IGF-1R inhibition enhances radiosensitivity and delays double-strand break repair by both non-homologous end-joining and homologous recombination

Oncogene

Volumn 33, Issue 45, 2014, Pages 5262-5273

  Chitnis, M M ^a,b   Lodhia, K A ^a   Aleksic, T ^a   Gao, S ^a   Protheroe, A S ^b   Macaulay, V M ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CHURCHILL HOSPITAL   (United Kingdom)

Author keywords

DNA repair; double strand break; homologous recombination; IGF 1R; non homologous end joining; radiosensitization

Indexed keywords

2-MORPHOLIN-4-YL-6-THIANTHREN-1-YL-PYRAN-4-ONE; AZ 12253801; H2AFX PROTEIN, HUMAN; HISTONE; ISOXAZOLE DERIVATIVE; MORPHOLINE DERIVATIVE; PYRIMIDINE DERIVATIVE; PYRONE DERIVATIVE; QUINOLINE DERIVATIVE; RO 3306; SOMATOMEDIN C RECEPTOR; THIAZOLE DERIVATIVE;

ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL CYCLE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; FIBROBLAST; GENETICS; HEK293 CELL LINE; HOMOLOGOUS RECOMBINATION; HUMAN; KNOCKOUT MOUSE; METABOLISM; RADIATION DOSE; RADIATION RESPONSE; RECOMBINATION REPAIR; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; FIBROBLASTS; HEK293 CELLS; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; ISOXAZOLES; MICE, KNOCKOUT; MORPHOLINES; PYRIMIDINES; PYRONES; QUINOLINES; RADIATION TOLERANCE; RECEPTOR, IGF TYPE 1; RECOMBINATIONAL DNA REPAIR; THIAZOLES;

EID: 84926126979     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.460     Document Type: Article

References (73)

1. Rochester MA, Riedemann J, Hellawell GO, Brewster SF, Macaulay VM. Silencing of the IGF1R gene enhances sensitivity to DNA-damaging agents in both PTEN wild-type and mutant human prostate cancer. Cancer Gene Ther 2005; 12: 90–100. DOI: 10.1038/sj.cgt.7700775
2. Riesterer O, Yang Q, Raju U, Torres M, Molkentine D, Patel N et al. Combination of anti-IGF-1R antibody A12 and ionizing radiation in upper respiratory tract cancers. Int J Radiat Oncol Biol Phys 2011; 79: 1179–1187. DOI: 10.1016/j.ijrobp.2010.10.003
3. Isebaert SF, Swinnen JV, McBride WH, Haustermans KM. Insulin-like growth factor-type 1 receptor inhibitor NVP-AEW541 enhances radiosensitivity of PTEN wild-type but not PTEN-deficient human prostate cancer cells. Int J Radiat Oncol Biol Phys 2011; 81: 239–247. DOI: 10.1016/j.ijrobp.2011.03.030
4. Ferte C, Loriot Y, Clemenson C, Commo F, Gombos A, Bibault JE et al. IGF-1R targeting increases the antitumor effects of DNA damaging agents in SCLC model: an opportunity to increase the efficacy of standard therapy. Mol Cancer Ther 2013; 12: 1213–1222. DOI: 10.1158/1535-7163.MCT-12-1067
5. Molife LR, Fong PC, Paccagnella L, Reid AH, Shaw HM, Vidal L et al. The insulin-like growth factor-I receptor inhibitor figitumumab (CP-751,871) in combination with docetaxel in patients with advanced solid tumours: results of a phase Ib dose-escalation, open-label study. Br J Cancer 2010; 103: 332–339. DOI: 10.1038/sj.bjc.6605767
6. Javle MM, Varadhachary GR, Fogelman DR, Shroff RT, Overman MJ, Ukegbu L et al. Randomized phase II study of gemcitabine (G) plus anti-IGF-1R antibody MK-0646, G plus erlotinib (E) plus MK-0646 and G plus E for advanced pancreatic cancer. J Clin Oncol 2011; 29 (suppl)abstr 4026. DOI: 10.1200/jco.2011.29.15_suppl.4026
7. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? J Natl Cancer Inst 2012; 104: 975–981. DOI: 10.1093/jnci/djs258
8. Hellawell GO, Turner GD, Davies DR, Poulsom R, Brewster SF, Macaulay VM. Expression of the type 1 insulin-like growth factor receptor is up-regulated in primary prostate cancer and commonly persists in metastatic disease. Cancer Res 2002; 62: 2942–2950.
9. Grzmil M, Hemmerlein B, Thelen P, Schweyer S, Burfeind P. Blockade of the type I IGF receptor expression in human prostate cancer cells inhibits proliferation and invasion, up-regulates IGF binding protein-3, and suppresses MMP-2 expression. J Pathol 2004; 202: 50–59. DOI: 10.1002/path.1492
10. Krueckl SL, Sikes RA, Edlund NM, Bell RH, Hurtado-Coll A, Fazli L et al. Increased insulin-like growth factor I receptor expression and signaling are components of androgen-independent progression in a lineage-derived prostate cancer progression model. Cancer Res 2004; 64: 8620–8629. DOI: 10.1158/0008-5472.CAN-04-2446
11. Liao Y, Abel U, Grobholz R, Hermani A, Trojan L, Angel P et al. Up-regulation of insulin-like growth factor axis components in human primary prostate cancer correlates with tumor grade. Hum Pathol 2005; 36: 1186–1196. DOI: 10.1016/j.humpath.2005.07.023
12. Sroka IC, McDaniel K, Nagle RB, Bowden GT. Differential localization of MT1-MMP in human prostate cancer tissue: role of IGF-1R in MT1-MMP expression. Prostate 2008; 68: 463–476. DOI: 10.1002/pros.20718
13. Turney BW, Kerr M, Chitnis MM, Lodhia K, Wang Y, Riedemann J et al. Depletion of the type 1 IGF receptor delays repair of radiation-induced DNA double strand breaks. Radiother Oncol 2012; 103: 402–409. DOI: 10.1016/j.radonc.2012.03.009
14. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461: 1071–1078. DOI: 10.1038/nature08467
15. Aleksic T, Chitnis MM, Perestenko OV, Gao S, Thomas PH, Turner GD et al. Type 1 insulin-like growth factor receptor translocates to the nucleus of human tumor cells. Cancer Res 2010; 70: 6412–6419. DOI: 10.1158/0008-5472.CAN-10-0052
16. Shaw PH, Maughan TS, Clarke AR. Dual inhibition of epidermal growth factor and insulin-like 1 growth factor receptors reduce intestinal adenoma burden in the Apc(min/+) mouse. Br J Cancer 2011; 105: 649–657. DOI: 10.1038/bjc.2011.291
17. Sell C, Dumenil G, Deveaud C, Miura M, Coppola D, DeAngelis T et al. Effect of a null mutation of the insulin-like growth factor I receptor gene on growth and transformation of mouse embryo fibroblasts. Mol Cell Biol 1994; 14: 3604–3612. DOI: 10.1128/MCB.14.6.3604
18. Tezuka M, Watanabe H, Nakamura S, Yu D, Aung W, Sasaki T et al. Antiapoptotic activity is dispensable for insulin-like growth factor I receptor-mediated clonogenic radioresistance after gamma-irradiation. Clin Cancer Res 2001; 7: 3206–3214.
19. Reiss K, Wang JY, Romano G, Furnari FB, Cavenee WK, Morrione A et al. IGF-I receptor signaling in a prostatic cancer cell line with a PTEN mutation. Oncogene 2000; 19: 2687–2694. DOI: 10.1038/sj.onc.1203587
20. McConkey DJ, Greene G, Pettaway CA. Apoptosis resistance increases with metastatic potential in cells of the human LNCaP prostate carcinoma line. Cancer Res 1996; 56: 5594–5599.
21. Kurmasheva RT, Houghton PJ. IGF-I mediated survival pathways in normal and malignant cells. Biochim Biophys Acta 2006; 1766: 1–22.
22. Dupont J, Holzenberger M. IGF type 1 receptor: a cell cycle progression factor that regulates aging. Cell Cycle 2003; 2: 270–272. DOI: 10.4161/cc.2.4.408
23. Bowen C, Birrer M, Gelmann EP. Retinoblastoma protein-mediated apoptosis after gamma-irradiation. J Biol Chem 2002; 277: 44969–44979. DOI: 10.1074/jbc.M202000200
24. Kuemmerle JF, Zhou H, Bowers JG. IGF-I stimulates human intestinal smooth muscle cell growth by regulation of G1 phase cell cycle proteins. Am J Physiol Gastrointest Liver Physiol 2004; 286: G412–G419. DOI: 10.1152/ajpgi.00403.2003
25. Wu JD, Odman A, Higgins LM, Haugk K, Vessella R, Ludwig DL et al. In vivo effects of the human type I insulin-like growth factor receptor antibody A12 on androgen-dependent and androgen-independent xenograft human prostate tumors. Clin Cancer Res 2005; 11: 3065–3074. DOI: 10.1158/1078-0432.CCR-04-1586
26. Flanigan SA, Pitts TM, Eckhardt SG, Tentler JJ, Tan AC, Thorburn A et al. The insulin-like growth factor I receptor/insulin receptor tyrosine kinase inhibitor PQIP exhibits enhanced antitumor effects in combination with chemotherapy against colorectal cancer models. Clin Cancer Res 2010; 16: 5436–5446. DOI: 10.1158/1078-0432.CCR-10-2054
27. Bielen A, Box G, Perryman L, Bjerke L, Popov S, Jamin Y et al. Dependence of Wilms tumor cells on signaling through insulin-like growth factor 1 in an orthotopic xenograft model targetable by specific receptor inhibition. Proc Natl Acad Sci USA 2012; 109: E1267–E1276. DOI: 10.1073/pnas.1105034109
28. Hinz JM, Yamada NA, Salazar EP, Tebbs RS, Thompson LH. Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair 2005; 4: 782–792. DOI: 10.1016/j.dnarep.2005.03.005
29. Shrivastav M, De Haro LP, Nickoloff JA. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008; 18: 134–147. DOI: 10.1038/cr.2007.111
30. Zhang R, Adams PD. Heterochromatin and its relationship to cell senescence and cancer therapy. Cell Cycle 2007; 6: 784–789. DOI: 10.4161/cc.6.7.4079
31. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008; 31: 167–177. DOI: 10.1016/j.molcel.2008.05.017
32. Sprenger CC, Vail ME, Evans K, Simurdak J, Plymate SR. Over-expression of insulin-like growth factor binding protein-related protein-1(IGFBP-rP1/mac25) in the M12 prostate cancer cell line alters tumor growth by a delay in G1 and cyclin A associated apoptosis. Oncogene 2002; 21: 140–147. DOI: 10.1038/sj.onc.1205021
33. Scurr LL, Pupo GM, Becker TM, Lai K, Schrama D, Haferkamp S et al. IGFBP7 is not required for B-RAF-induced melanocyte senescence. Cell 2010; 141: 717–727. DOI: 10.1016/j.cell.2010.04.021
34. Ewald JA, Desotelle JA, Wilding G, Jarrard DF. Therapy-induced senescence in cancer. J Natl Cancer Inst 2010; 102: 1536–1546. DOI: 10.1093/jnci/djq364
35. Steiner MS, Zhang Y, Farooq F, Lerner J, Wang Y, Lu Y. Adenoviral vector containing wild-type p16 suppresses prostate cancer growth and prolongs survival by inducing cell senescence. Cancer Gene Ther 2000; 7: 360–372. DOI: 10.1038/sj.cgt.7700151
36. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15: 1153–1162. DOI: 10.1038/cdd.2008.47
37. Wouters BG. Cell Death After Irradiation: How, When and Why Cells Die 4th Edn-Great Britain (ed) Hodder Arnold, London UK, 2009). DOI: 10.1201/b13224-4
38. Trojanek J, Ho T, Del Valle L, Nowicki M, Wang JY, Lassak A et al. 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 2003; 23: 7510–7524. DOI: 10.1128/MCB.23.21.7510-7524.2003
39. Cosaceanu D, Budiu RA, Carapancea M, Castro J, Lewensohn R, Dricu A. 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 2007; 26: 2423–2434. DOI: 10.1038/sj.onc.1210037
40. Lobrich M, Shibata A, Beucher A, Fisher A, Ensminger M, Goodarzi AA et al. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010; 9: 662–669. DOI: 10.4161/cc.9.4.10764
41. Ward IM, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001; 276: 47759–47762. DOI: 10.1074/jbc.C100569200
42. Solier S, Pommier Y. The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases. Cell Cycle 2009; 8: 1853–1859. DOI: 10.4161/cc.8.12.8865
43. Solier S, Pommier Y. MDC1 cleavage by caspase-3: a novel mechanism for inactivating the DNA damage response during apoptosis. Cancer Res 2011; 71: 906–913. DOI: 10.1158/0008-5472.CAN-10-3297
44. Wang B, Matsuoka S, Carpenter PB, Elledge SJ. 53BP1, a mediator of the DNA damage checkpoint. Science 2002; 298: 1435–1438. DOI: 10.1126/science.1076182
45. Macaulay VM, Salisbury AJ, Bohula EA, Playford MP, Smorodinsky NI, Shiloh Y. Downregulation of the type 1 insulin-like growth factor receptor in mouse melanoma cells is associated with enhanced radiosensitivity and impaired activation of Atm kinase. Oncogene 2001; 20: 4029–4040. DOI: 10.1038/sj.onc.1204565
46. Jeon JH, Kim SK, Kim HJ, Chang J, Ahn CM, Chang YS. Insulin-like growth factor-1 attenuates cisplatin-induced gammaH2AX formation and DNA double-strand breaks repair pathway in non-small cell lung cancer. Cancer Lett 2008; 272: 232–241. DOI: 10.1016/j.canlet.2008.07.011
47. Rothkamm K, Kruger I, Thompson LH, Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003; 23: 5706–5715. DOI: 10.1128/MCB.23.16.5706-5715.2003
48. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011; 25: 409–433. DOI: 10.1101/gad.2021311
49. Allalunis-Turner MJ, Zia PK, Barron GM, Mirzayans R, Day RS 3rd. Radiation-induced DNA damage and repair in cells of a radiosensitive human malignant glioma cell line. Radiat Res 1995; 144: 288–293. DOI: 10.2307/3578948
50. Zhao Y, Thomas HD, Batey MA, Cowell IG, Richardson CJ, Griffin RJ et al. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res 2006; 66: 5354–5362. DOI: 10.1158/0008-5472.CAN-05-4275
51. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 2008; 4: e1000110. DOI: 10.1371/journal.pgen.1000110
52. Johnson N, Li YC, Walton ZE, Cheng KA, Li D, Rodig SJ et al. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat Med 2011; 17: 875–882. DOI: 10.1038/nm.2377
53. Litzenburger BC, Creighton CJ, Tsimelzon A, Chan BT, Hilsenbeck SG, Wang T et al. High IGF-IR activity in triple-negative breast cancer cell lines and tumorgrafts correlates with sensitivity to anti-IGF-IR therapy. Clin Cancer Res 2011; 17: 2314–2327. DOI: 10.1158/1078-0432.CCR-10-1903
54. Fabbri F, Amadori D, Carloni S, Brigliadori G, Tesei A, Ulivi P et al. Mitotic catastrophe and apoptosis induced by docetaxel in hormone-refractory prostate cancer cells. J Cell Physiol 2008; 217: 494–501. DOI: 10.1002/jcp.21522
55. Carboni JM, Wittman M, Yang Z, Lee F, Greer A, Hurlburt W et al. BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Mol Cancer Ther 2009; 8: 3341–3349. DOI: 10.1158/1535-7163.MCT-09-0499
56. Gonzalez-Vasconcellos I, Anastasov N, Sanli-Bonazzi B, Klymenko O, Atkinson MJ, Rosemann M. Rb1 haploinsufficiency promotes telomere attrition and radiation-induced genomic instability. Cancer Res 2013; 73: 4247–4255. DOI: 10.1158/0008-5472.CAN-12-3117
57. Xu N, Lao Y, Zhang Y, Gillespie DA. Akt: a double-edged sword in cell proliferation and genome stability. J Oncol 2012; 2012: 951724. DOI: 10.1155/2012/951724
58. Lloret M, Lara PC, Bordon E, Fontes F, Rey A, Pinar B et al. Major vault protein may affect nonhomologous end-joining repair and apoptosis through Ku70/80 and bax downregulation in cervical carcinoma tumors. Int J Radiat Oncol Biol Phys 2009; 73: 976–979. DOI: 10.1016/j.ijrobp.2008.11.013
59. Valenciano A, Henriquez-Hernandez LA, Moreno M, Lloret M, Lara PC. Role of IGF-1 receptor in radiation response. Trans Oncol 2012; 5: 1–9. DOI: 10.1593/tlo.11265
60. Sehat B, Tofigh A, Lin Y, Trocme E, Liljedahl U, Lagergren J et al. SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor. Sci Signal 2010; 3: ra10. DOI: 10.1126/scisignal.2000628
61. Sarfstein R, Pasmanik-Chor M, Yeheskel A, Edry L, Shomron N, Warman N et al. Insulin-like growth factor-I receptor (IGF-IR) translocates to nucleus and autoregulates IGF-IR gene expression in breast cancer cells. J Biol Chem 2012; 287: 2766–2776. DOI: 10.1074/jbc.M111.281782
62. Dittmann K, Mayer C, Fehrenbacher B, Schaller M, Raju U, Milas L et al. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 2005; 280: 31182–31189. DOI: 10.1074/jbc.M506591200
63. Kornmann M, Arber N, Korc M. Inhibition of basal and mitogen-stimulated pancreatic cancer cell growth by cyclin D1 antisense is associated with loss of tumorigenicity and potentiation of cytotoxicity to cisplatinum. J Clin Invest 1998; 101: 344–352. DOI: 10.1172/JCI1323
64. Jirawatnotai S, Hu Y, Michowski W, Elias JE, Becks L, Bienvenu F et al. A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature 2011; 474: 230–234. DOI: 10.1038/nature10155
65. Yata K, Esashi F. Dual role of CDKs in DNA repair: to be, or not to be. DNA Repair 2009; 8: 6–18. DOI: 10.1016/j.dnarep.2008.09.002
66. Bolderson E, Richard DJ, Zhou BB, Khanna KK. Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair. Clin Cancer Res 2009; 15: 6314–6320. DOI: 10.1158/1078-0432.CCR-09-0096
67. Harrington KJ, Billingham LJ, Brunner TB, Burnet NG, Chan CS, Hoskin P et al. Guidelines for preclinical and early phase clinical assessment of novel radiosensitisers. Br J Cancer 2011; 105: 628–639. DOI: 10.1038/bjc.2011.240
68. Roberts DJ, Spellman RA, Sanok K, Chen H, Chan M, Yurt P et al. Interlaboratory assessment of mitotic index by flow cytometry confirms superior reproducibility relative to microscopic scoring. Environ Mol Mutagen 2012; 53: 297–303. DOI: 10.1002/em.21684
69. Sramkoski RM, Pretlow TG 2nd, Giaconia JM, Pretlow TP, Schwartz S, Sy MS et al. A new human prostate carcinoma cell line, 22Rv1. In Vitro Cell Dev Biol Anim 1999; 35: 403–409. DOI: 10.1007/s11626-999-0115-4
70. Fraser M, Zhao H, Luoto KR, Lundin C, Coackley C, Chan N et al. PTEN deletion in prostate cancer cells does not associate with loss of RAD51 function: implications for radiotherapy and chemotherapy. Clin Cancer Res 2012; 18: 1015–1027. DOI: 10.1158/1078-0432.CCR-11-2189
71. Lehmann BD, McCubrey JA, Jefferson HS, Paine MS, Chappell WH, Terrian DM. A dominant role for p53-dependent cellular senescence in radiosensitization of human prostate cancer cells. Cell Cycle 2007; 6: 595–605. DOI: 10.4161/cc.6.5.3901
72. Scott SL, Earle JD, Gumerlock PH. Functional p53 increases prostate cancer cell survival after exposure to fractionated doses of ionizing radiation. Cancer Res 2003; 63: 7190–7196.
73. Mujoo K, Watanabe M, Khokhar AR, Siddik ZH. Increased sensitivity of a metastatic model of prostate cancer to a novel tetravalent platinum analog. Prostate 2005; 62: 91–100. DOI: 10.1002/pros.20114