Regulation of the Src family kinases by Csk

International Journal of Biological Sciences

Volumn 8, Issue 10, 2012, Pages 1385-1397

  Okada, Masato ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Csk; Src family; Tyrosine kinases

Indexed keywords

CSK TYROSINE PROTEIN KINASE; CSK TYROSINE-PROTEIN KINASE; PROTEIN TYROSINE KINASE;

AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYLOGENY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BINDING SITES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SRC-FAMILY KINASES;

EID: 84869780894     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.5141     Document Type: Review

References (97)

1. Hunter T. Tyrosine phosphorylation: thirty years and counting. Curr Opin Cell Biol. 2009; 21: 140-146.
2. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature. 2001; 411: 355-365.
3. Brown M, Cooper J. Regulation, substrates and functions of src. Biochim Biophys Acta. 1996; 1287: 121-149.
4. Thomas S, Brugge J. Cellular Functions regulated by Src Family Kinases. Ann Rev Cell Biol. 1997; 13: 513-609.
5. Wilde A, Beattie EC, Lem L, Riethof DA, Liu SH, Mobley WC, et al. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell. 1999; 96: 677-687.
6. Bishop JM, Baker B, Fujita D, McCombe P, Sheiness D, Smith K, et al. Genesis of a virus-transforming gene. National Cancer Institute monograph. 1978;: 219-223.
7. Hunter T. Protein phosphorylated by the RSV transforming function. Cell. 1980; 22: 647-8.
8. Varmus HE, Cohen JC, Hughes SH, Majors J, Bishop JM. The origin and structure of endogenous retroviral DNA. Annals of the New York Academy of Sciences. 1980; 354: 379-383.
9. Toyoshima K, Yoshida M, Kawai S, Kitamura N, Yamamoto T, Segawa K. Oncogene and its production of an avian sarcoma virus Y73. Princess Takamatsu Symp. 1982; 12: 275-283.
10. Takeya T, Hanafusa H. Structure and sequence of the cellular gene homologous to the RSV src gene and the mechanism for generating the transforming virus. Cell. 1983; 32: 881-890.
11. Hanafusa H, Halpern CC, Buchhagen DL, Kawai S. Recovery of avian sarcoma virus from tumors induced by transformation-defective mutants. J Exp Med. 1977; 146: 1735-1747.
12. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer. 2004; 4: 470-480.
13. Frame M. Newest findings on the oldest oncogene; how activated src does it. J Cell Sci. 2004; 117: 989-998.
14. Oneyama C, Iino T, Saito K, Suzuki K, Ogawa A, Okada M. Transforming potential of Src family kinases is limited by the cholesterol-enriched membrane microdomain. Mol Cell Biol. 2009; 29: 6462-6472.
15. Courtneidge SA. Activation of the pp60c-src kinase by middle T antigen binding or by dephosphorylation. EMBO J. 1985; 4: 1471-1477.
16. Cooper JA, Gould KL, Cartwright CA, Hunter T. Tyr527 is phosphorylated in pp60c-src: implications for regulation. Science. 1986; 231: 1431-1434.
17. Jove R, Hanafusa H. Cell transformation by the viral src oncogene. Annu Rev Cell Biol. 1987; 3: 31-56.
18. Cooper JA, Howell B. The when and how of Src regulation. Cell. 1993; 73: 1051-1054. doi:0092-8674(93)90634-3 [pii].
19. Cowan-Jacob SW, Fendrich G, Manley PW, Jahnke W, Fabbro D, Liebetanz J, et al. The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure. 2005; 13: 861-871.
20. Xu W, Harrison S, Eck M. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 1997; 385: 595-602.
21. Young MA, Gonfloni S, Superti-Furga G, Roux B, Kuriyan J. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell. 2001; 105: 115-126.
22. Knighton DR, Xuong NH, Taylor SS, Sowadski JM. Crystallization studies of cAMP-dependent protein kinase. Cocrystals of the catalytic subunit with a 20 amino acid residue peptide inhibitor and MgATP diffract to 3.0 A resolution. J Mol Biol. 1991; 220: 217-220.
23. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, et al. SH2 domains recognize specific phosphopeptide sequences. Cell. 1993; 72: 767-778.
24. Harte MT, Hildebrand JD, Burnham MR, Bouton AH, Parsons JT. p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J Biol Chem. 1996; 271: 13649-13655.
25. Courtneidge SA, Dhand R, Pilat D, Twamley GM, Waterfield MD, Roussel MF. Activation of Src family kinases by colony stimulating factor-1, and their association with its receptor. EMBO J. 1993; 12: 943-950.
26. Kypta RM, Goldberg Y, Ulug ET, Courtneidge SA. Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell. 1990; 62: 481-492.
27. Cheadle C, Ivashchenko Y, South V, Searfoss GH, French S, Howk R, et al. Identification of a Src SH3 domain binding motif by screening a random phage display library. J Biol Chem. 1994; 269: 24034-24039.
28. Seals DF, Azucena EF, Jr., Pass I, Tesfay L, Gordon R, Woodrow M, et al. The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell. 2005; 7: 155-165.
29. Liu X, Marengere LE, Koch CA, Pawson T. The v-Src SH3 domain binds phosphatidylinositol 3'-kinase. Mol Cell Biol. 1993; 13: 5225-5232.
30. Kuroiwa M, Oneyama C, Nada S, Okada M. The guanine nucleotide exchange factor Arhgef5 plays crucial roles in Src-induced podosome formation. J Cell Sci. 2011; 124: 1726-1738.
31. Hakak Y, Martin GS. Ubiquitin-dependent degradation of active Src. Curr Biol. 1999; 9: 1039-1042.
32. Martinez R, Mathey-Prevot B, Bernards A, Baltimore D. Neuronal pp60c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science. 1987; 237: 411-5.
33. Sorge LK, Levy BT, Maness PF. pp60c-src is developmentally regulated in the neural retina. Cell. 1984; 36: 249-257.
34. 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. 1988; 104: 297-305.
35. 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. 1988; 154: 796-802.
36. Okada M, Nada S, Yamanashi Y, Yamamoto T, Nakagawa H. CSK: a protein-tyrosine kinase involved in regulation of src family kinases. J Biol Chem. 1991; 266: 24249-24252.
37. Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature. 1991; 351: 69-72.
38. Bergman M, Mustelin T, Oetken C, Partanen J, Flint NA, Amrein KE, et al. The human p50csk tyrosine kinase phosphorylates p56lck at Tyr-505 and down regulates its catalytic activity. EMBO J. 1992; 11: 2919-2924.
39. Sabe H, Knudsen B, Okada M, Nada S, Nakagawa H, Hanafusa H. Molecular cloning and expression of chicken C-terminal Src kinase: lack of stable association with c-Src protein. Proc Natl Acad Sci U S A. 1992; 89: 2190-2194.
40. Sabe H, Okada M, Nakagawa H, Hanafusa H. Activation of c-Src in cells bearing v-Crk and its suppression by Csk. Mol Cell Biol. 1992; 12: 4706-4713.
41. Nada S, Yagi T, Takeda H, Tokunaga T, Nakagawa H, Ikawa Y, et al. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell. 1993; 73: 1125-1135.
42. Imamoto A, Soriano P. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell. 1993; 73: 1117-1124.
43. Thomas RM, Schmedt C, Novelli M, Choi BK, Skok J, Tarakhovsky A, et al. C-terminal SRC kinase controls acute inflammation and granulocyte adhesion. Immunity. 2004; 20: 181-191.
44. Schmedt C, Saijo K, Niidome T, Kuhn R, Aizawa S, Tarakhovsky A. Csk controls antigen receptor-mediated development and selection of T-lineage cells. Nature. 1998; 394: 901-904.
45. Yagi R, Waguri S, Sumikawa Y, Nada S, Oneyama C, Itami S, et al. C-terminal Src kinase controls development and maintenance of mouse squamous epithelia. EMBO J. 2007; 26: 1234-1244.
46. Nada S, Okada M, Aizawa S, Nakagawa H. Identification of major tyrosine-phosphorylated proteins in Csk-deficient cells. Oncogene. 1994; 9: 3571-3578.
47. Read RD, Bach EA, Cagan RL. Drosophila C-terminal Src kinase negatively regulates organ growth and cell proliferation through inhibition of the Src, Jun N-terminal kinase, and STAT pathways. Mol Cell Biol. 2004; 24: 6676-6689.
48. Takata N, Itoh B, Misaki K, Hirose T, Yonemura S, Okada M. Non-receptor tyrosine kinase CSK-1 controls pharyngeal muscle organization in Caenorhabditis elegans. Genes Cells. 2009; 14: 381-393.
49. Segawa Y, Suga H, Iwabe N, Oneyama C, Akagi T, Miyata T, et al. Functional development of Src tyrosine kinases during evolution from a unicellular ancestor to multicellular animals. Proc Natl Acad Sci U S A. 2006; 103: 12021-12026.
50. Bennett BD, Cowley S, Jiang S, London R, Deng B, Grabarek J, et al. Identification and characterization of a novel tyrosine kinase from megakaryocytes. J Biol Chem. 1994; 269: 1068-1074.
51. Sakano S, Iwama A, Inazawa J, Ariyama T, Ohno M, Suda T. Molecular cloning of a novel non-receptor tyrosine kinase, HYL (hematopoietic consensus tyrosine-lacking kinase). Oncogene. 1994; 9: 1155-1161.
52. Klages S, Adam D, Class K, Fargnoli J, Bolen JB, Penhallow RC. Ctk: a protein-tyrosine kinase related to Csk that defines an enzyme family. Proc Natl Acad Sci U S A. 1994; 91: 2597-2601.
53. McVicar DW, Lal BK, Lloyd A, Kawamura M, Chen YQ, Zhang X, et al. Molecular cloning of lsk, a carboxyl-terminal src kinase (csk) related gene, expressed in leukocytes. Oncogene. 1994; 9: 2037-2044.
54. Hamaguchi I, Iwama A, Yamaguchi N, Sakano S, Matsuda Y, Suda T. Characterization of mouse non-receptor tyrosine kinase gene, HYL. Oncogene. 1994; 9: 3371-3374.
55. Grgurevich S, Linnekin D, Musso T, Zhang X, Modi W, Varesio L, et al. The Csk-like proteins Lsk, Hyl, and Matk represent the same Csk homologous kinase (Chk) and are regulated by stem cell factor in the megakaryoblastic cell line MO7e. Growth Factors. 1997; 14: 103-115.
56. Hamaguchi I, Yamaguchi N, Suda J, Iwama A, Hirao A, Hashiyama M, et al. Analysis of CSK homologous kinase (CHK/HYL) in hematopoiesis by utilizing gene knockout mice. Biochem Biophys Res Commun. 1996; 224: 172-179.
57. Lee S, Ayrapetov MK, Kemble DJ, Parang K, Sun G. Docking-based substrate recognition by the catalytic domain of a protein tyrosine kinase, C-terminal Src kinase (Csk). J Biol Chem. 2006; 281: 8183-8189.
58. Lee S, Lin X, Nam NH, Parang K, Sun G. Determination of the substrate-docking site of protein tyrosine kinase C-terminal Src kinase. Proc Natl Acad Sci U S A. 2003; 100: 14707-14712.
59. Levinson NM, Seeliger MA, Cole PA, Kuriyan J. Structural basis for the recognition of c-Src by its inactivator Csk. Cell. 2008; 134: 124-134.
60. Sabe H, Hata A, Okada M, Nakagawa H, Hanafusa H. Analysis of the binding of the Src homology 2 domain of Csk to tyrosine-phosphorylated proteins in the suppression and mitotic activation of c-Src. Proc Natl Acad Sci U S A. 1994; 91: 3984-3988.
61. D'Arco M, Giniatullin R, Leone V, Carloni P, Birsa N, Nair A, et al. 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. 2009; 284: 21393-21401.
62. Zhu F, Choi BY, Ma WY, Zhao Z, Zhang Y, Cho YY, et al. COOH-terminal Src kinase-mediated c-Jun phosphorylation promotes c-Jun degradation and inhibits cell transformation. Cancer Res. 2006; 66: 5729-5736.
63. Stewart RA, Li DM, Huang H, Xu T. A genetic screen for modifiers of the lats tumor suppressor gene identifies C-terminal Src kinase as a regulator of cell proliferation in Drosophila. Oncogene. 2003; 22: 6436-6444.
64. Roskoski R, Jr. Src kinase regulation by phosphorylation and dephosphorylation. Biochem Biophys Res Commun. 2005; 331: 1-14.
65. Zheng XM, Wang Y, Pallen CJ. Cell transformation and activation of pp60c-src by overexpression of a protein tyrosine phosphatase. Nature. 1992; 359: 336-339.
66. Granot-Attas S, Elson A. Protein tyrosine phosphatase epsilon activates Yes and Fyn in Neu-induced mammary tumor cells. Exp Cell Res. 2004; 294: 236-243.
67. Fang KS, Sabe H, Saito H, Hanafusa H. Comparative study of three protein-tyrosine phosphatases. Chicken protein-tyrosine phosphatase lambda dephosphorylates c-Src tyrosine 527. J Biol Chem. 1994; 269: 20194-20200.
68. Mustelin T, Altman A. Dephosphorylation and activation of the T cell tyrosine kinase pp56lck by the leukocyte common antigen (CD45). Oncogene. 1990; 5: 809-813.
69. Bjorge JD, Pang A, Fujita DJ. Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem. 2000; 275: 41439-41446.
70. Somani AK, Bignon JS, Mills GB, Siminovitch KA, Branch DR. Src kinase activity is regulated by the SHP-1 protein-tyrosine phosphatase. J Biol Chem. 1997; 272: 21113-21119.
71. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T, et al. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Molecular cell. 2004; 13: 341-355.
72. Ogawa A, Takayama Y, Sakai H, Chong KT, Takeuchi S, Nakagawa A, et al. Structure of the carboxyl-terminal Src kinase, Csk. J Biol Chem. 2002; 277: 14351-14354.
73. Wong L, Lieser SA, Miyashita O, Miller M, Tasken K, Onuchic JN, et al. Coupled motions in the SH2 and kinase domains of Csk control Src phosphorylation. J Mol Biol. 2005; 351: 131-143.
74. Cao H, Courchesne WE, Mastick CC. A phosphotyrosine-dependent protein interaction screen reveals a role for phosphorylation of caveolin-1 on tyrosine 14: recruitment of C-terminal Src kinase. J Biol Chem. 2002; 277: 8771-8774.
75. Sabe H, Hata A, Okada M, Nakagawa H, Hanafusa H. Analysis of the binding of the Src homology 2 domain of Csk to tyrosine-phosphorylated proteins in the suppression and mitotic activation of c-Src. Proc Natl Acad Sci U S A. 1994; 91: 3984-3988.
76. Zhou J, Scholes J, Hsieh JT. Characterization of a novel negative regulator (DOC-2/DAB2) of c-Src in normal prostatic epithelium and cancer. J Biol Chem. 2003; 278: 6936-6941.
77. Baumeister U, Funke R, Ebnet K, Vorschmitt H, Koch S, Vestweber D. Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J. 2005; 24: 1686-1695.
78. Arbet-Engels C, Tartare-Deckert S, Eckhart W. C-terminal Src kinase associates with ligand-stimulated insulin-like growth factor-I receptor. J Biol Chem. 1999; 274: 5422-5428.
79. Tobe K, Sabe H, Yamamoto T, Yamauchi T, Asai S, Kaburagi Y, et al. Csk enhances insulin-stimulated dephosphorylation of focal adhesion proteins. Mol Cell Biol. 1996; 16: 4765-4772.
80. Horejsí V. Transmembrane adaptor proteins in membrane microdomains: important regulators of immunoreceptor signaling. Immunol Lett. 2004; 92: 43-49.
81. Brdicková N, Brdicka T, Angelisová P, Horváth O, Spicka J, Hilgert I, et al. LIME: a new membrane Raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J Exp Med. 2003; 198: 1453-1462.
82. Kawabuchi M, Satomi Y, Takao T, Shimonishi Y, Nada S, Nagai K, et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 2000; 404: 999-1003.
83. Brdicka T, Pavlistova D, Leo A, Bruyns E, Korinek V, Angelisova P, et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med. 2000; 191: 1591-1604.
84. Oneyama C, Hikita T, Enya K, Dobenecker MW, Saito K, Nada S, et al. The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src. Molecular cell. 2008; 30: 426-436.
85. Kanou T, Oneyama C, Kawahara K, Okimura A, Ohta M, Ikeda N, et al. The transmembrane adaptor Cbp/PAG1 controls the malignant potential of human non-small cell lung cancers that have c-src upregulation. Mol Cancer Res. 2010; 9: 103-114.
86. Suzuki K, Oneyama C, Kimura H, Tajima S, Okada M. Down-regulation of the tumor suppressor C-terminal Src kinase (Csk)-binding protein (Cbp)/PAG1 is mediated by epigenetic histone modifications via the mitogen-activated protein kinase (MAPK)/phosphatidylinositol 3-kinase (PI3K) pathway. J Biol Chem. 2011; 286: 15698-15706.
87. Howell BW, Cooper JA. Csk suppression of Src involves movement of Csk to sites of Src activity. Mol Cell Biol. 1994; 14: 5402-5411.
88. Takeuchi M, Kuramochi S, Fusaki N, Nada S, Kawamura-Tsuzuku J, Matsuda S, et al. Functional and physical interaction of protein-tyrosine kinases Fyn and Csk in the T-cell signaling system. J Biol Chem. 1993; 268: 27413-27419.
89. Cloutier JF, Veillette A. Association of inhibitory tyrosine protein kinase p50csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO J. 1996; 15: 4909-4918.
90. Veillette A, Rhee I, Souza CM, Davidson D. PEST family phosphatases in immunity, autoimmunity, and autoinflammatory disorders. Immunol Rev. 2009; 228: 312-324.
91. Vang T, Liu WH, Delacroix L, Wu S, Vasile S, Dahl R, et al. LYP inhibits T-cell activation when dissociated from CSK. Nat Chem Biol. 2012; 8: 437-446.
92. Zhong MC, Veillette A. Immunology: Csk keeps LYP on a leash. Nat Chem Biol. 2012; 8: 412-423.
93. Mills JE, Whitford PC, Shaffer J, Onuchic JN, Adams JA, Jennings PA. A novel disulfide bond in the SH2 Domain of the C-terminal Src kinase controls catalytic activity. J Mol Biol. 2007; 365: 1460-1468.
94. Yaqub S, Abrahamsen H, Zimmerman B, Kholod N, Torgersen KM, Mustelin T, et al. Activation of C-terminal Src kinase (Csk) by phosphorylation at serine-364 depends on the Csk-Src homology 3 domain. Biochem J. 2003; 372: 271-278.
95. Inomata M, Takayama Y, Kiyama H, Nada S, Okada M, Nakagawa H. Regulation of Src family kinases in the developing rat brain: correlation with their regulator kinase, Csk. J Biochem. 1994; 116: 386-392.
96. Masaki T, Okada M, Tokuda M, Shiratori Y, Hatase O, Shirai M, et al. Reduced C-terminal Src kinase (Csk) activities in hepatocellular carcinoma. Hepatology. 1999; 29: 379-384.
97. Watanabe N, Matsuda S, Kuramochi S, Tsuzuku J, Yamamoto T, Endo K. Expression of C-terminal src kinase in human colorectal cancer cell lines. Jpn J Clin Oncol. 1995; 25: 5-9.