidge SA, Mann M, Wierenga RK, Superti-Furga G. 1996. The purification and characterization of the catalytic domain of Src expressed in Schizosaccharomyces pombe. Comparison of unphosphorylated and tyrosine phosphorylated species. Eur J Biochem. 240:756–764.
  • Williams DM, Wang D, Cole PA. 2000. Chemical rescue of a mutant protein-tyrosine kinase. J Biol Chem. 275:38127–38130.
  • Wong L, Lieser S, Chie-Leon B, Miyashita O, Aubol B, Shaffer J, Onuchic JN, Jennings PA, Woods VLJr, Adams JA. 2004. Dynamic coupling between the SH2 domain and active site of the COOH terminal Src kinase, Csk. J Mol Biol. 341:93–106.
  • Wong L, Lieser SA, Miyashita O, Miller M, Tasken K, Onuchic JN, Adams JA, Woods VLJr, Jennings PA. 2005. Coupled motions in the SH2 and kinase domains of Csk control Src phosphorylation. J Mol Biol. 351:131–143.
  • Xu W, Harrison SC, Eck MJ. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 385:595–602.
  • Yaqub S, Abrahamsen H, Zimmerman B, Kholod N, Torgersen KM, Mustelin T, Herberg FW, Tasken K, Vang T. 2003. Activation of C-terminal Src kinase (Csk) by phosphorylation at serine-364 depends on the Csk-Src homology 3 domain. Biochem J. 372:271–278.
  • Yeatman TJ. 2004. A renaissance for SRC. Nat Rev Cancer. 4:470–480.
  • Zagozdzon R, Kaminski R, Fu Y, Fu W, Bougeret C, Avraham HK. 2006. Csk homologous kinase (CHK), unlike Csk, enhances MAPK activation via Ras-mediated signaling in a Src-independent manner. Cell Signal. 18:871–881.
  • Zhang J, Yang PL, Gray NS. 2009. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer. 9:28–39.
  • Zhu F, Choi BY, Ma WY, Zhao Z, Zhang Y, Cho YY, Choi HS, Imamoto A, Bode AM, Dong Z. 2006. COOH-terminal Src kinase-mediated c-Jun phosphorylation promotes c-Jun degradation and inhibits cell transformation. Cancer Res. 66:5729–5736.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.