Cockayne syndrome protein B interacts with and is phosphorylated by c-Abl tyrosine kinase

Nucleic Acids Research

Volumn 35, Issue 15, 2007, Pages 4941-4951

  Imam, Syed Z ^a,d   Indig, Fred E ^a   Cheng, Wen Hsing ^a   Saxena, Satya P ^a   Stevnsner, Tinna ^b   Kufe, Donald ^c   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b AARHUS UNIVERSITY   (Denmark)

^c HARVARD MEDICAL SCHOOL   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; COCKAYNE SYNDROME GROUP B PROTEIN; HYDROGEN PEROXIDE; IMATINIB; PHOSPHOPROTEIN; PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NUCLEOLUS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CELL LINE; CELLS, CULTURED; DNA HELICASES; DNA REPAIR ENZYMES; HUMANS; MICE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-ABL; TYROSINE;

EID: 34548570178     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm386     Document Type: Article

References (50)

1. van Hoffen,A., Natarajan,A.T., Mayne,L.V., van Zeeland,A.A. and Mullenders,L.H. (1993) Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells. Nucleic Acids Res., 21, 5890-5895.
2. Balajee,A.S. and Bohr,V.A. (2000) Genomic heterogeneity of nucleotide excision repair. Gene, 250, 15-30.
3. Licht CL, Stevnsner T, Bohr VA. (2004). Cockayne syndrome group B cellular and biochemical functions. Am. J. Hum. Genet., 6, 1217-39.
4. Mayne,L.V. and Lehmann,A.R. (1982) Failure of RNA synthesis to recover after UV irradiation: And early defect in cells from individuals with Cockayne's syndrome and xeroderma pigmentosum. Cancer Res., 42 1473-1478.
5. Friedberg,E.C. (1996) Cockayne syndrome-a primary defect in DNA repair, transcription, both or neither? Bioessays, 18, 731-738.
6. Troelstra,C., van Gool,A., De Wit,J., Vermeulen,W., Bootsma,D. and Hoeijmakers,H.J. (1992) ERCC6a member of a subfamily of putative helicases is involved in Cockaynes's syndrome and preferential repair of active genes. Cell, 71, 939-953.
7. Tuo,J., Jaruga,P., Rodriguez,H., Bohr,V.A. and Dizdaroglu,M. (2003) Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. FASEB J., 17, 668-674.
8. Tuo,J., Muftuoglu,M., Chen,C., Jaruga,P., Selzer,R.R., Brosh,R.M.Jr, Rodriguez,H., Dizdaroglu,M. and Bohr,V.A. (2001) The Cockayne Syndrome group B gene product is involved in general genome base excision repair of 8-hydroxyguanine in DNA. J. Biol. Chem., 276, 45772-45779.
9. Tuo,J., Jaruga,P., Rodriguez,H., Dizdaroglu,M. and Bohr,V.A. (2002) The cockayne syndrome group B gene product is involved in cellular repair of 8-hydroxyadenine in DNA. J. Biol. Chem., 277, 30832-30837.
10. Sun,X., Majumder,P., Shioya,H., Wu,F., Kumar,S., Weichselbaum,R., Kharbanda,S. and Kufe,D. (2000) Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J. Biol. Chem., 275 17237-17240.
11. Kharbanda,S., Ren,R., Pandey,P., Shafman,T.D., Feller,S.M., Weichselbaum,R.R. and Kufe,D.W. (1995) Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature, 376, 785-788.
12. Jin,S., Kharbanda,S., Mayer,B., Kufe,D. and Weaver,D.T. (1997) Binding of Ku and c-Abl at the kinase homology region of DNA-dependent protein kinase catalytic subunit. J Biol. Chem., 272, 24763-24766.
13. Kharbanda,S., Pandey,P., Jin,S., Inoue,S., Bharti,A., Yuan,Z.M., Weichselbaum,R., Weaver,D. and Kufe,D. (1997) Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature, 386 732-735.
14. Yuan,Z.M., Huang,Y., Ishiko,T., Nakada,S., Utsugisawa,T., Kharbanda,S., Wang,R., Sung,P., Shinohara,A. et al. (1998) Regulation of Rad51 function by c-Abl in response to DNA damage. J. Biol. Chem., 273, 3799-3802.
15. Sun,X., Wu,F., Datta,R., Kharbanda,S. and Kufe,D. (2000) Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem., 275, 7470-7473.
16. Sun,X., Majumder,P., Shioya,H., Wu,F., Kumar,S., Weichselbaum,R., Kharbanda,S. and Kufe,D. (2000) Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J. Biol. Chem., 275 17237-17240.
17. Sun,X., Wu,F., Datta,R., Kharbanda,S. and Kufe,D. (2000) Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem., 275, 7470-7473.
18. Jin,S., Kharbanda,S., Mayer,B., Kufe,D. and Weaver,D.T. (1997) Binding of Ku and c-Abl at the kinase homology region of DNA-dependent protein kinase catalytic subunit. J Biol. Chem., 272, 24763-24766.
19. Kharbanda,S., Pandey,P., Jin,S., Inoue,S., Bharti,A., Yuan,Z.M., Weichselbaum,R., Weaver,D. and Kufe,D. (1997) Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature, 386 732-735.
20. Agami,R., Blandino,G., Oren,M. and Shaul,Y. (1999) Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature, 399, 809-813.
21. Gong,J.G., Costanzo,A., Yang,H.Q., Melino,G., Kaelin,W.G.Jr, Levrero,M. and Wang,J.Y. (1999) The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature, 399 806-809.
22. Yoshida,K., Komatsu,K., Wang,H.G. and Kufe,D. (2002) c-Abl tyrosine kinase regulates the human Rad9 checkpoint protein in response to DNA damage. Mol. Cell Biol., 22, 3292-3300.
23. Yuan,Z.M., Huang,Y., Fan,M.M., Sawyers,C., Kharbanda,S. and Kufe,D. (1996) Genotoxic drugs induce interaction of the c-Abl tyrosine kinase and the tumor suppressor protein p53. J. Biol. Chem., 271, 26457-26460.
24. Yoshida,K., Komatsu,K., Wang,H.G. and Kufe,D. (2002) c-Abl tyrosine kinase regulates the human Rad9 checkpoint protein in response to DNA damage. Mol. Cell. Biol., 22, 3292-3300.
25. Yuan,Z.M., Huang,Y., Fan,M.M., Sawyers,C., Kharbanda,S. and Kufe,D. (1996) Genotoxic drugs induce interaction of the c-Abl tyrosine kinase and the tumor suppressor protein p53. J. Biol. Chem., 271, 26457-26460.
26. Yuan,Z.M., Shioya,H., Ishiko,T., Sun,X., Gu,J., Huang,Y.Y., Lu,H., Kharbanda,S., Weichselbaum,R. et al. (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature 399, 814-817.
27. Sun,X., Majumder,P., Shioya,H., Wu,F., Kumar,S., Weichselbaum,R., Kharbanda,S. and Kufe,D. (2000) Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J. Biol. Chem., 275 17237-17240.
28. Sun,X., Wu,F., Datta,R., Kharbanda,S. and Kufe,D. (2000) Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem., 275, 7470-7473.
29. Kay,B.K., Williamson,M.P. and Sudol,M. (2000) The importance of being proline: The interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J., 14, 231-241.
30. Mayer,B.J. (2001) SH3 domains: Complexity in moderation. J. Cell Sci. 114, 1253-1263.
31. Yu,D., Khan,E., Khaleque,M.A., Lee,J., Laco,G., Kohlhagen,G., Kharbanda,S., Cheng,Y.C., Pommier,Y. et al. (2004) Phosphorylation of DNA topoisomerase I by the c-Abl tyrosine kinase confers camptothecin sensitivity. J. Biol. Chem., 279, 51851-51861.
32. Conilleau,S., Takizawa,Y., Tachiwana,H., Fleury,F., Kurumizaka,H. and Takahashi,M. (2004) Location of tyrosine 315, a target for phosphorylation by cAbl tyrosine kinase, at the edge of the subunit-subunit interface of the human Rad51 filament. J. Mol. Biol. 339, 797-804.
33. Yoshida,K., Komatsu,K., Wang,H.G. and Kufe,D. (2002) c-Abl tyrosine kinase regulates the human Rad9 checkpoint protein in response to DNA damage. Mol. Cell. Biol., 22, 3292-3300.
34. Christiansen,M., Stevnsner,T., Modin,C., Martensen,P.M., Brosh,R.M.Jr and Bohr,V.A. (2003) Functional consequences of mutations in the conserved SF2 motifs and post-translational phosphorylation of the CSB protein. Nucleic Acids Res., 31, 963-973.
35. Cheng,W.H., von,K.C., Opresko,P.L., Fields,K.M., Ren,J., Kufe,D. and Bohr,V.A. (2003) Werner syndrome protein phosphorylation by abl tyrosine kinase regulates its activity and distribution. Mol. Cell Biol., 23, 6385-6395.
36. Mirzoeva,O.K. and Petrini,J.H. (2001) DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell Biol., 21, 281-288.
37. Partridge,J.J., Lopreiato,J.O.Jr, Latterich,M. and Indig,F.E. (2003) DNA damage modulates nucleolar interaction of the Werner protein with the AAA ATPase p97/VCP. Mol. Cell Biol., 14, 4221-4229.
38. Kumar,S., Mishra,N., Raina,D., Saxena,S. and Kufe,D. (2003) Abrogation of the cell death response to oxidative stress by the c-Abl tyrosine kinase inhibitor STI571. Mol. Pharmacol., 63, 276-282.
39. Sawyers,C.L., McLaughlin,J., Goga,A., Havlik,M. and Witte,O. (1994) The nuclear tyrosine kinase c-Abl negatively regulates cell growth. Cell 77, 121-131.
40. Bartova,E., Harnicarova,A., Pachernik,J. and Kozubek,S. (2005) Nuclear topography and expression of the BCR/ABL fusion gene and its protein level influenced by cell differentiation and RNA interference. Leuk. Res., 29, 901-913.
41. Christiansen,M., Stevnsner,T., Modin,C., Martensen,P.M., Brosh,R.M.Jr. and Bohr,V.A. (2003) Functional consequences of mutations in the conserved SF2 motifs and post-translational phosphorylation of the CSB protein. Nucleic Acids Res., 31, 963-973.
42. Cao,C., Leng,Y., Huang,W., Liu,X. and Kufe,D. (2003) Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases. J. Biol. Chem., 278, 39609-39614.
43. Cao,C., Leng,Y. and Kufe,D. (2003) Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J. Biol. Chem., 278, 29667-29675.
44. Tuo,J., Jaruga,P., Rodriguez,H., Bohr,V.A. and Dizdaroglu,M. (2003) Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. FASEB J., 17, 668-674.
45. Thorslund,T., von,K.C., Harrigan,J.A., Indig,F.E., Christiansen,M., Stevnsner,T. and Bohr,V.A. (2005) Cooperation of the Cockayne syndrome group B protein and poly(ADP-ribose) polymerase 1 in the response to oxidative stress. Mol. Cell Biol., 25, 7625-7636.
46. Trapp,C., Reite,K., Klungland,A. and Epe,B. (2007) Deficiency of the Cockayne syndrome B (CSB) gene aggravates the genomic instability caused by endogenous oxidative DNA base damage in mice. Oncogene, In Press.
47. Thorslund,T., Sunesen,M., Bohr,V.A. and Stevnsner,T. (2002) Repair of 8-oxoG is slower in endogenous nuclear genes than in mitochondrial DNA and is without strand bias. DNA Repair (Amst.), 1, 261-273.
48. Ren,R. (2005) Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat. Rev. Cancer, 5, 172-183.
49. Lu,Y., Mani,S., Kandimalla,E.R., Yu,D., Agrawal,S., States,J.C. and Bregman,D.B. (2001) The Cockayne syndrome group B DNA repair protein as an anti-cancer target. Int. J. Oncol., 19, 1089-1097.
50. Lu,Y., Lian,H., Sharma,P., Schreiber-Agus,N., Russell,R.G., Chin,L., van der Horst,G.T. and Bregman,D.B. (2001) Disruption of the Cockayne syndrome B gene impairs spontaneous tumorigenesis in cancer-predisposed Ink4a/ARF knockout mice. Mol. Cell. Biol., 21, 1810-1818.