DNA Damage Is a Prerequisite for p53-Mediated Proteasomal Degradation of HIF-1α in Hypoxic Cells and Downregulation of the Hypoxia Marker Carbonic Anhydrase IX

REFERENCES

• Achison, M., and Hupp T. R.. 2003. Hypoxia attenuates the p53 response to cellular damage. Oncogene 22:3431–3440.
   PubMed Web of Science ®Google Scholar
• Agani, F., Kirsch D. G., Friedman S. L., Kastan M. B., and Semenza G. L.. 1997. p53 does not repress hypoxia-induced transcription of the vascular endothelial growth factor gene. Cancer Res. 57:4474–4477.
   PubMedGoogle Scholar
• Airley, R. E., Loncaster J., Raleigh J. A., Harris A. L., Davidson S. E., Hunter R. D., West C. M. L., and Stratford I. J.. 2003. Glut-1 and CAIX as intrinsic markers of hypoxia in carcinoma of the cervix: relationship to pimonidazole binding. Int. J. Cancer 104:85–91.
   PubMed Web of Science ®Google Scholar
• Arany, Z., Huang L. E., Eckner R., Bhattacharya S., Jiang C., Goldberg M. A., Bunn H. F., and Livingston D. M.. 1996. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. USA 93:12969–12973.
   PubMed Web of Science ®Google Scholar
• Ashcroft, M., Taya Y., and Vousden K. H.. 2000. Stress signals utilize multiple pathways to stabilize p53. Mol. Cell. Biol. 20:3224–3233.
   PubMed Web of Science ®Google Scholar
• Bai, J., and Cederbaum A. I.. 2003. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents by accelerating the degradation of p53. J. Biol. Chem. 278:4660–4667.
   PubMed Web of Science ®Google Scholar
• Blagosklonny, M. V., An W. G., Romanova L. Y., Trepel J., Fojo T., and Neckers L.. 1998. p53 inhibits hypoxia-inducible factor-stimulated transcription. J. Biol. Chem. 273:1995–11998.
   Google Scholar
• Brown, J. M., and Giaccia A. J.. 1998. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 58:1408–1416.
   PubMed Web of Science ®Google Scholar
• Bui, M. H. T., Seligson D., Han K., Pantuck A. J., Dorey F. J., Huang Y., Horvath S., Leibovich B. C., Chopra S., Liao S.-Y., Stanbridge E., Lerman M. I., Palotie A., Figlin R. A., and Belldegrun A. S.. 2003. Carbonic anhydrase IX is an independent predictor of survival in advanced renal clear cell carcinoma: implications for prognosis and therapy. Clin. Cancer Res. 9:802–811.
   PubMed Web of Science ®Google Scholar
• Bunz, F., Dutriaux A., Lengauer C., Waldman T., Zhou S., Brown J. P., Sedivy J. M., Kinzler K. W., and Vogelstein B.. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science (Washington, D.C.) 282:1497–1501.
   PubMed Web of Science ®Google Scholar
• Chen, X., Ko L. J., Jayaraman L., and Prives C.. 1996. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 10:2438–2451.
   PubMed Web of Science ®Google Scholar
• Chen, D., Li M., Luo J., and Gu W.. 2003. Direct interactions between HIF-1α and mdm2 modulate p53 function. J. Biol. Chem. 278:13595–13598.
   PubMed Web of Science ®Google Scholar
• Divgi, C. R., Bander N. H., Scott A. M., O'Donoghue J. A., Sgouros G., Welt S., Finn R. D., Morrissey F., Capitelli P., Williams J. M., Deland D., Nakhre A., Oosterwijk E., Gulec S., Graham M. C., Larson S. M., and Old L. J.. 1998. Phase I/II radioimmunotherapy trial with iodine-131-labeled monoclonal antibody G250 in metastatic renal carcinoma. Clin. Cancer Res. 4:2729–2739.
   PubMed Web of Science ®Google Scholar
• Giaccia, A. J., and Kastan M. B.. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12:2973–2983.
   PubMed Web of Science ®Google Scholar
• Giatromanolaki, A., Koukourakis M. I., Sivridis E., Pastorek J., Wykoff C. C., Gatter K. C., and Harris A. L.. 2001. Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in non-small cell lung cancer. Cancer Res. 61:7992–7998.
   PubMed Web of Science ®Google Scholar
• Girnita, L., Girnita A., and Larsson O.. 2003. Mdm2-dependent ubiquitination and degradation of the insulin-like growth factor 1 receptor. Proc. Natl. Acad. Sci. USA 100:8247–8252.
   PubMed Web of Science ®Google Scholar
• Graeber, T. G., Osmanian C., Jacks T., Housman D. E., Koch C. J., Lowe S. W., and Giaccia A. J.. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumors. Nature 379:88–91.
   PubMed Web of Science ®Google Scholar
• Hammond, E. M., Denko N. C., Dorie M. J., Abraham R. T., and Giaccia A. J.. 2002. Hypoxia links ATR and p53 through replication arrest. Mol. Cell. Biol. 22:1834–1843.
   PubMed Web of Science ®Google Scholar
• Harris, A. L. 2002. Hypoxia-a key regulatory factor in tumor growth. Nat. Rev. Cancer 2:38–47.
   PubMed Web of Science ®Google Scholar
• Hollstein, M., Sidransky D., Vogelstein B., and Harris C. C.. 1991. p53 mutations in human cancers. Science 253:49–53.
   PubMed Web of Science ®Google Scholar
• Isaacs, J. S., Jung Y.-J., Mimnaugh E. G., Martinez A., Cuttita F., and Neckers L. M.. 2002. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J. Biol. Chem. 277:29936–29944.
   PubMed Web of Science ®Google Scholar
• Ivan, M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J. M., Lane W. S., and Kaelin W. G.. 2001. HIF α targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464–468.
   PubMed Web of Science ®Google Scholar
• Ivanov, S., S.-Y., Liao, Ivanova A., Danilkovitch-Miagkova A., Tarasova N., Weirich G., Merril M. J., Proescholdt M. A., Oldfield E. H., Lee J., Závada J., Waheed A., Sly W., Lerman M. I., and Stanbridge E. J.. 2001. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 158:905–919.
   PubMed Web of Science ®Google Scholar
• Ivanov, S. V., Kuzmin I., Wei M.-H., Pack S., Geil L., Johnson B. E., Stanbridge E. J., and Lerman M. I.. 1998. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc. Natl. Acad. Sci. USA 95:12596–12601.
   PubMed Web of Science ®Google Scholar
• Jaakkola, P., Mole D. R., Tian Y.-M., Wilson M. I., Gielbert J., Gaskell S. J., von Kriegsheim A., Hebestreit H. F., Mukherji M., Schofield C. J., Maxwell P. H., Pugh C. W., and Ratcliffe P. J.. 2001. Targeting of HIF α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468–472.
   PubMed Web of Science ®Google Scholar
• Jongmans, W., van den Oudenalder K., Tiemessen D. M., Molkenboer J., Willemsen R., Mulders P. F. A., and Oosterwijk E.. 2003. Targeting of adenovirus to human renal cell carcinoma cells. Urology 62:559–565.
   PubMed Web of Science ®Google Scholar
• Kaluz, S., Kaluzová M., Opavský R., Pastoreková S., Gibadulinová A., Dequiedt F., Kettmann R., and Pastorek J.. 1999. Transcriptional regulation of the MN/CA 9 gene coding for the tumor-associated carbonic anhydrase IX. Identification and characterization of a proximal silencer element. J. Biol. Chem. 274:32588–32595.
   PubMedGoogle Scholar
• Kaluz, S., Kaluzová M., Chrastina A., Olive P. L., Pastoreková S., Pastorek J., Lerman M. I., and Stanbridge E. J.. 2002. Lowered oxygen tension induces expression of the hypoxia marker MN/carbonic anhydrase IX in the absence of hypoxia-inducible factor 1α stabilization: a role for phosphatidylinositol 3′-kinase. Cancer Res. 62:4469–4477.
   PubMed Web of Science ®Google Scholar
• Kaluz, S., Kaluzová M., and Stanbridge E. J.. 2003. Expression of the hypoxia marker carbonic anhydrase IX is critically dependent on SP1 activity. Identification of a novel type of hypoxia-responsive enhancer. Cancer Res. 63:917–922.
   PubMed Web of Science ®Google Scholar
• Kaluzová, M., Pastoreková S., Pastorek J., and Kaluz S.. 2000. P53 tumour suppressor modulates transcription of the TATA-less gene coding for the tumour-associated carbonic anhydrase MN/CAIX in MaTu cells. Biochim. Biophys. Acta 1491:20–26.
   PubMedGoogle Scholar
• Kaluzová, M., Pastoreková S., Svastová E., Pastorek J., Stanbridge E. J., and Kaluz S.. 2001. Characterization of the MN/CA 9 promoter proximal region-a role for SP and AP1 factors. Biochem. J. 359:669–677.
   PubMedGoogle Scholar
• Kern, S. E., Pietenpol J. A., Thiagalingam S., Seymour A., Kinzler K. W., Vogelstein B.. 1992. Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256:827–830.
   PubMed Web of Science ®Google Scholar
• Koumenis, C., Alarcon R., Hammond E., Suthpin P., Hoffman W., Murphy M., Derr J., Taya Y., Lowe S. W., Kastan M., and Giaccia A. J.. 2001. Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol. Cell. Biol. 21:1297–1310.
   PubMed Web of Science ®Google Scholar
• Kubbutat, M. H., Jones S. N., and Vousden K. H.. 1997. Regulation of p53 stability by Mdm2. Nature 387:299–303.
   PubMed Web of Science ®Google Scholar
• Lieskovská, J., Kaluzová M., Opavský R., Kaluz S., Pastorek J., Kettmann R., and Pastoreková S.. 1998. Up-regulation of p53 by antisense expression of HPV 18 E6 oncogene does not influence the level of MN/CA IX tumor-associated protein in HeLa cervical carcinoma cells. Int. J. Oncol. 13:1081–1086.
   PubMedGoogle Scholar
• Loncaster, J. A., Harris A. L., Davidson S. E., Logue J. P., Hunter R. D., Wykoff C. C., Pastorek J., Ratcliffe P. J., Stratford I. J., and West C. M. L.. 2001. Carbonic anhydrase (CAIX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 61:6394–6399.
   PubMed Web of Science ®Google Scholar
• Maxwell, P. H., Wiesener M., Chang G-W., Clifford S., Vaux E., Cockman M., Wykoff C. C., Pugh C., Maher E., and Ratcliffe P. J.. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature (London) 399:271–275.
   PubMed Web of Science ®Google Scholar
• Pal, S., Datta K., and Mukhopadhyay D.. 2001. Central role of p53 on regulation of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) expression in mammary carcinoma. Cancer Res. 61:6952–6957.
   PubMed Web of Science ®Google Scholar
• Post, D. E., and van Meir E. G.. 2001. Generation of bi-directional hypoxia/HIF-responsive expression vectors to target gene expression to hypoxic cells. Gene Ther. 8:1801–1807.
   PubMedGoogle Scholar
• Ravi, R., Mookerjee B., Bhujwalla Z. M., Sutter C. H., Artemov D., Zeng Q., Dillehay L. E., Madan A., Semenza G. L., and Bedi A.. 2000. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev. 14:34–44.
   PubMed Web of Science ®Google Scholar
• Salnikow, K., Costa M., Figg W. D., and Blagosklonny M. V.. 2000. Hyperinducibility of hypoxia-responsive genes without p53/p21-dependent checkpoint in aggressive prostate cancer. Cancer Res. 60:5630–5634.
   PubMedGoogle Scholar
• Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nature Rev. Cancer. 3:721–732.
   PubMed Web of Science ®Google Scholar
• Sheta, E. A., Trout H., Gildea J. J., Harding M. A., and Theodorescu D.. 2001. Cell density mediated pericellular hypoxia leads to induction of HIF-1α via nitric oxide and Ras/MAP kinase mediated signaling pathways. Oncogene 20:7624–7634.
   PubMed Web of Science ®Google Scholar
• Stanbridge, E. J. 1981. Mycoplasma detection-an obligation to scientific accuracy. Isr. J. Med. Sci. 17:563–568.
   PubMedGoogle Scholar
• Thomlinson, R., and Gray L.. 1955. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer. 9:539–549.
   PubMed Web of Science ®Google Scholar
• Vogelstein, B., Lane D., and Levine A. J.. 2000. Surfing the p53 network. Nature 408:307–310.
   PubMed Web of Science ®Google Scholar
• Wang, G. L., Jiang B. H., Rue E. A., and Semenza G. L.. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92:5510–5514.
   PubMed Web of Science ®Google Scholar
• Wykoff, C. C., Beasley N. J., Watson P. H., Turner K. J., Pastorek J., Sibtain A., Wilson G. D., Turley H., Talks K. L., Maxwell P. H., Pugh C. W., Ratcliffe P. J., and Harris A. L.. 2000. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 60:7075–7083.
   PubMed Web of Science ®Google Scholar
• Wykoff, C. C., Beasley N. J., Watson P. H., Campo L., Chia S. K., English R., Pastorek J., Sly W. S., Ratcliffe P. J., and Harris A. L.. 2001. Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am. J. Pathol. 158:1011–1019.
   PubMed Web of Science ®Google Scholar
• Závada, J., Závadová Z., Pastoreková S., Ciampor F., Pastorek J., and Zelník V.. 1993. Expression of MaTu-MN protein in human tumor cultures and in clinical specimens. Int. J. Cancer. 54:268–274.
   PubMed Web of Science ®Google Scholar
• Zhang, L., Yu D., Hu M., Xiong S., Lang A., Ellis L. M., and Pollock R. E.. 2000. Wild-type p53 suppresses angiogenesis in human leiomyosarcoma and synovial sarcoma by transcriptional suppression of vascular endothelial growth factor expression. Cancer Res. 60:3655–3661.
   PubMed Web of Science ®Google Scholar
• Zietz, C., Rossle M., Haas C., Sendelhofert A., Hirschmann A., Sturzl M., and Lohrs U.. 1998. MDM-2 oncoprotein overexpression, p53 gene mutation, and VEGF up-regulation in angiosarcomas. Am. J. Pathol. 153:1425–1433.
   PubMed Web of Science ®Google Scholar