DNA damage stress response in germ cells: Role of c-Abl and clinical implications

Oncogene

Volumn 29, Issue 47, 2010, Pages 6193-6202

  Gonfloni, S ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

c Abl tyrosine kinase; chemotherapy; DNA damage response; germ cells; TAp63

Indexed keywords

ABELSON KINASE; BINDING PROTEIN; CISPLATIN; HISTONE H2AX; PROTEIN P53; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; DNA DAMAGE; GERM CELL; LETHALITY; LYMPHOCYTOPENIA; MYRISTYLATION; OSTEOPOROSIS; OVARIAN RESERVE; PERINATAL MORTALITY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STRESS; SUBFERTILITY; SURVIVAL RATE;

ANIMALS; CELL NUCLEUS; DNA DAMAGE; GERM CELLS; HUMANS; PROTO-ONCOGENE PROTEINS C-ABL; TUMOR SUPPRESSOR PROTEIN P53;

MUS;

EID: 78649498783     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.410     Document Type: Review

References (141)

1. Adrian FJ, Ding Q, Sim T, Velentza A, Sloan C, Liu Y et al. (2006). Allosteric inhibitors of Bcr-abl-dependent cell proliferation. Nat Chem Biol 2: 95-102.
2. Agami R, Blandino G, Oren M, Shaul Y. (1999). Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature 399: 809-813.
3. Backhus LE, Kondapalli LA, Chang RJ, Coutifaris C, Kazer R, Woodruff TK. (2007). Oncofertility Consortium consensus statement: guidelines for ovarian tissue cryopreservation. Cancer Treat Res 138: 235-239.
4. Bartek J, Lukas J. (2007). DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19: 238-245.
5. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K et al. (2005). DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434: 864-870.
6. Baskaran R, Wood LD, Whitaker LL, Canman CE, Morgan SE, Xu Y et al. (1997). Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 387: 516-519.
7. Belyi VA, Ak P, Markert E, Wang H, Hu W, Puzio-Kuter A et al. (2010). The origins and evolution of the p53 family of genes. Cold Spring Harb Perspect Biol 2: a001198.
8. Bourdon JC, Fernandes K, Murray-Zmijewski F, Liu G, Diot A, Xirodimas DP et al. (2005). p53 isoforms can regulate p53 transcriptional activity. Genes Dev 19: 2122-2137.
9. Brodsky MH, Nordstrom W, Tsang G, Kwan E, Rubin GM, Abrams JM. (2000). Drosophila p53 binds a damage response element at the reaper locus. Cell 101: 103-113.
10. Brodsky MH, Weinert BT, Tsang G, Rong YS, McGinnis NM, Golic KG et al. (2004). Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol Cell Biol 24: 1219-1231.
11. Burma S, Chen DJ. (2004). Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst) 3: 909-918.
12. Carson CT, Schwartz RA, Stracker TH, Lilley CE, Lee DV, Weitzman MD. (2003). The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J 22: 6610-6620.
13. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A et al. (2003). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5: 675-679.
14. Chen G, Yuan SS, Liu W, Xu Y, Trujillo K, Song B et al. (1999a). Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J Biol Chem 274: 12748-12752.
15. Chen X, Zhang J, Lee J, Lin PS, Ford JM, Zheng N et al. (2006). A kinase-independent function of c-Abl in promoting proteolytic destruction of damaged DNA binding proteins. Mol Cell 22: 489-499.
16. Chen Z, Seimiya H, Naito M, Mashima T, Kizaki A, Dan S et al. (1999b). ASK1 mediates apoptotic cell death induced by genotoxic stress. Oncogene 18: 173-180.
17. Chow CS, Barnes CM, Lippard SJ. (1995). A single HMG domain in high-mobility group 1 protein binds to DNAs as small as 20 base pairs containing the major cisplatin adduct. Biochemistry 34: 2956-2964.
18. Collis SJ, DeWeese TL, Jeggo PA, Parker AR. (2005). The life and death of DNA-PK. Oncogene 24: 949-961.
19. Cong F, Tang J, Hwang BJ, Vuong BQ, Chu G, Goff SP. (2002). Interaction between UV-damaged DNA binding activity proteins and the c-Abl tyrosine kinase. J Biol Chem 277: 34870-34878.
20. David-Cordonnier MH, Hamdane M, Bailly C, D'Halluin JC. (1998). The DNA binding domain of the human c-Abl tyrosine kinase preferentially binds to DNA sequences containing an AAC motif and to distorted DNA structures. Biochemistry 37: 6065-6076.
21. Deng X, Hofmann ER, Villanueva A, Hobert O, Capodieci P, Veach DR et al. (2004). Caenorhabditis elegans ABL-1 antagonizes p53-mediated germline apoptosis after ionizing irradiation. Nat Genet 36: 906-912.
22. Derry WB, Putzke AP, Rothman JH. (2001). Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294: 591-595.
23. Dery U, Masson JY. (2007). Twists and turns in the function of DNA damage signaling and repair proteins by post-translational modifications. DNA Repair (Amst) 6: 561-577.
24. Dunn L, Fox KR. (2009). Techniques for fertility preservation in patients with breast cancer. Curr Opin Obstet Gynecol 21: 68-73.
25. Durocher D, Jackson SP. (2001). DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr Opin Cell Biol 13: 225-231.
26. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, Heyer J et al. (1999). Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21: 123-127.
27. Falck J, Coates J, Jackson SP. (2005). Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434: 605-611.
28. Foray N, Marot D, Randrianarison V, Venezia ND, Picard D, Perricaudet M et al. (2002). Constitutive association of BRCA1 and c-Abl and its ATM-dependent disruption after irradiation. Mol Cell Biol 22: 4020-4032.
29. Gardino SL, Jeruss JS, Woodruff TK. (2010). Using decision trees to enhance interdisciplinary team work: the case of oncofertility. J Assist Reprod Genet 27: 227-231.
30. Gellert M. (2002). V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71: 101-132.
31. Goddard JM, Weiland JJ, Capecchi MR. (1986). Isolation and characterization of Caenorhabditis elegans DNA sequences homologous to the v-abl oncogene. Proc Natl Acad Sci USA 83: 2172-2176.
32. Goff SP, Gilboa E, Witte ON, Baltimore D. (1980). Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell 22: 777-785.
33. Goldberg Z, Vogt Sionov R, Berger M, Zwang Y, Perets R, Van Etten RA et al. (2002). Tyrosine phosphorylation of Mdm2 by c-Abl: implications for p53 regulation. EMBO J 21: 3715-3727.
34. Gonfloni S. (2010). Modulating c-Abl nuclear activity as a strategy to preserve female fertility. Cell Cycle 9: 217-218.
35. Gonfloni S, Di Tella L, Caldarola S, Cannata SM, Klinger FG, Di Bartolomeo C et al. (2009). Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nat Med 15: 1179-1185.
36. Gonfloni S, Williams JC, Hattula K, Weijland A, Wierenga RK, Superti-Furga G. (1997). The role of the linker between the SH2 domain and catalytic domain in the regulation and function of Src. EMBO J 16: 7261-7271.
37. Gong JG, Costanzo A, Yang HQ, Melino G, Kaelin Jr WG, Levrero M et al. (1999). The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature 399: 806-809.
38. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T et al. (2005). Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434: 907-913.
39. Gu JJ, Ryu JR, Pendergast AM. (2009). Abl tyrosine kinases in T-cell signaling. Immunol Rev 228: 170-183.
40. Hantschel O, Nagar B, Guettler S, Kretzschmar J, Dorey K, Kuriyan J., et al. (2003). A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 112: 845-857.
41. Hantschel O, Superti-Furga G. (2004). Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5: 33-44.
42. Hardin JD, Boast S, Schwartzberg PL, Lee G, Alt FW, Stall AM et al.(1996). Abnormal peripheral lymphocyte function in c-abl mutant mice. Cell Immunol 172: 100-107.
43. Her C, Doggett NA. (1998). Cloning, structural characterization, and chromosomal localization of the human orthologue of Sacchar-omyces cerevisiae MSH5 gene. Genomics 52: 50-61.
44. Her C, Zhao N, Wu X, Tompkins JD. (2007). MutS homologues hMSH4 and hMSH5: diverse functional implications in humans. Front Biosci 12: 905-911.
45. Hulvat MC, Jeruss JS. (2009). Maintaining fertility in young women with breast cancer. Curr Treat Options Oncol 10: 308-317.
46. Iwaoki Y, Matsuda H, Mutter GL, Watrin F, Wolgemuth DJ. (1993). Differential expression of the proto-oncogenes c-abl and c-mos in developing mouse germ cells. Exp Cell Res 206: 212-219.
47. Jackson SP, Bartek J. (2009). The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
48. Jeruss JS, Woodruff TK. (2009). Preservation of fertility in patients with cancer. N Engl J Med 360: 902-911.
49. Johnston RJ, Wallace WH. (2009). Normal ovarian function and assessment of ovarian reserve in the survivor of childhood cancer. Pediatr Blood Cancer 53: 296-302.
50. Jones EV, Dickman MJ, Whitmarsh AJ. (2007). Regulation of p73-mediated apoptosis by c-Jun N-terminal kinase. Biochem J 405: 617-623.
51. Junttila MR, Evan GI. (2009). p53-a Jack of all trades but master of none. Nat Rev Cancer 9: 821-829.
52. Kastan MB, Bartek J. (2004). Cell-cycle checkpoints and cancer. Nature 432: 316-323.
53. Khanna KK, Jackson SP. (2001). DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 27: 247-254.
54. Kharbanda S, Pandey P, Jin S, Inoue S, Bharti A, Yuan ZM et al. (1997a). Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature 386: 732-735.
55. Kharbanda S, Pandey P, Morris PL, Whang Y, Xu Y, Sawant S et al. (1998). Functional role for the c-Abl tyrosine kinase in meiosis I. Oncogene 16: 1773-1777.
56. Kharbanda S, Yuan ZM, Weichselbaum R, Kufe D. (1997b). Functional role for the c-Abl protein tyrosine kinase in the cellular response to genotoxic stress. Biochim Biophys Acta 1333: O1-O7.
57. Kitao H, Yuan ZM. (2002). Regulation of ionizing radiation-induced Rad52 nuclear foci formation by c-Abl-mediated phosphorylation. J Biol Chem 277: 48944-48948.
58. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou Jr H et al. (2000). MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14: 1085-1097.
59. Ko LJ, Prives C. (1996). p53: puzzle and paradigm. Genes Dev 10: 1054-1072.
60. Kurita T, Cunha GR, Robboy SJ, Mills AA, Medina RT. (2005). Differential expression of p63 isoforms in female reproductive organs. Mech Dev 122: 1043-1055.
61. Kuriyan J, Eisenberg D. (2007). The origin of protein interactions and allostery in colocalization. Nature 450: 983-990.
62. Lee JH, Paull TT. (2005). ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308: 551-554.
63. Lev Z, Leibovitz N, Segev O, Shilo BZ. (1984). Expression of the src and abl cellular oncogenes during development of Drosophila melanogaster. Mol Cell Biol 4: 982-984.
64. Li B, Boast S, de los Santos K, Schieren I, Quiroz M, Teitelbaum SL, et al. (2000). Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nat Genet 24: 304-308.
65. Lieber MR, Ma Y, Pannicke U, Schwarz K. (2004). The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. DNA Repair (Amst) 3: 817-826.
66. Lobo RA. (2005). Potential options for preservation of fertility in women. N Engl J Med 353: 64-73.
67. Lukas C, Falck J, Bartkova J, Bartek J, Lukas J. (2003). Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat Cell Biol 5: 255-260.
68. Maltaris T, Beckmann MW, Dittrich R. (2009). Review. Fertility preservation for young female cancer patients. In vivo 23: 123-130.
69. Maltaris T, Weigel M, Mueller A, Schmidt M, Seufert R, Fischl F et al.(2008). Cancer and fertility preservation: fertility preservation in breast cancer patients. Breast Cancer Res 10: 206.
70. Mandon-Pepin B, Touraine P, Kuttenn F, Derbois C, Rouxel A, Matsuda F et al. (2008). Genetic investigation of four meiotic genes in women with premature ovarian failure. Eur J Endocrinol 158:107-115.
71. Meijer D, Hermans A, von Lindern M, van Agthoven T, de Klein A, Mackenbach P et al. (1987). Molecular characterization of the testis specific c-abl mRNA in mouse. EMBO J 6: 4041-4048.
72. Michel B, Ehrlich SD, Uzest M. (1997). DNA double-strand breaks caused by replication arrest. EMBO J 16: 430-438.
73. Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, Haimovitz-Friedman A et al. (2000). Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat Med 6: 1109-1114.
74. Muller R, Slamon DJ, Tremblay JM, Cline MJ, Verma IM. (1982). Differential expression of cellular oncogenes during pre- and postnatal development of the mouse. Nature 299: 640-644.
75. Nagar B. (2007). c-Abl tyrosine kinase and inhibition by the cancer drug imatinib (Gleevec/STI-571). J Nutr 137: 1518S-1523S, discussion 1548S.
76. Nagar B, Hantschel O, Young MA, Scheffzek K, Veach D, Bornmann W et al. (2003). Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112: 859-871.
77. Nehme A, Baskaran R, Aebi S, Fink D, Nebel S, Cenni B et al. (1997). Differential induction of c-Jun NH2-terminal kinase and c-Abl kinase in DNA mismatch repair-proficient and -deficient cells exposed to cisplatin. Cancer Res 57: 3253-3257.
78. Ohndorf UM, Rould MA, He Q, Pabo CO, Lippard SJ. (1999). Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins. Nature 399: 708-712.
79. Ohren JF, Sebolt-Leopold JS. (2006). Inhibitors of Bcr-abl. Breaking new ground again. Nat Chem Biol 2: 63-64.
80. Ollmann M, Young LM, Di Como CJ, Karim F, Belvin M, Robertson S et al. (2000). Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101: 91-101.
81. Oppi C, Shore SK, Reddy EP. (1987). Nucleotide sequence of testis-derived c-abl cDNAs: implications for testis-specific transcription and abl oncogene activation. Proc Natl Acad Sci USA 84: 8200-8204.
82. Pandita TK. (2003). A multifaceted role for ATM in genome maintenance. Expert Rev Mol Med 5: 1-21.
83. Panier S, Durocher D. (2009). Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair (Amst) 8: 436-443.
84. Peate M, Meiser B, Hickey M, Friedlander M. (2009). The fertility-related concerns, needs and preferences of younger women with breast cancer: a systematic review. Breast Cancer Res Treat 116: 215-223.
85. Pendergast AM. (2002). The Abl family kinases: mechanisms of regulation and signaling. Adv Cancer Res 85: 51-100.
86. Petrini JH, Stracker TH. (2003). The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol 13: 458-462.
87. Ponzetto C, Wolgemuth DJ. (1985). Haploid expression of a unique c-abl transcript in the mouse male germ line. Mol Cell Biol 5: 1791-1794.
88. Propst F, Rosenberg MP, Oskarsson MK, Russell LB, Nguyen-Huu MC, Nadeau J et al. (1988). Genetic analysis and developmental regulation of testis-specific RNA expression of Mos, Abl, actin and Hox-1.4. Oncogene 2: 227-233.
89. Raina D, Ahmad R, Kumar S, Ren J, Yoshida K, Kharbanda S et al. (2006). MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J 25: 3774-3783.
90. Richardson C, Horikoshi N, Pandita TK. (2004). The role of the DNA double-strand break response network in meiosis. DNA Repair (Amst) 3: 1149-1164.
91. Riley T, Sontag E, Chen P, Levine A. (2008). Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9: 402-412.
92. Rogakou EP, Boon C, Redon C, Bonner WM. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
93. Rutkowski R, Hofmann K, Gartner A. (2010). Phylogeny and function of the invertebrate p53 superfamily. Cold Spring Harb Perspect Biol 2: a001131.
94. Sawyers CL, McLaughlin J, Goga A, Havlik M, Witte O. (1994). The nuclear tyrosine kinase c-Abl negatively regulates cell growth. Cell 77: 121-131.
95. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J. (2000). Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289: 1938-1942.
96. Schumacher B, Hofmann K, Boulton S, Gartner A. (2001). The C elegans homolog of the p 53 tumor suppressor is required for DNA damage-induced apoptosis. Curr Biol 11: 1722-1727.
97. Schumacher B, Schertel C, Wittenburg N, Tuck S, Mitani S, Gartner A et al. (2005). C elegans ced- 13 can promote apoptosis and is induced in response to DNA damage. Cell Death Differ 12:153-161.
98. Schwartzberg PL, Stall AM, Hardin JD, Bowdish KS, Humaran T, Boast S et al. (1991). Mice homozygous for the ablm1 mutation show poor viability and depletion of selected B and T cell populations. Cell 65: 1165-1175.
99. Shafman T, Khanna KK, Kedar P, Spring K, Kozlov S, Yen T et al. (1997). Interaction between ATM protein and c-Abl in response to DNA damage. Nature 387: 520-523.
100. Shaul Y. (2000). c-Abl: activation and nuclear targets. Cell Death Differ 7: 10-16.
101. Shaul Y, Ben-Yehoyada M. (2005). Role of c-Abl in the DNA damage stress response. Cell Res 15: 33-35.
102. Shilo BZ, Weinberg RA. (1981). DNA sequences homologous to vertebrate oncogenes are conserved in Drosophila melanogaster. Proc Natl Acad Sci USA 78: 6789-6792.
103. Shimizu H, Popova M, Fleury F, Kobayashi M, Hayashi N, Sakane I et al. (2009). c-ABL tyrosine kinase stabilizes RAD51 chromatin association. Biochem Biophys Res Commun 382: 286-291.
104. Sirvent A, Benistant C, Roche S. (2008). Cytoplasmic signalling by the c-Abl tyrosine kinase in normal and cancer cells. Biol Cell 100:617-631.
105. Sogame N, Kim M, Abrams JM. (2003). Drosophila p53 preserves genomic stability by regulating cell death. Proc Natl Acad Sci USA 100: 4696-4701.
106. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG et al. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72: 767-778.
107. Stojic L, Brun R, Jiricny J. (2004). Mismatch repair and DNA damage signalling. DNA Repair (Amst) 3: 1091-1101.
108. Suh EK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z et al. (2006). p63 protects the female germ line during meiotic arrest. Nature 444: 624-628.
109. Sun H, Treco D, Schultes NP, Szostak JW. (1989). Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338: 87-90.
110. Taagepera S, McDonald D, Loeb JE, Whitaker LL, McElroy AK, Wang JY et al. (1998). Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc Natl Acad Sci USA 95: 7457-7462.
111. Takao N, Mori R, Kato H, Shinohara A, Yamamoto K. (2000). c-Abl tyrosine kinase is not essential for ataxia telangiectasia mutated functions in chromosomal maintenance. J Biol Chem 275: 725-728.
112. Ting NS, Lee WH. (2004). The DNA double-strand break response pathway: becoming more BRCAish than ever. DNA Repair (Amst) 3: 935-944.
113. Tompkins JD, Wu X, Chu YL, Her C. (2009). Evidence for a direct involvement of hMSH5 in promoting ionizing radiation induced apoptosis. Exp Cell Res 315: 2420-2432.
114. Tybulewicz VL, Crawford CE, Jackson PK, Bronson RT, Mulligan RC. (1991). Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65:1153-1163.
115. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. (2003). Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 22: 5612-5621.
116. van der Kaaij MAE, van Echten-Arends J, Simons AH, Kluin-Nelemans HC. (2010). Fertility preservation after chemotherapy for Hodgkin lymphoma. Hematol Oncol (e-pub ahead of print 15 March 2010).
117. Vigneri P, Wang JY. (2001). Induction of apoptosis in chronic myelogenous leukemia cells through nuclear entrapment of BCR-ABL tyrosine kinase. Nat Med 7: 228-234.
118. Wang JY. (2000). Regulation of cell death by the Abl tyrosine kinase. Oncogene 19: 5643-5650.
119. Wang JY. (2004). Controlling Abl: auto-inhibition and co-inhibition? Nat Cell Biol 6: 3-7.
120. Wang JY, Baltimore D. (1983). Cellular RNA homologous to the Abelson murine leukemia virus transforming gene: expression and relationship to the viral sequence. Mol Cell Biol 3: 773-779.
121. Wang JY, Ki SW. (2001). Choosing between growth arrest and apoptosis through the retinoblastoma tumour suppressor protein, Abl and p73. Biochem Soc Trans 29: 666-673.
122. Ward JF. (1988). DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and repar-ability. Prog Nucleic Acid Res Mol Biol 35: 95-125.
123. Weinert TA, Hartwell LH. (1988). The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241: 317-322.
124. Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A, Griffin JD. (2007). Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat Rev Cancer 7: 345-356.
125. Wen ST, Jackson PK, Van Etten RA. (1996). The cytostatic function of c-Abl is controlled by multiple nuclear localization signals and requires the p53 and Rb tumor suppressor gene products. EMBO J 15: 1583-1595.
126. West ER, Zelinski MB, Kondapalli LA, Gracia C, Chang J, Coutifaris C et al. (2009). Preserving female fertility following cancer treatment: current options and future possibilities. Pediatr Blood Cancer 53: 289-295.
127. Williams JC, Weijland A, Gonfloni S, Thompson A, Courtneidge SA, Superti-Furga G et al. (1997). The 2.35 A crystal structure of the inactivated form of chicken Src: a dynamic molecule with multiple regulatory interactions. J Mol Biol 274: 757-775.
128. Woodruff TK. (2007). The emergence of a new interdiscipline: oncofertility. Cancer Treat Res 138: 3-11.
129. Woodruff TK. (2008). Making eggs: is it now or later? Nat Med 14:1190-1191.
130. Woodruff TK. (2009). Preserving fertility during cancer treatment. Nat Med 15: 1124-1125.
131. Xu W, Harrison SC, Eck MJ. (1997). Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595-602.
132. Yi W, Lee TH, Tompkins JD, Zhu F, Wu X, Her C. (2006). Physical and functional interaction between hMSH5 and c-Abl. Cancer Res 66: 151-158.
133. Yi W, Wu X, Lee TH, Doggett NA, Her C. (2005). Two variants of MutS homolog hMSH5: prevalence in humans and effects on protein interaction. Biochem Biophys Res Commun 332: 524-532.
134. Yoshida K. (2008). Nuclear trafficking of pro-apoptotic kinases in response to DNA damage. Trends Mol Med 14: 305-313.
135. Yoshida K, Yamaguchi T, Natsume T, Kufe D, Miki Y. (2005). JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat Cell Biol 7: 278-285.
136. Yuan J, Chen J. (2010). MRE11-RAD50-NBS1 complex dictates DNA repair independent of H2AX. J Biol Chem 285: 1097-1104.
137. Yuan SS, Chang HL, Lee EY. (2003). Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM(-/-) and c-Abl(-/-) cells. Mutat Res 525: 85-92.
138. Yuan SS, Lee SY, Chen G, Song M, Tomlinson GE, Lee EY. (1999). BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res 59: 3547-3551.
139. Yuan ZM, Huang Y, Ishiko T, Nakada S, Utsugisawa T, Kharbanda S et al. (1998). Regulation of Rad51 function by c-Abl in response to DNA damage. J Biol Chem 273: 3799-3802.
140. Zhang J, Adrian FJ, Jahnke W, Cowan-Jacob SW, Li AG, Iacob RE et al. (2010). Targeting Bcr-Abl by combining allosteric with ATP- binding-site inhibitors. Nature 463: 501-506.
141. Zhu J, Wang JY. (2004). Death by Abl: a matter of location. Curr Top Dev Biol 59: 165-192.