Impaired DNA double-strand break repair contributes to chemoresistance in HIF-1α-deficient mouse embryonic fibroblasts

Carcinogenesis

Volumn 29, Issue 12, 2008, Pages 2306-2316

  Wirthner, Renato ^a   Wrann, Simon ^a   Balamurugan, Kuppusamy ^a   Wenger, Roland H ^a   Stiehl, Daniel P ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; ETOPOSIDE; HISTONE H2AX; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEIN P53;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; ELECTROPHORESIS; EMBRYONIC FIBROBLAST; FIBROBLAST; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; COMET ASSAY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; EMBRYO, MAMMALIAN; ETOPOSIDE; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; RNA INTERFERENCE; RNA, MESSENGER; TRANSFECTION;

EID: 57349157684     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgn231     Document Type: Article

References (62)

1. Brown,J.M. et al. (1998) The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res., 58, 1408-1416.
2. Brown,J.M. et al. (2004) Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer, 4, 437-447.
3. Pouysségur,J. et al. (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature, 441, 437-443.
4. 2-regulated gene expression. FASEB J., 16, 1151-1162.
5. Schofield,C.J. et al. (2004) Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol., 5, 343-354.
6. Wenger,R.H. et al. (2005) Integration of oxygen signaling at the consensus HRE. Sci. STKE, 2005, re12.
7. Seagroves,T.N. et al. (2001) Transcription factor HIF-1 is a necessary mediator of the Pasteur effect in mammalian cells. Mol. Cell. Biol., 21, 3436-3444.
8. Svastova,E. et al. (2004) Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett., 577, 439-445.
9. Minchenko,A. et al. (2002) Hypoxia-inducible factor-1 (HIF-1) mediated expression of the 6-phosphofructo-2-kinase/ fructose-2,6-bisphosphatase-3 (PFKBF3) gene: Its possible role in the Warburg effect. J. Biol. Chem., 277, 6183-6187.
10. Schroeder,T. et al. (2005) Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res., 65, 5163-5171.
11. Ryan,H.E. et al. (1998) HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J., 17, 3005-3015.
12. Ryan,H.E. et al. (2000) Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res., 60, 4010-4015.
13. Krieg,M. et al. (2000) Up-regulation of hypoxia-inducible factors HIF-1α and HIF-2α under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function. Oncogene 19, 5435-5443.
14. Zundel,W. et al. (2000) Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev., 14, 391-396.
15. Ravi,P. et al. (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev. 14, 34-44.
16. Jiang,B.H. et al. (1997) V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: Involvement of HIF-1 in tumor progression. Cancer Res., 57, 5328-5335.
17. Zhong,H. et al. (1999) Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res., 59, 5830-5835.
18. Birner,P. et al. (2000) Overexpression of hypoxia-inducible factor 1α is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res., 60, 4693-4696.
19. Aebersold,D.M. et al. (2001) Expression of hypoxia-inducible factor-1α: A novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res., 61, 2911-2916.
20. Koukourakis,M.I. et al. (2002) Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer. Int. J. Radiat. Oncol. Biol. Phys., 53 1192-1202.
21. Bachtiary,B. et al. (2003) Overexpression of hypoxia-inducible factor 1α indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clin. Cancer Res., 9, 2234-2240.
22. Generali,D. et al. (2006) Hypoxia-inducible factor-1α expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin. Cancer Res., 12, 4562-4568.
23. Comerford,K.M. et al. (2002) Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res., 62, 3387-3394.
24. Wartenberg,M. et al. (2003) Regulation of the multidrug resistance transporter P-glycoprotein in multicellular tumor spheroids by hypoxia-inducible factor (HIF-1) and reactive oxygen species. FASEB J., 17, 503-505.
25. Erler,J.T. et al. (2004) Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol. Cell. Biol., 24, 2875-2889.
26. Sermeus,A. et al. (2008) Hypoxia induces protection against etoposide-induced apoptosis: Molecular profiling of changes in gene expression and transcription factor activity. Mol. Cancer, 7 27.
27. Wenger,R.H. et al. (1998) Up-regulation of hypoxia-inducible factor-1α is not sufficient for hypoxic/anoxic p53 induction. Cancer Res., 58, 5678-5680.
28. Moeller,B.J. et al. (2006) HIF-1 and tumour radiosensitivity. Br. J. Cancer, 95, 1-5.
29. Unruh,A. et al. (2003) The hypoxia-inducible factor-1α is a negative factor for tumor therapy. Oncogene, 22, 3213-3220.
30. Zhang,X. et al. (2004) Enhancement of hypoxia-induced tumor cell death in vitro and radiation therapy in vivo by use of small interfering RNA targeted to hypoxia-inducible factor-1α. Cancer Res. 64, 8139-8142.
31. Williams,K.J. et al. (2005) Enhanced response to radiotherapy in tumours deficient in the function of hypoxia-inducible factor-1. Radiother. Oncol., 75, 89-98.
32. Moeller,B.J. et al. (2005) Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell, 8, 99-110.
33. Brown,L.M. et al. (2006) Reversing hypoxic cell chemoresistance in vitro using genetic and small molecule approaches targeting hypoxia inducible factor-1. Mol. Pharmacol., 69, 411-418.
34. Song,X. et al. (2006) Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1α gene. Cancer Chemother. Pharmacol., 58, 108-111.
35. Li,J. et al. (2006) Knockdown of hypoxia-inducible factor-1α in breast carcinoma MCF-7 cells results in reduced tumor growth and increased sensitivity to methotrexate. Biochem Biophys. Res. Commun. 342, 1341-1351.
36. Sasabe,E. et al. (2007) The involvement of hypoxia-inducible factor-1α in the susceptibility to gamma-rays and chemotherapeutic drugs of oral squamous cell carcinoma cells. Int. J. Cancer, 120, 268-277.
37. Li,L. et al. (2006) Hypoxia-inducible factor-1 inhibition in combination with temozolomide treatment exhibits robust antitumor efficacy in vivo. Clin. Cancer Res., 12, 4747-4754.
38. Martinive,P. et al. (2006) Preconditioning of the tumor vasculature and tumor cells by intermittent hypoxia: Implications for anticancer therapies. Cancer Res., 66, 11736-11744.
39. Ji,Z. et al. (2006) Induction of hypoxia-inducible factor-1α overexpression by cobalt chloride enhances cellular resistance to photodynamic therapy. Cancer Lett., 244, 182-189.
40. Feldser,D. et al. (1999) Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res., 59, 3915-3918.
41. Stiehl,D.P. et al. (2006) Increased prolyl 4-hydroxylase domain proteins compensate for decreased oxygen levels. Evidence for an autoregulatory oxygen-sensing system. J. Biol. Chem., 281, 23482-23491.
42. Singh,N.P. et al. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res., 175, 184-191.
43. Wanner,R.M. et al. (2000) Epolones induce erythropoietin expression via hypoxia-inducible factor-1α activation. Blood, 96, 1558-1565.
44. Burden,D.A. et al. (1998) Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim. Biophys. Acta, 1400, 139-154.
45. Carrière,A. et al. (2004) Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: A mechanism for hypoxia-dependent effect. J. Biol. Chem., 279, 40462-40469.
46. Connelly,M.A. et al. (1998) The promoters for human DNA-PKcs (PRKDC) and MCM4: Divergently transcribed genes located at chromosome 8 band q11. Genomics, 47, 71-83.
47. Saito,T. et al. (1998) Mouse cdc21 only 0.5 kb upstream from DNA-PKcs in a head-to-head organization: An implication of co-evolution of ATM family members and cell cycle regulating genes. Mamm. Genome 9, 769-772.
48. Jin,S. et al. (1998) Differential etoposide sensitivity of cells deficient in the Ku and DNA-PKcs components of the DNA-dependent protein kinase. Carcinogenesis, 19, 965-971.
49. Errami,A. et al. (1996) Ku86 defines the genetic defect and restores X-ray resistance and V(D)J recombination to complementation group 5 hamster cell mutants. Mol. Cell. Biol., 16, 1519-1526.
50. Singleton,B,K. et al. (1997) Molecular and biochemical characterization of xrs mutants defective in Ku80. Mol. Cell. Biol. 17, 1264-1273.
51. Lees-Miller,S.P. et al. (1995) Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science, 267, 1183-1185.
52. Zhao,Y. et al. (2006) Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res., 66 5354-5362.
53. Xu,W. et al. (2000) Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell Biol., 2, 339-345.
54. Um,J.H. et al. (2004) Association of DNA-dependent protein kinase with hypoxia inducible factor-1 and its implication in resistance to anticancer drugs in hypoxic tumor cells. Exp. Mol. Med., 36, 233-242.
55. Ginis,I. et al. (2000) Hypoxia affects tumor cell invasiveness in vitro: The role of hypoxia-activated ligand HAL1/13 (Ku86 autoantigen). Cancer Lett., 154, 163-174.
56. Lynch,E.M. et al. (2001) Hypoxia-activated ligand HAL-1/13 is lupus autoantigen Ku80 and mediates lymphoid cell adhesion in vitro. Am. J. Physiol. Cell Physiol., 280, C897-C911.
57. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev., 12, 149-162.
58. Welford,S.M. et al. (2006) HIF1α delays premature senescence through the activation of MIF. Genes Dev., 20, 3366-3371.
59. Le Bras,A. et al. (2007) HIF-2α specifically activates the VE-cadherin promoter independently of hypoxia and in synergy with Ets-1 through two essential ETS-binding sites. Oncogene, 26, 7480-7489.
60. Zeng,L. et al. (2007) Hypoxia inducible factor-1 influences sensitivity to paclitaxel of human lung cancer cell lines under normoxic conditions. Cancer Sci., 98, 1394-1401.
61. Dominguez-Sola,D. et al. (2007) Non-transcriptional control of DNA replication by c-Myc. Nature, 448, 445-451.
62. Huang,L.E. et al. (2007) Hypoxia-induced genetic instability - a calculated mechanism underlying tumor progression. J. Mol. Med., 85, 139-148.