Hypoxia and DNA repair

Yale Journal of Biology and Medicine

Volumn 86, Issue 4, 2013, Pages 443-451

  Glazer, Peter M ^a   Hegan, Denise C ^a   Lu, Yuhong ^a   Czochor, Jennifer ^a   Scanlon, Susan E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BRCA1; DNA repair; Epigenetics; Homologous recombination; Hypoxia; MicroRNAs; Mismatch repair; MLH1; Silencing

Indexed keywords

CHECKPOINT KINASE 2; DNA; MICRORNA; MICRORNA 155; MYC PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN MLH1; PROTEIN MSH2; PROTEIN P130; RAD51 PROTEIN; TRANSCRIPTION FACTOR E2F4;

ARTICLE; CANCER CELL; CANCER GROWTH; DNA REPAIR; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC STABILITY; HUMAN; HYPOXIA; MLH1 GENE; MMR GENE; MSH2 GENE; PHENOTYPE; PROMOTER REGION; PROTEIN BINDING; RAD51 GENE; RADIOSENSITIVITY; SENSITIVITY ANALYSIS; SOLID TUMOR; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE;

BRCA1; DNA REPAIR; EPIGENETICS; HOMOLOGOUS RECOMBINATION; HYPOXIA; MICRORNAS; MISMATCH REPAIR; MLH1; SILENCING;

ANOXIA; CELL HYPOXIA; CELL LINE, TUMOR; DNA REPAIR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HUMANS; MODELS, GENETIC; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84891139530     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Williams KJ, Cowen RL, Stratford IJ. Hypoxia and oxidative stress. Tumour hypoxia--therapeutic considerations. Breast Cancer Res. 2001;3(5):328-331. [PMC free article][PubMed]
2. Nordsmark M, Overgaard M, Overgaard J. Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck. Radiother Oncol. 1996;41(1):31-39. [PubMed]
3. Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Dodge RK, Charles HC. et al. Radiation therapy and hyperthermia improve the oxygenation of human soft tissue sarcomas. Cancer Res. 1996;56(23):5347-5350. [PubMed]
4. Gruber G, Greiner RH, Hlushchuk R, Aebersold DM, Altermatt HJ, Berclaz G. et al. Hypoxia-inducible factor 1 alpha in high-risk breast cancer: an independent prognostic parameter? Breast Cancer Res. 2004;6(3):R191-R198. [PMC free article][PubMed]
5. Rockwell S. Oxygen delivery: implications for the biology and therapy of solid tumors. Oncol Res. 1997;9(6-7):383-390. [PubMed]
6. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 1996;56(19):4509-4515. [PubMed]
7. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol. 2000;35(2):71-103. [PubMed]
8. Koong AC, Denko NC, Hudson KM, Schindler C, Swiersz L, Koch C. et al. Candidate genes for the hypoxic tumor phenotype. Cancer Res. 2000;60(4):883-887. [PubMed]
9. Sutherland RM. Tumor hypoxia and gene expression--implications for malignant progression and therapy. Acta Oncol. 1998;37(6):567-574. [PubMed]
10. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ. et al. Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci USA. 1997;94(15):8104-8109. [PMC free article][PubMed]
11. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW. et al. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med. 2001;7(4):437-443. [PubMed]
12. Ivanova AV, Ivanov SV, Danilkovitch-Miagkova A, Lerman MI. Regulation of STRA13 by the von Hippel-Lindau tumor suppressor protein, hypoxia, and the UBC9/ubiquitin proteasome degradation pathway. J Biol Chem. 2001;276(18):15306-15315. [PubMed]
13. Denko N, Wernke-Dollries K, Johnson AB, Hammond E, Chiang CM, Barton MC. Hypoxia actively represses transcription by inducing negative cofactor 2 (Dr1/DrAP1) and blocking preinitiation complex assembly. J Biol Chem. 2003;278(8):5744-5749. [PubMed]
14. Alarcon RM, Denko NC, Giaccia AJ. Genetic determinants that influence hypoxia-induced apoptosis. Novartis Found Symp. 2001;240:115-128, discussion 128-132. [PubMed]
15. Dong Z, Venkatachalam MA, Wang J, Patel Y, Saikumar P, Semenza GL. et al. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia. Hif-1-independent mechanisms. J Biol Chem. 2001;276(22):18702-18709. [PMC free article][PubMed]
16. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment. Cancer Res. 1996;56(24):5754-5757. [PubMed]
17. Bindra RS, Glazer PM. Genetic instability and the tumor microenvironment: towards the concept of microenvironment-induced mutagenesis. Mutat Res. 2005;569(1-2):75-85. [PubMed]
18. Li CY, Little JB, Hu K, Zhang W, Zhang L, Dewhirst MW. et al. Persistent genetic instability in cancer cells induced by non-DNA-damaging stress exposures. Cancer Res. 2001;61(2):428-432. [PubMed]
19. Paquette B, Little JB. In vivo enhancement of genomic instability in minisatellite sequences of mouse C3H/10T1/2 cells transformed in vitro by X-rays. Cancer Res. 1994;54(12):3173-3178. [PubMed]
20. Yuan J, Narayanan L, Rockwell S, Glazer PM. Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Res. 2000;60(16):4372-4376. [PubMed]
21. Yuan J, Glazer PM. Mutagenesis induced by the tumor microenvironment. Mutat Res. 1998;400(1-2):439-446. [PubMed]
22. Rockwell S, Yuan J, Peretz S, Glazer PM. Genomic instability in cancer. Novartis Found Symp. 2001;240:133-142; discussion 142-151. [PubMed]
23. Mihaylova VT, Bindra RS, Yuan J, Campisi D, Narayanan L, Jensen R. et al. Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells. Mol Cell Biol. 2003;23(9):3265-3273. [PMC free article][PubMed]
24. Koshiji M, To KK, Hammer S, Kumamoto K, Harris AL, Modrich P. et al. HIF-1alpha induces genetic instability by transcriptionally downregulating MutSalpha expression. Mol Cell. 2005;17(6):793-803. [PubMed]
25. Hammond EM, Giaccia AJ. The role of ATM and ATR in the cellular response to hypoxia and re-oxygenation. DNA Repair (Amst) 2004;3(8-9):1117-1122. [PubMed]
26. Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME. et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol. 2004;24(19):8504-8518. [PMC free article][PubMed]
27. Bindra RS, Glazer PM. Co-repression of mismatch repair gene expression by hypoxia in cancer cells: Role of the Myc/Max network. Cancer Lett. 2007;252(1):93-103. [PubMed]
28. Bindra RS, Glazer PM. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene. 2006;26(14):2048-2057. [PubMed]
29. Bindra RS, Gibson SL, Meng A, Westermark U, Jasin M, Pierce AJ. et al. Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res. 2005;65(24):11597-11604. [PubMed]
30. Papp-Szabo E, Josephy PD, Coomber BL. Microenvironmental influences on mutagenesis in mammary epithelial cells. Int J Cancer. 2005;116(5):679-685. [PubMed]
31. Shahrzad S, Quayle L, Stone C, Plumb C, Shirasawa S, Rak JW. et al. Ischemia-induced K-ras mutations in human colorectal cancer cells: role of microenvironmental regulation of MSH2 expression. Cancer Res. 2005;65(18):8134-8141. [PubMed]
32. Hammond EM, Green SL, Giaccia AJ. Comparison of hypoxia-induced replication arrest with hydroxyurea and aphidicolin-induced arrest. Mutat Res. 2003;532(1-2):205-213. [PubMed]
33. Coquelle A, Toledo F, Stern S, Bieth A, Debatisse M. A new role for hypoxia in tumor progression: induction of fragile site triggering genomic rearrangements and formation of complex DMs and HSRs. Mol Cell. 1998;2(2):259-265. [PubMed]
34. Young SD, Marshall RS, Hill RP. Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc Natl Acad Sci USA. 1988;85(24):9533-9537. [PMC free article][PubMed]
35. Francia G, Green SK, Bocci G, Man S, Emmenegger U, Ebos JM. et al. Down-regulation of DNA mismatch repair proteins in human and murine tumor spheroids: implications for multicellular resistance to alkylating agents. Mol Cancer Ther. 2005;4(10):1484-1494. [PubMed]
36. Bindra RS, Glazer PM. Basal repression of BRCA1 by multiple E2Fs and pocket proteins at adjacent E2F sites. Cancer Biol Ther. 2006;5(10):1400-1407. [PubMed]
37. Gibson SL, Bindra RS, Glazer PM. Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Res. 2005;65(23):10734-10741. [PubMed]
38. Gibson SL, Bindra RS, Glazer PM. CHK2-dependent phosphorylation of BRCA1 in hypoxia. Radiat Res. 2006;166(4):646-651. [PubMed]
39. Liang X, Reed E, Yu JJ. Protein phosphatase 2A interacts with Chk2 and regulates phosphorylation at Thr-68 after cisplatin treatment of human ovarian cancer cells. Int J Mol Med. 2006;17(5):703-708. [PubMed]
40. Dozier C, Bonyadi M, Baricault L, Tonasso L, Darbon JM. Regulation of Chk2 phosphorylation by interaction with protein phosphatase 2A via its B' regulatory subunit. Biol Cell. 2004;96(7):509-517. [PubMed]
41. Gibson SL, Narayanan L, Hegan DC, Buermeyer AB, Liskay RM, Glazer PM. Overexpression of the DNA mismatch repair factor, PMS2, confers hypermutability and DNA damage tolerance. Cancer Lett. 2006;244(2):195-202. [PubMed]
42. Hegan DC, Narayanan L, Jirik FR, Edelmann W, Liskay RM, Glazer PM. Differing patterns of genetic instability in mice deficient in the mismatch repair genes Pms2, Mlh1, Msh2, Msh3 and Msh6. Carcinogenesis. 2006;27(12):2402-2408. [PMC free article][PubMed]
43. Smith-Roe SL, Lohr CV, Bildfell RJ, Fischer KA, Hegan DC, Glazer PM. et al. Induction of aberrant crypt foci in DNA mismatch repair-deficient mice by the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine (PhIP) Cancer Lett. 2006;244(1):79-85. [PubMed]
44. Smith-Roe SL, Hegan DC, Glazer PM, Buermeyer AB. Mlh1-dependent suppression of specific mutations induced in vivo by the food-borne carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine (PhIP) Mutat Res. 2006;594(1-2):101-112. [PubMed]
45. Adhikary S, Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol. 2005;6(8):635-645. [PubMed]
46. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999;13(20):2633-2638. [PMC free article][PubMed]
47. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E. et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434(7035):913-917. [PubMed]
48. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917-921. [PubMed]
49. Hegan DC, Lu Y, Stachelek GC, Crosby ME, Bindra RS, Glazer PM. Inhibition of poly(ADP-ribose) polymerase down-regulates BRCA1 and RAD51 in a pathway mediated by E2F4 and p130. Proc Natl Acad Sci USA. 2010;107(5):2201-2206. [PMC free article][PubMed]
50. Chan N, Koritzinsky M, Zhao H, Bindra R, Glazer PM, Powell S. et al. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res. 2008;68(2):605-614. [PubMed]
51. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res. 2009;69(3):1221-1229. [PMC free article][PubMed]
52. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F. et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103(7):2257-2261. [PMC free article][PubMed]
53. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M. et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9(3):189-198. [PubMed]
54. Donnem T, Eklo K, Berg T, Sorbye SW, Lonvik K, Al-Saad S. et al. Prognostic impact of MiR-155 in non-small cell lung cancer evaluated by in situ hybridization. J Transl Med. 2011;9:6. [PMC free article][PubMed]
55. Babar IA, Czochor J, Steinmetz A, Weidhaas JB, Glazer PM, Slack FJ. Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther. 2011;12(10):908-914. [PMC free article][PubMed]
56. Valeri N, Gasparini P, Fabbri M, Braconi C, Veronese A, Lovat F. et al. Modulation of mismatch repair and genomic stability by miR-155. Proc Natl Acad Sci USA. 2010;107(15):6982-6987. [PMC free article][PubMed]
57. Bindra RS, Gibson SL, Meng A, Westermark U, Jasin M, Pierce AJ. et al. Hypoxia-Induced Down-regulation of BRCA1 Expression by E2Fs. Cancer Res. 2005;65(24):11597-11604. [PubMed]
58. Bindra RS, Glazer PM. Genetic instability and the tumor microenvironment: towards the concept of microenvironment-induced mutagenesis. Mutat Res. 2005;569(1-2):75-85. [PubMed]
59. Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME. et al. Down-Regulation of Rad51 and Decreased Homologous Recombination in Hypoxic Cancer Cells. Mol Cell Biol. 2004;24(19):8504-8518. [PMC free article][PubMed]
60. Bindra RS, Glazer PM. Co-repression of mismatch repair gene expression by hypoxia in cancer cells: Role of the Myc/Max network. Cancer Lett. 2007;252(1):93-103. [PubMed]
61. Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa J-PJ. et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA. 1998;95(12):6870-6875. [PMC free article][PubMed]
62. Esteller M, Corn PG, Baylin SB, Herman JG. A Gene Hypermethylation Profile of Human Cancer. Cancer Res. 2001;61(8):3225-3229. [PubMed]
63. Catteau A, Harris WH, Xu CF, Solomon E. Methylation of the BRCA1 promoter region in sporadic breast and ovarian cancer: correlation with disease characteristics. Oncogene. 1999;18(11):1957-1965. [PubMed]
64. Chen H, Yan Y, Davidson TL, Shinkai Y, Costa M. Hypoxic Stress Induces Dimethylated Histone H3 Lysine 9 through Histone Methyltransferase G9a in Mammalian Cells. Cancer Res. 2006;66(18):9009-9016. [PubMed]
65. McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, Baylin SB. Silenced Tumor Suppressor Genes Reactivated by DNA Demethylation Do Not Return to a Fully Euchromatic Chromatin State. Cancer Res. 2006;66(7):3541-3549. [PubMed]
66. Vakoc CR, Sachdeva MM, Wang H, Blobel GA. Profile of Histone Lysine Methylation across Transcribed Mammalian Chromatin. Mol Cell Biol. 2006;26(24):9185-9195. [PMC free article][PubMed]
67. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C. et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet. 2008;40(6):741-750. [PubMed]
68. Li X, Liu J, Zhou R, Huang S, Chen XM. Gene silencing of MIR22 in acute lymphoblastic leukaemia involves histone modifications independent of promoter DNA methylation. Br J Haematol. 2010;148(1):69-79. [PubMed]
69. Lee SH, Kim J, Kim WH, Lee YM. Hypoxic silencing of tumor suppressor RUNX3 by histone modification in gastric cancer cells. Oncogene. 2008;28(2):184-194. [PubMed]
70. Johnson AB, Denko N, Barton MC. Hypoxia induces a novel signature of chromatin modifications and global repression of transcription. Mutat Res. 2008;640(1-2):174-179. [PMC free article][PubMed]
71. Kasper LH, Boussouar F, Boyd K, Xu W, Biesen M, Rehg J. et al. Two transactivation mechanisms cooperate for the bulk of HIF-1-responsive gene expression. EMBO J. 2005;24(22):3846-3858. [PMC free article][PubMed]
72. Beyer S, Kristensen MM, Jensen KS, Johansen JV, Staller P. The Histone Demethylases JMJD1A and JMJD2B Are Transcriptional Targets of Hypoxia-inducible Factor HIF. J Biol Chem. 2008;283(52):36542-36552. [PMC free article][PubMed]
73. Xia X, Lemieux ME, Li W, Carroll JS, Brown M, Liu XS. et al. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc Natl Acad Sci USA. 2009;106(11):4260-4265. [PMC free article][PubMed]
74. Yang J, Ledaki I, Turley H, Gatter KC, Montero J-CM, Li J-L. et al. Role of Hypoxia-Inducible Factors in Epigenetic Regulation via Histone Demethylases. Ann NY Acad Sci. 2009;1177:185-197. [PubMed]
75. Krieg AJ, Rankin EB, Chan D, Razorenova O, Fernandez S, Giaccia AJ. Regulation of the Histone Demethylase JMJD1A by Hypoxia-Inducible Factor 1{alpha} Enhances Hypoxic Gene Expression and Tumor Growth. Mol Cell Biol. 2010;30(1):344-353. [PMC free article][PubMed]
76. Vasilatos SN, Broadwater G, Barry WT, Baker JC, Lem S, Dietze EC. et al. CpG Island Tumor Suppressor Promoter Methylation in Non-BRCA-Associated Early Mammary Carcinogenesis. Cancer Epidemiol Biomarkers Prev. 2009;18(3):901-914. [PMC free article][PubMed]
77. Mirza S, Sharma G, Prasad CP, Parshad R, Srivastava A, Gupta SD. et al. Promoter hypermethylation of TMS1, BRCA1, ER[alpha] and PRB in serum and tumor DNA of invasive ductal breast carcinoma patients. Life Sci. 2007;81(4):280-287. [PubMed]
78. Jin W, Chen L, Chen Y, Xu S-g, Di G-h, Yin W-j. et al. UHRF1 is associated with epigenetic silencing of BRCA1 in sporadic breast cancer. Breast Cancer Res Treat. 2010;123(2):359-373. [PubMed]
79. Lu Y, Chu A, Turker MS, Glazer PM. Hypoxia-induced epigenetic regulation and silencing of the BRCA1 promote. Mol Cell Biol. 2011;31(16):3339-3350. [PMC free article][PubMed]