Tumor hypoxia and genetic alterations in sporadic cancers

Journal of Obstetrics and Gynaecology Research

Volumn 37, Issue 2, 2011, Pages 85-98

  Koi, Minoru ^a,b   Boland, Clement R ^a,b  

^a BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^b BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; HYPOXIA INDUCIBLE FACTOR 1; MAMMALIAN TARGET OF RAPAMYCIN; NIBRIN;

ARTICLE; CANCER GENETICS; CARCINOGENESIS; CELL HYPOXIA; CELLULAR IMMUNITY; CHROMOSOME ABERRATION; DNA REPAIR; DNA SEQUENCE; EXCISION REPAIR; GENE MUTATION; GENOME; HUMAN; MISMATCH REPAIR; NONHUMAN; OXIDATIVE STRESS; SISTER CHROMATID EXCHANGE; TETRAPLOIDY; TISSUE OXYGENATION; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOMAL INSTABILITY; DNA REPAIR; DNA, NEOPLASM; GENE EXPRESSION; GENOMIC INSTABILITY; HUMANS; NEOPLASMS; OXIDATIVE STRESS; RADIATION ONCOLOGY; TOR SERINE-THREONINE KINASES;

EID: 79955971818     PISSN: 13418076     EISSN: 14470756     Source Type: Journal    
DOI: 10.1111/j.1447-0756.2010.01377.x     Document Type: Article

References (111)

1. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004; 10: 789-799. (Pubitemid 39070849)
2. Hanahan D, Weinberg RA. The Hallmarks of Cancer. Cell 2000; 100: 57-70. (Pubitemid 30046295)
3. Stratton MR, Campbell PJ, Futreal PA. The Cancer Genome. Nature 2009; 458: 719-724.
4. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 1991; 51: 3075-3079.
5. Loeb LA, Loeb KR, Anderson JP. Multiple mutations and cancer. Proc Natl Acad Sci USA 2003; 100: 776-781. (Pubitemid 36183906)
6. Rajagopalan H, Nowak MA, Vogelstein B, Lengauer C. The significance of unstable chromosomes in colorectal cancer. Nat Rev Cancer 2003; 3: 695-699.
7. Sieber OM, Heinimann K, Tomlinson IP. Genomic instability - the engine of tumorigenesis? Nat Rev Cancer 2003; 3: 701-708. (Pubitemid 37328825)
8. Moulder JE, Rockwell S. Tumor hypoxia: Its impact on cancer therapy. Cancer Metastasis Rev 1987; 5: 313-341.
9. Hockel M, Vaupel P. Tumor hypoxia: Definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 2001; 93: 266-276. (Pubitemid 32219813)
10. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment. Cancer Res 1996; 56: 5754-5757. (Pubitemid 26422184)
11. Bindra RS, Crosby ME, Glazer PM. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev 2007; 26:249-260. (Pubitemid 47101664)
12. Huang LE, Bindra RS, Glazer PM, Harris AL. Hypoxia-induced genetic instability -a calculated mechanism underlying tumor progression. J Mol Med 2007; 85: 139-148. (Pubitemid 46188219)
13. Mottram JC. A factor of importance in the radio sensitivity of tumours. Br J Radiol 1936; 9: 606-614.
14. Thomlinson RH, Gray LH. The histological structure of some human lung cancers and the possible implications for radio-therapy. Br J Cancer 1955; 9: 539-549.
15. Gatenby RA, Kessler HB, Rosenblum JS et al. Oxygen distribution in squamous cell carcinoma metastases and its relationship to outcome of radiation therapy. Int J Radiat Oncol Biol Phys 1988; 14: 831-838.
16. Vaupel P, Kelleher DK, Hockel M. Oxygenation status of malignant tumors: Pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 2001; 28: 29-35. (Pubitemid 32522235)
17. Hockel M, Schlenger K, Aral B, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996; 56:4509-4515. (Pubitemid 26330463)
18. Teicher BA, Holden SA, Al-Achi A, Herman TS. Classification of antineoplastic treatments by their differential toxicity toward putative oxygenated and hypoxic tumor subpopulations in Vivo in the FSaIIC murine fibrosarcoma. Cancer Res 1990; 50: 3339-3344. (Pubitemid 20190142)
19. Chaplin DJ, Durand RE, Olive PL. Acute hypoxia in tumors: Implications for modifiers of radiation effects. Int J Radiat Oncol Biol Phys 1986; 12: 1279-1282. (Pubitemid 16030598)
20. Bristow RG, Hill RP. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 2008; 8: 180-192.
21. 2 availability on human cancer. Nat Rev Cancer 2008; 8: 967-975.
22. 2 tension. Proc Natl Acad Sci USA 1995; 92: 5510-5514.
23. Jiang B-H, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 1996; 271: 17771-17778. (Pubitemid 26250751)
24. Forsythe JA, Jiang B-H, Iyer NV et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16: 4604-4613. (Pubitemid 26272112)
25. Semenza GL, Jiang B-H, Leung SW et al. Hypoxia response elements in the aldolase A, Enolase 1 and Lactate Dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 1996; 271: 32529-32537.
26. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005; 306: 1-13.
27. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 1998; 95: 7987-7992.
28. Maxwell PH, Wiesener MS, Chang GW et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271-275. (Pubitemid 29246458)
29. Ohh M, Park CW, Ivan M et al. Ubiquitination of hypoxia- inducible factor requires direct binding to the β-domain of the von Hippel-Lindau protein. Nat Cell Biol 2000; 2: 423-427.
30. 2-regulated prolyl hydroxylation. Science 2001; 292: 468-471.
31. 2 sensing. Science 2001; 292: 464-68. (Pubitemid 32335941)
32. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 2002; 16: 1466-1471. (Pubitemid 34686328)
33. 300/ CBP binding protein during transactivation by HIF-1. Genes Dev 1999; 13: 64-75. (Pubitemid 29045116)
34. Webb JD, Coleman ML, Pugh CW. Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell Mol Life Sci 2009; 66: 3539-3554.
35. Foster KG, Fingar DC. mTOR: Conducting the cellular signaling symphony. J Biol Chem 2010; 285: 14071-14077.
36. Wouters BG, Koritzinsky M. Hypoxia signaling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008; 8: 851-864.
37. Brugarolas J, Lei K, Hurley RL et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/ TSC2 tumor suppressor complex. Genes Dev 2004; 18: 2893-2904. (Pubitemid 39602308)
38. Sofer A, Lei K, Johannessen CM, Ellisen LW. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol 2005; 25: 5834-5845. (Pubitemid 40946541)
39. DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW. Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev 2008; 22: 239-251.
40. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell 2006; 21: 521-531. (Pubitemid 43228007)
41. 3 mediates the hypoxia- induced inhibition on mammalian target of rapamycin by interacting with Rheb. J Biol Chem 2007; 282: 35803-35813. (Pubitemid 350277153)
42. Bernardi R, Guernah I, Jin D et al. PML inhibits HIF-1α translation and neoangiogenesis through repression of mTOR. Nature 2006; 442: 779-785. (Pubitemid 44258904)
43. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529. (Pubitemid 46985379)
44. Li C, Jackson RM. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002; 282: C227-C241. (Pubitemid 34663181)
45. 53 cell selection and tumour progression. Bull Math Biol 1999; 61: 759-778. (Pubitemid 29354973)
46. Sekiguchi M, Tsuzuki T. Oxidative nucleotide damage: Consequences and prevention. Oncogene 2002; 21: 8895-8904. (Pubitemid 36110820)
47. Ito A, Koshikawa N, Mochizuki S, Omura K, Takenaga K. Hypoxia-inducible factor-1 mediates the expression of DNA polymerase l in human tumor cells. Biochem Biophys Res Commun 2006; 351: 306-311. (Pubitemid 44740417)
48. Greenman C, Stephens P, Smith R et al. Patterns of somatic mutation in human cancer genomes. Nature 2007; 446: 153-158. (Pubitemid 46398669)
49. Zienolddiny S, Ryberg D, Haugen A. Induction of microsatellite mutations by oxidative agents in human lung cancer cell lines. Carcinogenesis 2000; 121: 1521-1526. (Pubitemid 30601643)
50. Gasche C, Chang CL, Rhees J, Goel A, Boland CR. Oxidative stress increases frameshift mutations in human colorectal cancer cells. Cancer Res 2001; 61: 7444-7448. (Pubitemid 32995032)
51. Yamada NA, Parker JM, Farber RA. Mutation frequency analysis of mononucleotide and dinucleotide repeats after oxidative stress. Environ Mol Mutagen 2003; 42: 75-84. (Pubitemid 37087469)
52. Chang CL, Marra G, Chauhan DP et al. Oxidative stress inactivates the human DNA mismatch repair system. Am J Physiol Cell Physiol 2002; 283: C148-C154. (Pubitemid 34670558)
53. Bencokova Z, Kaufmann MR, Pires IM, Lecane PS, Hammond EM. ATM activation and signaling under hypoxic conditions. Mol Cell Biol 2009; 29: 526-537.
54. Pires IM, Bencokova Z, Milani M et al. Effects of acute versus chronic hypoxia on DNA damage responses and genomic instability. Cancer Res 2010; 70: 925-935.
55. Hammond EM, Dorie MJ, Giaccia AJ. ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J Biol Chem 2003; 278: 12207-12213. (Pubitemid 36800201)
56. Freiberg RA, Hammond EM, Dorie MJ, Welford SM, Giaccia AJ. DNA damage during reoxygenation elicits a Chk2- dependent checkpoint response. Mol Cell Biol 2006; 26: 1598-1609.
57. Langauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997; 386: 623-627. (Pubitemid 27175430)
58. Schvartzman J-M, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: Mouse modeling of the human disease. Nat Rev Cancer 2010; 10: 102-113.
59. Aguilera A, Gomez-Gonzalez B. Genome instability: A mechanistic view of its causes and consequences. Nat Rev Genet 2008; 9: 204-217. (Pubitemid 351271797)
60. Umar A, Kunkel TA. DNA-replication fidelity, mismatch repair and genome instability in cancer cells. Eur J Biochem 1996; 238: 297-307. (Pubitemid 26188243)
61. Boland CR, Thibodeau SN, Hamilton SR et al. A National Cancer Institute workshop on microsatellite instability for cancer detection and familial predisposition: Development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 1998; 58: 5248-5257. (Pubitemid 28521189)
62. Bielas JH, Loeb KR, Rubin BP, True LD, Loeb LA. Human cancers express a mutator phenotype. Proc Natl Acad Sci USA 2006; 103: 18238-18242. (Pubitemid 44871642)
63. 21 cooperate to suppress aneuploidy and subsequent tumor development. Cancer Res 2005; 65: 8747-8753. (Pubitemid 41377363)
64. Chester N, Babbe H, Pinkas J, Manning C, Leder P. Mutation of the murine bloom's syndrome gene produces global genome destabilization. Mol Cell Biol 2006; 26: 6713-6726. (Pubitemid 44277905)
65. Taniguchi T, D'Andrea AD. Molecular pathogenesis of Fanconi anemia: Recent progress. Blood 2006; 107:4223-1233.
66. Shimada M, Sagae R, Kobayashi J, Habu T, Komatsu K. Inactivation of the Nijmegen breakage syndrome gene leads to excess centrosome duplication via the ATR/BRCA1 pathway. Cancer Res 2009; 69: 1768-1775.
67. Walsh T, King MC. Ten genes for inherited breast cancer. Cancer Cell 2007; 11: 103-105. (Pubitemid 46209856)
68. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability - an evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010; 11: 220-228.
69. Thompson ME, Jensen RA, Obermiller PS, Page DL, Holt JT. Decreased expression of BRCA1 accelerates growth and is often present during sporadic breast cancer progression. Nat Genet 1995; 9: 444-450.
70. Bieche I, Nogues C, Lidereau R. Overexpression of BRCA2 gene in sporadic breast tumours. Oncogene 1999; 18: 5232-5238. (Pubitemid 29460659)
71. Wreesmann VB, Estilo C, Eisele DW, Singh B, Wang SJ. Downregulation of Fanconi anemia genes in sporadic head and neck squamous cell carcinoma. J Otorhinolaryngol Relat Spec 2007; 69: 218-225. (Pubitemid 46934196)
72. Rice GC, Spiro IJ, Ling CC. Detection of S-phase overrepli- cation following chronic hypoxia using a monoclonal anti-BrdUrd. Int J Radiat Oncol Biol Phys 1985; 11: 1817-1822. (Pubitemid 16224021)
73. Rice GC, Hoy C, Schimke RT. Transient hypoxia enhances the frequency of dihydrofolate reductase gene amplification in Chinese hamster ovary cells. Proc Natl Acad Sci USA 1986; 83: 5978-5982. (Pubitemid 16000637)
74. 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: 9533-9537. (Pubitemid 19027161)
75. 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: 259-265. (Pubitemid 128373652)
76. Sutherland G. Fragile sites on human chromosomes: Demonstration of their dependence on the type of tissue culture medium. Science 1977; 197: 265-266. (Pubitemid 8130438)
77. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet 2007; 41: 169-192.
78. Ciullo M, Debily M-A, RAozier L et al. Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: The model of PIP gene duplication from a break at FRA7I. Hum Mol Genet 2002; 11: 2887-2894.
79. Rofstad EK, Johnsen NM, Lyng H. Hypoxia-induced tetraploidisation of a diploid human melanoma cell line in vitro. Br J Cancer Suppl 1996; 27: S136-S139. (Pubitemid 26237947)
80. Yih L-H, Lee T-C. Induction of C-anaphase and diplochro- mosome through dysregulation of spindle assembly checkpoint by sodium arsenite in human fibroblasts. Cancer Res 2003; 63: 6680-6688. (Pubitemid 37322947)
81. Lee J-H, Choi I-J, Song D-K. Genetic instability in the human lymphocyte exposed to hypoxia. Cancer Genet Cytogenet 2010; 196: 83-88.
82. Keysar SB, Trncic N, LaRue SM, Fox MH. Hypoxia/reoxygenation-induced mutations in mammalian cells detected by the flow cytometry mutation assay and characterized by mutant spectrum. Radiat Res 2010; 173: 21-26.
83. Papp-Szabo E, Josephy PD, Coomber BL. Microenvironmental influences on mutagenesis in mammary epithelial cells. Int J Cancer 2005; 116: 679-685. (Pubitemid 41099698)
84. Maynard S, Schuman HS, Harboe C, de Souza-Pinto NC, Bohr VA. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2009; 30: 2-10.
85. Mihaylova VT, Bindra RS, Yuan J et al. Decreased expression of the DNA mismatch Repair Gene Mlh1 under Hypoxic Stress in Mammalian Cells. Mol Cell Biol 2003; 23: 3265-3273. (Pubitemid 36459239)
86. Koshiji M, To KK, Hammer S et al. HIF-1α induces genetic instability by transcriptionally downregulating MutSα expression. Mol Cell 2005; 17: 793-803. (Pubitemid 40386941)
87. Rodriguez-Jimenez FJ, Moreno-Manzano V, Lucas-Dominguez R, Sanchez-Puelles JM. Hypoxia causes down- regulation of mismatch repair system and genomic instability in stem cells. Stem Cells 2008; 26: 2052-2062.
88. Francia G, Green SK, Bocci G 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: 1484-1494. (Pubitemid 41556430)
89. Nakamura H, Tanimoto K, Hiyama K et al. Human mismatch repair gene, MLH1, is transcriptionally repressed by the hypoxia-inducible transcription factors, DEC1 and DEC2. Oncogene 2008; 27: 4200-4209. (Pubitemid 351969910)
90. Shahrzad S, Quayle L, Stone C et al. Ischemia-induced K-ras mutations in human colorectal cancer cells: Role of microen- vironmental regulation of MSH2 expression. Cancer Res 2005; 65: 8134-8141. (Pubitemid 41330576)
91. Moynahan ME, Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 2010; 11: 196-207.
92. Bunting SF, Callen E, Wong N et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141: 243-254.
93. Bindra RS, Schaffer PJ, Meng A et al. Down-regulation of RAd51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 2004; 24: 8504-8518. (Pubitemid 39245072)
94. Bindra RS, Gibson SL, Meng A et al. Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 2005; 65: 11597-11604. (Pubitemid 41821719)
95. Bindra RS, Glazer PM. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene 2007; 26: 2048-2057. (Pubitemid 46514738)
96. Meng AX, Jalali F, Cuddihy A et al. Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother Oncol 2005; 76: 168-176. (Pubitemid 41725444)
97. Chan N, Koritzinsky M, Zhao H et al. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res 2008; 68: 605-612.
98. Crosby ME, Kulshreshtha R, Ivan M et al. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 2009; 69: 1221-1229.
99. 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: 4372-4376. (Pubitemid 32103614)
100. Dantuma NP, Heinen C, Hoogstraten D. The ubiquitin receptor Rad23: At the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair 2009; 8: 449-460.
101. Boland CR, Koi M, Chang DK, Carethers JM. The biochemical basis of microsatellite instability and abnormal immunohistochemistry and clinical behavior in Lynch Syndrome: From bench to bedside. Fam Cancer 2008; 7: 41-52.
102. 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; 262: 93-103. (Pubitemid 46734558)
103. Haugen A, Goel A, Yamada K et al. Genetic instability caused by loss of MutS homologue 3 in human colorectal cancer. Cancer Res 2008; 68: 8465-8472.
104. Klein A, Flugel D, Kietzmann T. Transcriptional regulation of serine/threonine kinase-15 (STK15) expression by hopoxia and HIF-1. Mol Biol Cell 2008; 19: 3667-3675.
105. McDonald JP, Tissier A, Frank EG, Iwai S, Hanaoka F, Woodgate R. DNA polymerase iota and related Rad30-like enzymes. Philos Trans R Soc Lond B Biol Sci 2001; 356:53-60. (Pubitemid 32575588)
106. Zhang Y, Yuan F, Wu X, Taylor JS, Wang Z. Response of human DNA polymerase i to DNA lesions. Nucleic Acids Res 2001; 29: 928-935. (Pubitemid 32162261)
107. Budzowska M, Kanaar R. Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem Biophys 2009; 53: 17-31.
108. Yang J,' Chen Z,' Liu Y,' Hickey RJ,' Malkas LH. Altered DNA polymerase l expression in breast cancer cells leads to a reduction in DNA replication fidelity and a higher rate of mutagenesis. Cancer Res 2004; 64: 5597-5607. (Pubitemid 39095555)
109. To KK, Sedelnikova OA, Samons M, Bonner WM, Huang LE. The phosphorylation status of PAS-B distinguishes HIF-1α from HIF-2α in NBS1 repression. EMBO J 2006; 25: 4784-4794. (Pubitemid 44607024)
110. Pleasance ED, Cheetham RK, Stephens PJ, et al.Acomprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010; 463: 191-197.
111. Galluzzo M, Pennacchietti S, Rosano S, Comoglio PM, Michieli P. Prevention of hypoxia by myoglobin expression in human tumor cells promotes differentiation and inhibits metastasis. J Clin Invest 2009; 119: 865-875.