Lyn tyrosine kinase promotes silencing of ATM-dependent checkpoint signaling during recovery from DNA double-strand breaks

Biochemical and Biophysical Research Communications

Volumn 452, Issue 3, 2014, Pages 542-547

  Fukumoto, Yasunori ^a   Kuki, Kazumasa ^a   Morii, Mariko ^a   Miura, Takahito ^a   Honda, Takuya ^a   Ishibashi, Kenichi ^a,b   Hasegawa, Hitomi ^a   Kubota, Sho ^a   Ide, Yudai ^a   Yamaguchi, Noritaka ^a   Nakayama, Yuji ^a,c   Yamaguchi, Naoto ^a  

^a CHIBA UNIVERSITY   (Japan)

^b TEIKYO UNIVERSITY   (Japan)

^c KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Cell cycle; Checkpoint control; Checkpoint recovery; DNA damage; DNA damage response; Src

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; HISTONE H2AX; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; ATM PROTEIN, HUMAN; CHEK2 PROTEIN, HUMAN; DOXORUBICIN; GYRASE INHIBITOR; H2AFX PROTEIN, HUMAN; HISTONE; LYN PROTEIN-TYROSINE KINASE; REPRESSOR PROTEIN; SMALL INTERFERING RNA; TRIM28 PROTEIN, HUMAN;

ARTICLE; DNA DAMAGE CHECKPOINT; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; CHECKPOINT KINASE 2; DNA BREAKS, DOUBLE-STRANDED; DOXORUBICIN; GENE EXPRESSION REGULATION; HELA CELLS; HISTONES; HUMANS; PHOSPHORYLATION; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TOPOISOMERASE II INHIBITORS;

EID: 84907567976     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2014.08.113     Document Type: Article

References (44)

1. T.M. Calonge, and M.J. O'Connell Turning off the G2 DNA damage checkpoint DNA Repair 7 2008 136 140
2. C. Clémenson, and M.C. Marsolier-Kergoat DNA damage checkpoint inactivation: adaptation and recovery DNA Repair 8 2009 1101 1109
3. H.C. Reinhardt, and M.B. Yaffe Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2 Curr. Opin. Cell Biol. 21 2009 245 255
4. H.D. Thompson Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography Mutat. Res. 751 2012 158 246
5. Y. Ziv, D. Bielopolski, Y. Galanty, C. Lukas, Y. Taya, D.C. Schultz, J. Lukas, S. Bekker-Jensen, J. Bartek, and Y. Shiloh Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and Kap-1 dependent pathway Nat. Cell Biol. 8 2006 870 876
6. D.E. White, D. Negorev, H. Peng, A.V. Ivanov, G.G. Maul, and F.J. Rauscher III Kap1, a novel substrate for PIKK family members, colocalizes with numerous damage response factors at DNA lesions Cancer Res. 66 2006 11594 11599
7. D. Zhang, K. Zaugg, T.W. Mak, and S.J. Elledge A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response Cell 126 2006 529 542
8. E.M. Kass, J. Ahn, T. Tanaka, W.A. Freed-Pastor, S. Keezer, and C. Prives Stability of checkpoint kinase 2 is regulated via phosphorylation at serine 456 J. Biol. Chem. 282 2007 30311 30321
9. C.M. Lovly, L. Yan, C.E. Ryan, S. Takeda, and H. Piwnica-Worms Regulation of Chk2 ubiquitylation and signaling through autophosphorylation of serine 379 Mol. Cell. Biol. 28 2008 5874 5885
10. D.H. Lee, A.A. Goodarzi, G.O. Adelmant, Y. Pan, P.A. Jeggo, J.A. Marto, and D. Chowdhury Phosphoproteomic analysis reveals that PP4 dephosphorylates KAP-1 impacting the DNA damage response EMBO J. 31 2012 2403 2415
11. S.M. Thomas, and J.S. Brugge Cellular functions regulated by Src family kinases Annu. Rev. Cell Dev. Biol. 13 1997 513 609
12. V. Radha, S. Nambirajan, and G. Swarup Association of Lyn tyrosine kinase with the nuclear matrix and cell-cycle-dependent changes in matrix-associated tyrosine kinase activity Eur. J. Biochem. 236 1996 352 359
13. A.K. Jain, and A.K. Jaiswal GSK-3β acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2 J. Biol. Chem. 282 2007 16502 16510
14. P. Paliwal, V. Radha, and G. Swarup Regulation of p73 by Hck through kinase-dependent and independent mechanisms BMC Mol. Biol. 8 2007 45
15. K. Ikeda, Y. Nakayama, Y. Obata, T. Kuga, K. Kasahara, Y. Fukumoto, and N. Yamaguchi Nuclear localization of Lyn tyrosine kinase mediated by inhibition of its kinase activity Exp. Cell Res. 314 2008 3392 3404
16. A. Takahashi, Y. Obata, Y. Fukumoto, Y. Nakayama, K. Kasahara, T. Kuga, Y. Higashiyama, T. Saito, K.K. Yokoyama, and N. Yamaguchi Nuclear localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization Exp. Cell Res. 315 2009 1117 1141
17. S. Kharbanda, Z.M. Yuan, E. Rubin, R. Weichselbaum, and D. Kufe Activation of Src-like p56/p53 Lyn tyrosine kinase by ionizing radiation J. Biol. Chem. 269 1994 20739 20743
18. S. Kharbanda, A. Saleem, Z.M. Yuan, S. Kraeft, R. Weichselbaum, L.B. Chen, and D. Kufe Nuclear signaling induced by ionizing radiation involves colocalization of the activated p56/p53 Lyn tyrosine kinase with p34 cdc2 Cancer Res. 56 1996 3617 3621
19. S. Qin, Y. Minami, T. Kurosaki, and H. Yamamura Distinctive functions of Syk and Lyn in mediating osmotic stress- and ultraviolet C irradiation-induced apoptosis in chicken B cells J. Biol. Chem. 272 1997 17994 117999
20. A. Maruo, I. Oishi, K. Sada, M. Nomi, T. Kurosaki, Y. Minami, and H. Yamamura Protein tyrosine kinase Lyn mediates apoptosis induced by topoisomerase II inhibitors in DT40 cells Int. Immunol. 11 1999 1371 1380
21. K. Yoshida, R. Weichselbaum, S. Kharbanda, and D. Kufe Role for Lyn tyrosine kinase as a regulator of stress-activated protein kinase activity in response to DNA damage Mol. Cell. Biol. 20 2000 5370 5380
22. A.V. Grishin, O. Azhipa, I. Semenov, and S.J. Corey Interaction between growth arrest-DNA damage protein 34 and Src kinase Lyn negatively regulates genotoxic apoptosis Proc. Natl. Acad. Sci. U.S.A. 98 2001 10172 10177
23. Y. Fukumoto, M. Morii, T. Miura, S. Kubota, K. Ishibashi, T. Honda, A. Okamoto, N. Yamaguchi, A. Iwama, Y. Nakayama, and N. Yamaguchi Src family kinases promote silencing of ATR-Chk1 signaling in termination of DNA damage checkpoint J. Biol. Chem. 289 2014 12313 12329
24. S. Kubota, Y. Fukumoto, K. Aoyama, K. Ishibashi, R. Yuki, T. Morinaga, T. Honda, N. Yamaguchi, T. Kuga, T. Tomonaga, and N. Yamaguchi Phosphorylation of KRAB-associated protein 1 (KAP1) at Tyr-449, Tyr-458, and Tyr-517 by nuclear tyrosine kinases inhibits the association of KAP1 and heterochromatin protein 1α (HP1α) with heterochromatin J. Biol. Chem. 288 2013 17871 17883
25. Y. Fukumoto, Y. Obata, K. Ishibashi, N. Tamura, I. Kikuchi, K. Aoyama, Y. Hattori, K. Tsuda, Y. Nakayama, and N. Yamaguchi Cost-effective gene transfection by DNA compaction at pH 4.0 using acidified, long shelf-life polyethylenimine Cytotechnology 62 2010 73 82
26. Y. Obata, Y. Fukumoto, Y. Nakayama, T. Kuga, N. Dohmae, and N. Yamaguchi The Lyn kinase C-lobe mediates Golgi export of Lyn through conformation-dependent ACSL3 association J. Cell Sci. 123 2010 2649 2662
27. Y. Nakayama, A. Igarashi, I. Kikuchi, Y. Obata, Y. Fukumoto, and N. Yamaguchi Bleomycin-induced over-replication involves sustained inhibition of mitotic entry through the ATM/ATR pathway Exp. Cell Res. 315 2009 2515 2528
28. I. Kikuchi, Y. Nakayama, T. Morinaga, Y. Fukumoto, and N. Yamaguchi A decrease in cyclin B1 levels leads to polyploidization in DNA damage-induced senescence Cell Biol. Int. 34 2010 645 653
29. A. Slupianek, C. Schmutte, G. Tombline, M. Nieborowska-Skorska, G. Hoser, M.O. Nowicki, A.J. Pierce, R. Fishel, and T. Skorski BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance Mol. Cell 8 2001 795 806
30. J. Maurel, A.S. Martins, A. Poveda, J.A. López-Guerrero, R. Cubedo, A. Casado, J. Martinez-Trufero, J. Ramón Ayuso, A. Lopez-Pousa, X. Garcia-Albeniz, X. Garcia del Muro, and E. de Alava Imatinib plus low-dose doxorubicin in patients with advanced gastrointestinal stromal tumors refractory to high-dose imatinib: a phase I-II study by the Spanish Group for Research on Sarcomas Cancer 116 2010 3692 3701
31. D. White, I.U. Rafalska-Metcalf, A.V. Ivanov, A. Corsinotti, H. Peng, S.C. Lee, S.D. Trono, S.M. Janicki, and F.J. Rauscher III The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation Mol. Cancer Res. 10 2011 401 414
32. S.V. Kozlov, M.E. Graham, C. Peng, P. Chen, P.J. Robinson, and M.F. Lavin Involvement of novel autophosphorylation sites in ATM activation EMBO J. 25 2006 3504 3514
33. R.A. Blake, M.A. Broome, X. Liu, J. Wu, M. Gishizky, L. Sun, and S.A. Courtneidge SU6656, a selective Src family kinase inhibitor, used to probe growth factor signaling Mol. Cell. Biol. 20 2000 9018 9027
34. M.A. van Vugt, A. Brás, and R.H. Medema Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells Mol. Cell 15 2004 799 811
35. J. Li, and D.F. Stern Regulation of Chk2 by DNA-dependent protein kinase J. Biol. Chem. 280 2005 12041 12050
36. I. Hickson, Y. Zhao, C.J. Richardson, S.J. Green, N.M.B. Martin, A.I. Orr, P.M. Reaper, S.P. Jackson, N.J. Curtin, and G.C.M. Smith Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM Cancer Res. 64 2004 9152 9159
37. A. Jazayeri, J. Falck, C. Lukas, J. Bartek, G.C.M. Smith, J. Lukas, and S.P. Jackson ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks Nat. Cell Biol. 8 2006 37 45
38. I.M. Ward, and J. Chen Histone H2AX is phosphorylated in an ATR-dependent manner in response to replication stress J. Biol. Chem. 276 2001 47759 47762
39. Y. Matsui, Y. Nakayama, M. Okamoto, Y. Fukumoto, and N. Yamaguchi Enrichment of cell populations in metaphase, anaphase, and telophase by synchronization using nocodazole and blebbistatin: a novel method suitable for examining dynamic changes in proteins during mitotic progression Eur. J. Cell Biol. 91 2012 413 419
40. Y. Fukumoto, T. Miura, M. Morii, S. Kubota, T. Honda, S. Kubota, T. Morinaga, N. Yamaguchi, Y. Nakayama, and N. Yamaguchi V-Src inhibits the interaction between Rad17 and Rad9 and induces replication fork collapse Biochem. Biophys. Res. Commun. 450 2014 885 890
41. B. Xu, S.T. Kim, D.S. Lim, and M.B. Kastan Two molecularly distinct G2/M checkpoints are induced by ionizing irradiation Mol. Cell. Biol. 22 2002 1049 1059
42. A. Shibata, O. Barton, A.T. Noon, K. Dahm, D. Deckbar, A.A. Goodarzi, M. Löbrich, and P.A. Jeggo Role of ATM and the damage response mediator proteins 53BP1 and MDC1 in the maintenance of G2/M checkpoint arrest Mol. Cell. Biol. 30 2010 3371 3383
43. E.A. Kohn, C.J. Yoo, and A. Eastman The protein kinase C inhibitor Gö6976 is a potent inhibitor of DNA damage-induced S and G2 cell cycle checkpoints Cancer Res. 63 2003 31 35
44. Y. Ishimi, Y. Komamura-Kohno, H.J. Kwon, K. Yamada, and M. Nakanishi Identification of MCM4 as a target of the DNA replication block checkpoint system J. Biol. Chem. 278 2003 24644 24650