Cross talk of tyrosine kinases with the DNA damage signaling pathways

Nucleic Acids Research

Volumn 43, Issue 22, 2015, Pages 10588-10601

  Mahajan, Kiran ^a,b   Mahajan, Nupam P ^a,b  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; PROTEIN TYROSINE KINASE; CELL CYCLE PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL FATE; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; EPIGENETICS; GENE INTERACTION; GENE TARGETING; GENETIC REGULATION; HOMEOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; CELL CYCLE; GENETIC EPIGENESIS; METABOLISM;

CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; EPIGENESIS, GENETIC; HISTONES; HUMANS; PROTEIN-TYROSINE KINASES; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84964587601     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1166     Document Type: Article

References (160)

1. Krause, D.S. and Van Etten, R.A. (2005) Tyrosine kinases as targets for cancer therapy. N. Engl. J. Med., 353, 172-187.
2. Hartmann, J.T., Haap, M., Kopp, H.G. and Lipp, H.P. (2009) Tyrosine kinase inhibitors - a review on pharmacology, metabolism and side effects. Curr. Drug Metab., 10, 470-481.
3. Arora, A. and Scholar, E.M. (2005) Role of tyrosine kinase inhibitors in cancer therapy. J. Pharmacol. Exp. Ther., 315, 971-979.
4. O'Shea, J.J., Holland, S.M. and Staudt, L.M. (2013) JAKs and STATs in immunity, immunodeficiency, and cancer. N. Engl. J. Med., 368, 161-170.
5. Tu, C.C., Zhong, Y., Nguyen, L., Tsai, A., Sridevi, P., Tarn, W.Y. and Wang, J.Y. (2015) The kinase ABL phosphorylates the microprocessor subunit DGCR8 to stimulate primary microRNA processing in response to DNA damage. Sci. Signal., 8, ra64.
6. Reuven, N., Adler, J., Porat, Z., Polonio-Vallon, T., Hofmann, T.G. and Shaul, Y. (2015) The tyrosine kinase c-Abl promotes homeodomain-interacting protein kinase 2 (HIPK2) accumulation and activation in response to DNA damage. J. Biol. Chem., 290, 16478-16488.
7. Staquicini, F.I., Qian, M.D., Salameh, A., Dobroff, A.S., Edwards, J.K., Cimino, D.F., Moeller, B.J., Kelly, P., Nunez, M.I., Tang, X. et al. (2015) Receptor tyrosine kinase EphA5 is a functional molecular target in human lung cancer. J. Biol. Chem., 290, 7345-7359.
8. Chen, E., Ahn, J.S., Massie, C.E., Clynes, D., Godfrey, A.L., Li, J., Park, H.J., Nangalia, J., Silber, Y., Mullally, A. et al. (2014) JAK2V617F promotes replication fork stalling with disease-restricted impairment of the intra-S checkpoint response. Proc. Natl. Acad. Sci. U.S.A., 111, 15190-15195.
9. Reuven, N., Adler, J., Meltser, V. and Shaul, Y. (2013) The Hippo pathway kinase Lats2 prevents DNA damage-induced apoptosis through inhibition of the tyrosine kinase c-Abl. Cell Death Differ., 20, 1330-1340.
10. Kaidi, A. and Jackson, S.P. (2013) KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature, 498, 70-74.
11. Kondratova, A., Watanabe, T., Marotta, M., Cannon, M., Segall, A.M., Serre, D. and Tanaka, H. (2015) Replication fork integrity and intra-S phase checkpoint suppress gene amplification. Nucleic Acids Res, 43, 2678-2690.
12. Ghezraoui, H., Piganeau, M., Renouf, B., Renaud, J.B., Sallmyr, A., Ruis, B., Oh, S., Tomkinson, A.E., Hendrickson, E.A., Giovannangeli, C. et al. (2014) Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol. Cell, 55, 829-842.
13. Richardson, C. and Jasin, M. (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature, 405, 697-700.
14. Wray, J., Williamson, E.A., Singh, S.B., Wu, Y., Cogle, C.R., Weinstock, D.M., Zhang, Y., Lee, S.H., Zhou, D., Shao, L. et al. (2013) PARP1 is required for chromosomal translocations. Blood, 121, 4359-4365.
15. Li, X. and Heyer, W.D. (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Res., 18, 99-113.
16. Lieber, M.R., Gu, J., Lu, H., Shimazaki, N. and Tsai, A.G. (2010) Nonhomologous DNA end joining (NHEJ) and chromosomal translocations in humans. Sub-cell. Biochem., 50, 279-296.
17. Fattah, F., Lee, E.H., Weisensel, N., Wang, Y, Lichter, N. and Hendrickson, E.A. (2010) Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet., 6, e1000855.
18. Roberts, S.A., Strande, N, Burkhalter, M.D., Strom, C, Havener, J.M., Hasty, P. and Ramsden, D.A. (2010) Ku is a 5'-dRP/AP lyase that excises nucleotide damage near broken ends. Nature, 464, 1214-1217.
19. Bunting, S.F. and Nussenzweig, A. (2013) End-joining, translocations and cancer. Nat. Rev. Cancer, 13, 443-454.
20. O'Rourke, D.M., Kao, G.D., Singh, N., Park, B.W., Muschel, R.J., Wu, C.J. and Greene, M.I. (1998) Conversion of a radioresistant phenotype to a more sensitive one by disabling erbB receptor signaling in human cancer cells. Proc. Natl. Acad. Sci. U.S.A., 95, 10842-10847.
21. De Bacco, F., Luraghi, P, Medico, E., Reato, G., Girolami, F., Perera, T., Gabriele, P, Comoglio, PM. and Boccaccio, C. (2011) Induction of MET by ionizing radiation and its role in radioresistance and invasive growth of cancer. J. Natl. Cancer Inst., 103, 645-661.
22. Shields, B.J., Hauser, C, Bukczynska, PE., Court, N.W. and Tiganis, T. (2008) DNA replication stalling attenuates tyrosine kinase signaling to suppress S phase progression. Cancer Cell, 14, 166-179.
23. Valerie, K., Yacoub, A., Hagan, M.P, Curiel, DT, Fisher, PB., Grant, S. and Dent, P (2007) Radiation-induced cell signaling: inside-out and outside-in. Mol. Cancer Ther, 6, 789-801.
24. Motoyama, N and Naka, K. (2004) DNA damage tumor suppressor genes and genomic instability. Curr. Opin. Genet. Dev., 14, 11-16.
25. Gire, V, Roux, P, Wynford-Thomas, D, Brondello, J.M. and Dulic, V. (2004) DNA damage checkpoint kinase Chk2 triggers replicative senescence. EMBO J. 23, 2554-2563.
26. Hayashi, M.T., Cesare, A.J., Rivera, T. and Karlseder, J. (2015) Cell death during crisis is mediated by mitotic telomere deprotection. Nature, 522, 492-496.
27. Herbig, U., Jobling, W.A., Chen, B.P, Chen, DJ. and Sedivy, J.M. (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell, 14, 501-513.
28. Liberal, V, Martinsson-Ahlzen, H.S., Liberal, J., Spruck, CH., Widschwendter, M., McGowan, CH. and Reed, S.I. (2012) Cyclin-dependent kinase subunit (Cks) 1 or Cks2 overexpression overrides the DNA damage response barrier triggered by activated oncoproteins. Proc. Natl. Acad. Sci. U.S.A., 109, 2754-2759.
29. Toulany, M., Kasten-Pisula, U., Brammer, I., Wang, S., Chen, J., Dittmann, K., Baumann, M., Dikomey, E. and Rodemann, H.P (2006) Blockage of epidermal growth factor receptor-phosphatidylinositol 3-kinase-AKT signaling increases radiosensitivity of K-RAS mutated human tumor cells in vitro by affecting DNA repair. Clin. Cancer Res., 12, 4119-4126.
30. Trojanek, J., Ho, T, Del Valle, L., Nowicki, M., Wang, J.Y, Lassak, A., Peruzzi, F., Khalili, K., Skorski, T and Reiss, K. (2003) Role of the insulin-like growth factor I/insulin receptor substrate 1 axis in Rad51 trafficking and DNA repair by homologous recombination. Mol. Cell. Biol, 23, 7510-7524.
31. Fukumoto, Y, Morii, M., Miura, T, Kubota, S., Ishibashi, K., Honda, T, Okamoto, A., Yamaguchi, N, Iwama, A., Nakayama, Y et al. (2014) Src family kinases promote silencing of ATR-Chk1 signaling in termination of DNA damage checkpoint. J. Bol. Chem., 289, 12313-12329.
32. Fukumoto, Y, Kuki, K., Morii, M., Miura, T, Honda, T, Ishibashi, K., Hasegawa, H., Kubota, S., Ide, Y, Yamaguchi, N et al. (2014) Lyn tyrosine kinase promotes silencing of ATM-dependent checkpoint signaling during recovery from DNA double-strand breaks. Biochem. Biophys. Res. Commun., 452, 542-547.
33. Manning, G, Whyte, DB., Martinez, R., Hunter, T and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science (New York, N Y.), 298, 1912-1934.
34. Cosaceanu, D., Budiu, R.A., Carapancea, M., Castro, J., Lewensohn, R. and Dricu, A. (2007) Ionizing radiation activates IGF-1R triggering a cytoprotective signaling by interfering with Ku-DNA binding and by modulating Ku86 expression via a p38 kinase-dependent mechanism. Oncogene, 26, 2423-2434.
35. Schmidt-Ullrich, R.K, Mikkelsen, R.B., Dent, P, Todd, D.G, Valerie, K., Kavanagh, B.D, Contessa, J.N, Rorrer, W.K. and Chen, P.B. (1997) Radiation-induced proliferation of the human A431 squamous carcinoma cells is dependent on EGFR tyrosine phosphorylation. Oncogene, 15, 1191-1197.
36. Goldkorn, T., Balaban, N., Shannon, M. and Matsukuma, K. (1997) EGF receptor phosphorylation is affected by ionizing radiation. Biochim. Biophys. Acta, 1358, 289-299.
37. Bowers, G., Reardon, D., Hewitt, T., Dent, P., Mikkelsen, R.B., Valerie, K., Lammering, G., Amir, C. and Schmidt-Ullrich, R.K. (2001) The relative role of ErbB1-4 receptor tyrosine kinases in radiation signal transduction responses of human carcinoma cells. Oncogene, 20, 1388-1397.
38. Dittmann, K., Mayer, C., Kehlbach, R. and Rodemann, H.P. (2008) Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol. Cancer, 7, 69.
39. Teng, K., Zhang, Y., Hu, X., Ding, Y., Gong, R. and Liu, L. (2015) Nimotuzumab enhances radiation sensitivity of NSCLC H292 cells in vitro by blocking epidermal growth factor receptor nuclear translocation and inhibiting radiation-induced DNA damage repair. OncoTargets Ther., 8, 809-818.
40. Dittmann, K., Mayer, C. and Rodemann, H.P. (2005) Inhibition of radiation-induced EGFR nuclear import by C225 (Cetuximab) suppresses DNA-PK activity. Radiother. Oncol., 76, 157-161.
41. Dent, P., Reardon, D.B., Park, J.S., Bowers, G., Logsdon, C., Valerie, K. and Schmidt-Ullrich, R. (1999) Radiation-induced release of transforming growth factor alpha activates the epidermal growth factor receptor and mitogen-activated protein kinase pathway in carcinoma cells, leading to increased proliferation and protection from radiation-induced cell death. Mol. Biol. Cell, 10, 2493-2506.
42. Tanaka, T., Munshi, A., Brooks, C., Liu, J., Hobbs, M.L. and Meyn, R.E. (2008) Gefitinib radiosensitizes non-small cell lung cancer cells by suppressing cellular DNA repair capacity. Clin. Cancer Res., 14, 1266-1273.
43. Schulte, J.H., Kuhfittig-Kulle, S., Klein-Hitpass, L., Schramm, A., Biard, D.S., Pfeiffer, P. and Eggert, A. (2008) Expression of the TrkA or TrkB receptor tyrosine kinase alters the double-strand break (DSB) repair capacity of SY5Y neuroblastoma cells. DNA Repair, 7, 1757-1764.
44. Lammering, G., Hewit, T.H., Valerie, K., Contessa, J.N., Amorino, G.P., Dent, P. and Schmidt-Ullrich, R.K. (2003) EGFRvIII-mediated radioresistance through a strong cytoprotective response. Oncogene, 22, 5545-5553.
45. Learn, C.A., Hartzell, T.L., Wikstrand, C.J., Archer, G.E., Rich, J.N., Friedman, A.H., Friedman, H.S., Bigner, D.D. and Sampson, J.H. (2004) Resistance to tyrosine kinase inhibition by mutant epidermal growth factor receptor variant III contributes to the neoplastic phenotype of glioblastoma multiforme. Clin. Cancer Res., 10, 3216-3224.
46. Li, B., Yuan, M., Kim, I.A., Chang, C.M., Bernhard, E.J. and Shu, H.K. (2004) Mutant epidermal growth factor receptor displays increased signaling through the phosphatidylinositol-3 kinase/AKT pathway and promotes radioresistance in cells of astrocytic origin. Oncogene, 23, 4594-4602.
47. Golding, S.E., Morgan, R.N., Adams, B.R., Hawkins, A.J., Povirk, L.F. and Valerie, K. (2009) Pro-survival AKT and ERK signaling from EGFR and mutant EGFRvIII enhances DNA double-strand break repair in human glioma cells. Cancer Biol. Ther., 8, 730-738.
48. Kao, G.D., Jiang, Z., Fernandes, A.M., Gupta, A.K. and Maity, A. (2007) Inhibition of phosphatidylinositol-3-OH kinase/Akt signaling impairs DNA repair in glioblastoma cells following ionizing radiation. J. Biol. Chem., 282, 21206-21212.
49. Mukherjee, B., McEllin, B., Camacho, C.V., Tomimatsu, N., Sirasanagandala, S., Nannepaga, S., Hatanpaa, K.J., Mickey, B., Madden, C., Maher, E. et al. (2009) EGFRvIII and DNA double-strand break repair: a molecular mechanism for radioresistance in glioblastoma. Cancer Res., 69, 4252-4259.
50. Toulany, M., Kehlbach, R., Florczak, U., Sak, A., Wang, S., Chen, J., Lobrich, M. and Rodemann, H.P. (2008) Targeting of AKT1 enhances radiation toxicity of human tumor cells by inhibiting DNA-PKcs-dependent DNA double-strand break repair. Mol. Cancer Ther., 7, 1772-1781.
51. Friedmann, B., Caplin, M., Hartley, J.A. and Hochhauser, D. (2004) Modulation of DNA repair in vitro after treatment with chemotherapeutic agents by the epidermal growth factor receptor inhibitor gefitinib (ZD1839). Clin. Cancer Res., 10, 6476-6486.
52. Bozulic, L., Surucu, B., Hynx, D. and Hemmings, B.A. (2008) PKBalpha/Akt1 acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Mol. Cell, 30, 203-213.
53. Boehme, K.A., Kulikov, R. and Blattner, C. (2008) p53 stabilization in response to DNA damage requires Akt/PKB and DNA-PK. Proce. Natl. Acad. Sci. U.S.A., 105, 7785-7790.
54. Lees-Miller, S.P. (2008) PIKK-ing a new partner: a new role for PKB in the DNA damage response. Cancer Cell, 13, 379-380.
55. Mahajan, K., Coppola, D., Challa, S., Fang, B., Chen, Y.A., Zhu, W., Lopez, A.S., Koomen, J., Engelman, R.W., Rivera, C. et al. (2010) Ack1 mediated AKT/PKB tyrosine 176 phosphorylation regulates its activation. PLoS One, 5, e9646.
56. Mahajan, K., Coppola, D., Rawal, B., Chen, Y.A., Lawrence, H.R., Engelman, R.W., Lawrence, N.J. and Mahajan, N.P. (2012) Ack1-mediated androgen receptor phosphorylation modulates radiation resistance in castration-resistant prostate cancer. J. Biol. Chem., 287, 22112-22122.
57. Chou, R.H., Wang, Y.N., Hsieh, Y.H., Li, L.Y., Xia, W., Chang, W.C., Chang, L.C., Cheng, C.C., Lai, C.C., Hsu, J.L. et al. (2014) EGFR modulates DNA synthesis and repair through Tyr phosphorylation of histone H4. Dev. Cell, 30, 224-237.
58. Sanders, S.L., Portoso, M., Mata, J., Bahler, J., Allshire, R.C. and Kouzarides, T. (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell, 119, 603-614.
59. Pei, H., Zhang, L., Luo, K., Qin, Y., Chesi, M., Fei, F., Bergsagel, P.L., Wang, L., You, Z. and Lou, Z. (2011) MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature, 470, 124-128.
60. Wang, S.C., Nakajima, Y., Yu, Y.L., Xia, W., Chen, C.T., Yang, C.C., McIntush, E.W., Li, L.Y., Hawke, D.H., Kobayashi, R. et al. (2006) Tyrosine phosphorylation controls PCNA function through protein stability. Nat. Cell Biol., 8, 1359-1368.
61. Ortega, J., Li, J.Y., Lee, S., Tong, D., Gu, L. and Li, G.M. (2015) Phosphorylation of PCNA by EGFR inhibits mismatch repair and promotes misincorporation during DNA synthesis. Proc. Natl. Acad. Sci. U.S.A., 112, 5667-5672.
62. Zhao, H., Lo, Y.H., Ma, L., Waltz, S.E., Gray, J.K., Hung, M.C. and Wang, S.C. (2011) Targeting tyrosine phosphorylation of PCNA inhibits prostate cancer growth. Mol. Cancer Ther., 10, 29-36.
63. Kharbanda, S., Saleem, A., Yuan, Z.M., Kraeft, S., Weichselbaum, R., Chen, L.B. and Kufe, D. (1996) Nuclear signaling induced by ionizing radiation involves colocalization of the activated p56/p53lyn tyrosine kinase with p34cdc2. Cancer Res., 56, 3617-3621.
64. Srinivasan, D. and Plattner, R. (2006) Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res., 66, 5648-5655.
65. Tang, J., Wang, J.Y. and Parker, L.L. (2012) Detection of early Abl kinase activation after ionizing radiation by using a peptide biosensor. Chembiochem, 13, 665-673.
66. Meltser, V., Ben-Yehoyada, M. and Shaul, Y. (2011) c-Abl tyrosine kinase in the DNA damage response: cell death and more. Cell Death Differ., 18, 2-4.
67. Shaul, Y. (2000) c-Abl: activation and nuclear targets. Cell Death Differ., 7, 10-16.
68. Zuckerman, V., Lenos, K., Popowicz, G.M., Silberman, I., Grossman, T., Marine, J.C., Holak, T.A., Jochemsen, A.G. and Haupt, Y. (2009) c-Abl phosphorylates Hdmx and regulates its interaction with p53. J. Biol. Chem., 284, 4031-4039.
69. Yuan, Z.M., Shioya, H., Ishiko, T., Sun, X., Gu, J., Huang, Y.Y., Lu, H., Kharbanda, S., Weichselbaum, R. and Kufe, D. (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature, 399, 814-817.
70. Tsai, K.K. and Yuan, Z.M. (2003) c-Abl stabilizes p73 by a phosphorylation-augmented interaction. Cancer Res., 63, 3418-3424.
71. Mahajan, K., Challa, S., Coppola, D., Lawrence, H., Luo, Y., Gevariya, H., Zhu, W., Chen, Y.A., Lawrence, N.J. and Mahajan, N.P. (2010) Effect of Ack1 tyrosine kinase inhibitor on ligand-independent androgen receptor activity. Prostate, 70, 1274-1285.
72. Mahajan, N.P., Liu, Y., Majumder, S., Warren, M.R., Parker, C.E., Mohler, J.L., Earp, H.S. and Whang, Y.E. (2007) Activated Cdc42-associated kinase Ack1 promotes prostate cancer progression via androgen receptor tyrosine phosphorylation. Proc. Natl. Acadeedings. Sci. U.S.A., 104, 8438-8443.
73. Bakkenist, C.J. and Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421, 499-506.
74. Li, Z., Hosoi, Y., Cai, K., Tanno, Y., Matsumoto, Y., Enomoto, A., Morita, A., Nakagawa, K. and Miyagawa, K. (2006) Src tyrosine kinase inhibitor PP2 suppresses ERK1/2 activation and epidermal growth factor receptor transactivation by X-irradiation. Biochem. Biophys. Res. Commun., 341, 363-368.
75. Kharbanda, S., Yuan, Z.M., Rubin, E., Weichselbaum, R. and Kufe, D. (1994) Activation of Src-like p56/p53lyn tyrosine kinase by ionizing radiation. J. Biol. Chem., 269, 20739-20743.
76. Kharbanda, S., Yuan, Z.M., Taneja, N., Weichselbaum, R. and Kufe, D. (1994) p56/p53lyn tyrosine kinase activation in mammalian cells treated with mitomycin C. Oncogene, 9, 3005-3011.
77. Yoshida, K., Miki, Y. and Kufe, D. (2002) Activation of SAPK/JNK signaling by protein kinase Cdelta in response to DNA damage. J. Biol. Chem., 277, 48372-48378.
78. Kumar, S., Pandey, P., Bharti, A., Jin, S., Weichselbaum, R., Weaver, D., Kufe, D. and Kharbanda, S. (1998) Regulation of DNA-dependent protein kinase by the Lyn tyrosine kinase. J. Biol. Chem., 273, 25654-25658.
79. Aoyama, K., Fukumoto, Y., Ishibashi, K., Kubota, S., Morinaga, T., Horiike, Y., Yuki, R., Takahashi, A., Nakayama, Y. and Yamaguchi, N. (2011) Nuclear c-Abl-mediated tyrosine phosphorylation induces chromatin structural changes through histone modifications that include H4K16 hypoacetylation. Exp. Cell Res., 317, 2874-2903.
80. Keshet, R., Adler, J., Ricardo Lax, I., Shanzer, M., Porat, Z., Reuven, N. and Shaul, Y. (2015) c-Abl antagonizes the YAP oncogenic function. Cell Death Differ., 22, 935-945.
81. Hartwell, L.H., Culotti, J., Pringle, J.R. and Reid, B.J. (1974) Genetic control of the cell division cycle in yeast. Science (New York, N.Y.), 183, 46-51.
82. Mahajan, K. and Mahajan, N.P. (2013) WEE1 tyrosine kinase, a novel epigenetic modifier. Trends Genet., 29, 394-402.
83. Meeks-Wagner, D., Wood, J.S., Garvik, B. and Hartwell, L.H. (1986) Isolation of two genes that affect mitotic chromosome transmission in S. cerevisiae. Cell, 44, 53-63.
84. Wu, G., Broniscer, A., McEachron, T.A., Lu, C., Paugh, B.S., Becksfort, J., Qu, C., Ding, L., Huether, R., Parker, M. et al. (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat. Genet., 44, 251-253.
85. Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A., Tonjes, M. et al. (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature, 482, 226-231.
86. Wolffe, A.P. (1996) Chromatin and gene regulation at the onset of embryonic development. Reprod. Nutr. Dev., 36, 581-606.
87. Gunjan, A. and Verreault, A. (2003) A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell, 115, 537-549.
88. Singh, R.K., Kabbaj, M.H., Paik, J. and Gunjan, A. (2009) Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol., 11, 925-933.
89. Singh, R.K., Liang, D., Gajjalaiahvari, U.R., Kabbaj, M.H., Paik, J. and Gunjan, A. (2010) Excess histone levels mediate cytotoxicity via multiple mechanisms. Cell Cycle (Georgetown, Tex), 9, 4236-4244.
90. Holzen, T.M. and Sclafani, R. (2010) Genetic interaction of RAD53 protein kinase with histones is important for DNA replication. Cell Cycle (Georgetown, Tex), 9, 4735-4747.
91. Chen, S.H., Albuquerque, C.P., Liang, J., Suhandynata, R.T. and Zhou, H. (2010) A proteome-wide analysis of kinase-substrate network in the DNA damage response. J. Biol. Chem., 285, 12803-12812.
92. Mahajan, K., Fang, B., Koomen, J.M. and Mahajan, N.P. (2012) H2B Tyr37 phosphorylation suppresses expression of replication-dependent core histone genes. Nat. Struct. Mol. Biol., 19, 930-937.
93. Dawson, M.A., Bannister, A.J., Gottgens, B., Foster, S.D., Bartke, T., Green, A.R. and Kouzarides, T. (2009) JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature, 461, 819-822.
94. Pacaud, R., Cheray, M., Nadaradjane, A., Vallette, F.M. and Cartron, P.F. (2015) Histone H3 phosphorylation in GBM: a new rational to guide the use of kinase inhibitors in anti-GBM therapy. Theranostics, 5, 12-22.
95. Chitnis, M.M., Lodhia, K.A., Aleksic, T., Gao, S., Protheroe, A.S. and Macaulay, V.M. (2014) IGF-1R inhibition enhances radiosensitivity and delays double-strand break repair by both non-homologous end-joining and homologous recombination. Oncogene, 33, 5262-5273.
96. Turney, B.W., Kerr, M., Chitnis, M.M., Lodhia, K., Wang, Y., Riedemann, J., Rochester, M., Protheroe, A.S., Brewster, S.F. and Macaulay, V.M. (2012) Depletion of the type 1 IGF receptor delays repair of radiation-induced DNA double strand breaks. Radiother. Oncol., 103, 402-409.
97. Yang, S., Chintapalli, J., Sodagum, L., Baskin, S., Malhotra, A., Reiss, K. and Meggs, L.G. (2005) Activated IGF-1R inhibits hyperglycemia-induced DNA damage and promotes DNA repair by homologous recombination. Am. J. Physiol. Renal Physiol., 289, F1144-F1152.
98. Slupianek, A., Hoser, G., Majsterek, I., Bronisz, A., Malecki, M., Blasiak, J., Fishel, R. and Skorski, T. (2002) Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis. Mol. Cell. Biol., 22, 4189-4201.
99. Baskaran, R., Wood, L.D., Whitaker, L.L., Canman, C.E., Morgan, S.E., Xu, Y., Barlow, C., Baltimore, D., Wynshaw-Boris, A., Kastan, M.B. et al. (1997) Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature, 387, 516-519.
100. 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.
101. Sun, Y., Jiang, X., Chen, S., Fernandes, N. and Price, B.D. (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. U.S.A., 102, 13182-13187.
102. Sun, Y., Jiang, X., Xu, Y., Ayrapetov, M.K., Moreau, L.A., Whetstine, J.R. and Price, B.D. (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol., 11, 1376-1382.
103. Jiang, Z., Kamath, R., Jin, S., Balasubramani, M., Pandita, T.K. and Rajasekaran, B. (2011) Tip60-mediated acetylation activates transcription independent apoptotic activity of Abl. Mol. Cancer, 10, 88.
104. Kharbanda, S., Yuan, Z.M., Weichselbaum, R. and Kufe, D. (1997) Functional role for the c-Abl protein tyrosine kinase in the cellular response to genotoxic stress. Biochim. Biophys. Acta, 1333, O1-O7.
105. Wang, J.Y. (2004) Controlling Abl: auto-inhibition and co-inhibition? Nat. Cell Biol., 6, 3-7.
106. Kumar, V., Sabatini, D., Pandey, P., Gingras, A.C., Majumder, P.K., Kumar, M., Yuan, Z.M., Carmichael, G., Weichselbaum, R., Sonenberg, N. et al. (2000) Regulation of the rapamycin and FKBP-target 1/mammalian target of rapamycin and cap-dependent initiation of translation by the c-Abl protein-tyrosine kinase. J. Biol. Chem., 275, 10779-10787.
107. Yuan, Z.M., Utsugisawa, T., Huang, Y., Ishiko, T., Nakada, S., Kharbanda, S., Weichselbaum, R. and Kufe, D. (1997) Inhibition of phosphatidylinositol 3-kinase by c-Abl in the genotoxic stress response. J. Biol. Chem., 272, 23485-23488.
108. Chen, G., Yuan, S.S., Liu, W., Xu, Y., Trujillo, K., Song, B., Cong, F., Goff, S.P., Wu, Y., Arlinghaus, R. et al. (1999) Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J. Biol. Chem., 274, 12748-12752.
109. Shimizu, H., Popova, M., Fleury, F., Kobayashi, M., Hayashi, N., Sakane, I., Kurumizaka, H., Venkitaraman, A.R., Takahashi, M. and Yamamoto, K. (2009) c-ABL tyrosine kinase stabilizes RAD51 chromatin association. Biochem. Biophys. Res. Commun., 382, 286-291.
110. Kitao, H. and Yuan, Z.M. (2002) Regulation of ionizing radiation-induced Rad52 nuclear foci formation by c-Abl-mediated phosphorylation. J. Biol. Chem., 277, 48944-48948.
111. Honda, M., Okuno, Y., Yoo, J., Ha, T. and Spies, M. (2011) Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. EMBO J., 30, 3368-3382.
112. Xiao, A., Li, H., Shechter, D., Ahn, S.H., Fabrizio, L.A., Erdjument-Bromage, H., Ishibe-Murakami, S., Wang, B., Tempst, P., Hofmann, K. et al. (2009) WSTF regulates the H2A. X DNA damage response via a novel tyrosine kinase activity. Nature, 457, 57-62.
113. Cook, P.J., Ju, B.G., Telese, F., Wang, X., Glass, C.K. and Rosenfeld, M.G. (2009) Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature, 458, 591-596.
114. Singh, N., Basnet, H., Wiltshire, T.D., Mohammad, D.H., Thompson, J.R., Heroux, A., Botuyan, M.V., Yaffe, M.B., Couch, F.J., Rosenfeld, M.G. et al. (2012) Dual recognition of phosphoserine and phosphotyrosine in histone variant H2A.X by DNA damage response protein MCPH1. Proc. Nat. Acad. Sci. U.S.A., 109, 14381-14386.
115. Brown, J.A., Eykelenboom, J.K. and Lowndes, N.F. (2012) Co-mutation of histone H2AX S139A with Y142A rescues Y142A-induced ionising radiation sensitivity. FEBS Open Bio, 2, 313-317.
116. Sone, K., Piao, L., Nakakido, M., Ueda, K., Jenuwein, T., Nakamura, Y. and Hamamoto, R. (2014) Critical role of lysine 134 methylation on histone H2AX for gamma-H2AX production and DNA repair. Nat. Commun., 5, 5691.
117. Mahajan, K.N. and Mitchell, B.S. (2003) Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc. Natl. Acad. Sci. U.S.A., 100, 10746-10751.
118. Dellago, H., Khan, A., Nussbacher, M., Gstraunthaler, A., Lammermann, I., Schosserer, M., Muck, C., Anrather, D., Scheffold, A., Ammerer, G. et al. (2012) ATM-dependent phosphorylation of SNEVhPrp19/hPso4 is involved in extending cellular life span and suppression of apoptosis. Aging, 4, 290-304.
119. Beck, B.D., Park, S.J., Lee, Y.J., Roman, Y., Hromas, R.A. and Lee, S.H. (2008) Human Pso4 is a metnase (SETMAR)-binding partner that regulates metnase function in DNA repair. J. Biol. Chem., 283, 9023-9030.
120. Beck, B.D., Lee, S.S., Hromas, R. and Lee, S.H. (2010) Regulation of Metnase's TIR binding activity by its binding partner, Pso4. Arch. Biochem. Biophys., 498, 89-94.
121. Kubota, S., Morii, M., Yuki, R., Yamaguchi, N., Yamaguchi, H., Aoyama, K., Kuga, T., Tomonaga, T. and Yamaguchi, N. (2015) Role for Tyrosine Phosphorylation of A-kinase Anchoring Protein 8 (AKAP8) in Its Dissociation from Chromatin and the Nuclear Matrix. J. Biol. Chem., 290, 10891-10904.
122. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B.M., Strein, C., Davey, N.E., Humphreys, D.T., Preiss, T., Steinmetz, L.M. et al. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell, 149, 1393-1406.
123. Eide, T., Coghlan, V., Orstavik, S., Holsve, C., Solberg, R., Skalhegg, B.S., Lamb, N.J., Langeberg, L., Fernandez, A., Scott, J.D. et al. (1998) Molecular cloning, chromosomal localization, and cell cycle-dependent subcellular distribution of the A-kinase anchoring protein, AKAP95. Exp. Cell Res., 238, 305-316.
124. Guo, Z., Dai, B., Jiang, T., Xu, K., Xie, Y., Kim, O., Nesheiwat, I., Kong, X., Melamed, J., Handratta, V.D. et al. (2006) Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell, 10, 309-319.
125. Lim, D.S. and Hasty, P. (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol., 16, 7133-7143.
126. Tsuzuki, T., Fujii, Y., Sakumi, K., Tominaga, Y., Nakao, K., Sekiguchi, M., Matsushiro, A., Yoshimura, Y. and Morita, T. (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. U.S.A., 93, 6236-6240.
127. Fortschegger, K., Wagner, B., Voglauer, R., Katinger, H., Sibilia, M. and Grillari, J. (2007) Early embryonic lethality of mice lacking the essential protein SNEV. Mol. Cell. Biol., 27, 3123-3130.
128. Tominaga, Y., Li, C., Wang, R.H. and Deng, C.X. (2006) Murine Wee1 plays a critical role in cell cycle regulation and pre-implantation stages of embryonic development. Int. J. Biol. Sci., 2, 161-170.
129. Bhosle, J., Kiakos, K., Porter, A.C., Wu, J., Makris, A., Hartley, J.A. and Hochhauser, D. (2013) Treatment with gefitinib or lapatinib induces drug resistance through downregulation of topoisomerase IIalpha expression. Mol. Cancer Ther., 12, 2897-2908.
130. Kim, J.C., Ali, M.A., Nandi, A., Mukhopadhyay, P., Choy, H., Cao, C. and Saha, D. (2005) Correlation of HER1/EGFR expression and degree of radiosensitizing effect of the HER1/EGFR-tyrosine kinase inhibitor erlotinib. Indian J. Biochem. Biophys., 42, 358-365.
131. Raju, U., Riesterer, O., Wang, Z.Q., Molkentine, D.P., Molkentine, J.M., Johnson, F.M., Glisson, B., Milas, L. and Ang, K.K. (2012) Dasatinib, a multi-kinase inhibitor increased radiation sensitivity by interfering with nuclear localization of epidermal growth factor receptor and by blocking DNA repair pathways. Radiother. Oncol., 105, 241-249.
132. Sambade, M.J., Camp, J.T., Kimple, R.J., Sartor, C.I. and Shields, J.M. (2009) Mechanism of lapatinib-mediated radiosensitization of breast cancer cells is primarily by inhibition of the Raf>MEK>ERK mitogen-activated protein kinase cascade and radiosensitization of lapatinib-resistant cells restored by direct inhibition of MEK. Radiother. Oncol., 93, 639-644.
133. Dittmann, K., Mayer, C., Fehrenbacher, B., Schaller, M., Raju, U., Milas, L., Chen, D.J., Kehlbach, R. and Rodemann, H.P. (2005) Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J. Biol. Chem., 280, 31182-31189.
134. Liccardi, G., Hartley, J.A. and Hochhauser, D. (2011) EGFR nuclear translocation modulates DNA repair following cisplatin and ionizing radiation treatment. Cancer Res., 71, 1103-1114.
135. Baro, M., de Llobet, L.I., Figueras, A., Skvortsova, I., Mesia, R. and Balart, J. (2014) Dasatinib worsens the effect of cetuximab in combination with fractionated radiotherapy in FaDu- and A431-derived xenografted tumours. Br. J. Cancer, 111, 1310-1318.
136. Majsterek, I., Blasiak, J., Mlynarski, W., Hoser, G. and Skorski, T. (2002) Does the bcr/abl-mediated increase in the efficacy of DNA repair play a role in the drug resistance of cancer cells? Cell Biol. Int., 26, 363-370.
137. Tobin, L.A., Robert, C., Rapoport, A.P., Gojo, I., Baer, M.R., Tomkinson, A.E. and Rassool, F.V. (2013) Targeting abnormal DNA double-strand break repair in tyrosine kinase inhibitor-resistant chronic myeloid leukemias. Oncogene, 32, 1784-1793.
138. Canitrot, Y., Falinski, R., Louat, T., Laurent, G., Cazaux, C., Hoffmann, J.S., Lautier, D. and Skorski, T. (2003) p210 BCR/ABL kinase regulates nucleotide excision repair (NER) and resistance to UV radiation. Blood, 102, 2632-2637.
139. Qiao, B., Kerr, M., Groselj, B., Teo, M.T., Knowles, M.A., Bristow, R.G., Phillips, R.M. and Kiltie, A.E. (2013) Imatinib radiosensitizes bladder cancer by targeting homologous recombination. Cancer Res., 73, 1611-1620.
140. Yadav, A., Kumar, B., Teknos, T.N. and Kumar, P. (2011) Sorafenib enhances the antitumor effects of chemoradiation treatment by downregulating ERCC-1 and XRCC-1 DNA repair proteins. Mol. Cancer Ther., 10, 1241-1251.
141. Mahajan, K. and Mahajan, N.P. (2015) ACK1/TNK2 tyrosine kinase: molecular signaling and evolving role in cancers. Oncogene, 34, 4162-4167.
142. Mahajan, K., Lawrence, H.R., Lawrence, N.J. and Mahajan, N.P. (2014) ACK1 tyrosine kinase interacts with histone demethylase KDM3A to regulate the mammary tumor oncogene HOXA1. J. Biol. Chem., 289, 28179-28191.
143. Okada, Y., Scott, G., Ray, M.K., Mishina, Y. and Zhang, Y. (2007) Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature, 450, 119-123.
144. Yamane, K., Toumazou, C., Tsukada, Y., Erdjument-Bromage, H., Tempst, P., Wong, J. and Zhang, Y. (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell, 125, 483-495.
145. Mir, S.E., De Witt Hamer, P.C., Krawczyk, P.M., Balaj, L., Claes, A., Niers, J.M., Van Tilborg, A.A., Zwinderman, A.H., Geerts, D., Kaspers, G.J. et al. (2010) In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell, 18, 244-257.
146. De Witt Hamer, P.C., Mir, S.E., Noske, D., Van Noorden, C.J. and Wurdinger, T. (2011) WEE1 kinase targeting combined with DNA-damaging cancer therapy catalyzes mitotic catastrophe. Clini. Cancer Res., 17, 4200-4207.
147. Hirai, H., Arai, T., Okada, M., Nishibata, T., Kobayashi, M., Sakai, N., Imagaki, K., Ohtani, J., Sakai, T., Yoshizumi, T. et al. (2010) MK-1775, a small molecule Wee1 inhibitor, enhances anti-tumor efficacy of various DNA-damaging agents, including 5-fluorouracil. Cancer Biol. Ther., 9, 514-522.
148. Hong, M.K., Macintyre, G., Wedge, D.C., Van Loo, P., Patel, K., Lunke, S., Alexandrov, L.B., Sloggett, C., Cmero, M., Marass, F. et al. (2015) Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer. Nat. Commun., 6, 6605.
149. Goodwin, J.F., Schiewer, M.J., Dean, J.L., Schrecengost, R.S., de Leeuw, R., Han, S., Ma, T., Den, R.B., Dicker, A.P., Feng, F.Y. et al. (2013) A hormone-DNA repair circuit governs the response to genotoxic insult. Cancer Discovery, 3, 1254-1271.
150. Goldberg, Z., Vogt Sionov, R., Berger, M., Zwang, Y., Perets, R., Van Etten, R.A., Oren, M., Taya, Y. and Haupt, Y. (2002) Tyrosine phosphorylation of Mdm2 by c-Abl: implications for p53 regulation. EMBO J., 21, 3715-3727.
151. Dias, S.S., Milne, D.M. and Meek, D.W. (2006) c-Abl phosphorylates Hdm2 at tyrosine 276 in response to DNA damage and regulates interaction with ARF. Oncogene, 25, 6666-6671.
152. Chen, X., Gohain, N., Zhan, C., Lu, W.Y., Pazgier, M. and Lu, W. (2015) Structural basis of how stress-induced MDMX phosphorylation activates p53. Oncogene.
153. 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.
154. Gonfloni, S., Di Tella, L., Caldarola, S., Cannata, S.M., Klinger, F.G., Di Bartolomeo, C., Mattei, M., Candi, E., De Felici, M., Melino, G. et al. (2009) Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nat. Med., 15, 1179-1185.
155. Yi, W., Lee, T.H., Tompkins, J.D., Zhu, F., Wu, X. and Her, C. (2006) Physical and functional interaction between hMSH5 and c-Abl. Cancer Res., 66, 151-158.
156. 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.
157. Foray, N., Marot, D., Randrianarison, V., Venezia, N.D., Picard, D., Perricaudet, M., Favaudon, V. and Jeggo, P. (2002) Constitutive association of BRCA1 and c-Abl and its ATM-dependent disruption after irradiation. Mol. Cell. Biol., 22, 4020-4032.
158. Lee, H.J., Lan, L., Peng, G., Chang, W.C., Hsu, M.C., Wang, Y.N., Cheng, C.C., Wei, L., Nakajima, S., Chang, S.S. et al. (2015) Tyrosine 370 phosphorylation of ATM positively regulates DNA damage response. Cell Res., 25, 225-236.
159. Russell, P. and Nurse, P. (1987) Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell, 49, 559-567.
160. Rhind, N., Furnari, B. and Russell, P. (1997) Cdc2 tyrosine phosphorylation is required for the DNA damage checkpoint in fission yeast. Genes Dev., 11, 504-511.