Cellular redox status regulates hypoxia inducible factor-1 activity. Role in tumour development

Journal of Experimental and Clinical Cancer Research

Volumn 26, Issue 1, 2007, Pages 39-50

  Martínez Sánchez, Gregorio ^a,c   Giuliani, A ^b  

^a UNIVERSITY OF HAVANA   (Cuba)

^b UNIVERSITY OF MILAN   (Italy)

^c NONE   (Cuba)

Author keywords

Antioxidants; Free radicals; HIF 1; Hypoxia inducible factor; Oxidative stress; Tumour hypoxia

Indexed keywords

APIGENIN; BERBERINE; CYCLOSPORIN; DACTINOMYCIN; ERYTHROPOIETIN; GENISTEIN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; INSULIN; PICROSIDE I; PSEUDOLARIC ACID A; PSEUDOLARIC ACID B; REACTIVE OXYGEN METABOLITE; RESVERATROL; ROTENONE; TOPOTECAN; TRICHOSTATIN A;

ANGIOGENESIS; ASTROCYTOMA; BRAIN TUMOR; BREAST CANCER; BREAST CARCINOMA; BREAST HYPERPLASIA; CANCER STAGING; CARCINOGENESIS; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; ERYTHROPOIESIS; GENE EXPRESSION; GLIOBLASTOMA; GLUCOSE METABOLISM; HUMAN; OLIGODENDROGLIOMA; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; TISSUE INJURY; TUMOR GROWTH;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL HYPOXIA; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MODELS, MOLECULAR; NEOPLASMS; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN; PROTEIN CONFORMATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 34247524169     PISSN: 03929078     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (82)

1. Kietzmann T., Dimova E.Y., Flugel D., Scharf J.G.: Oxygen: Modulator of Physiological and Pathophysiological Processes in the Liver. Z. Gastroenterol. 44: 67-76, 2006.
2. Semenza G.L.: Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. TRENDS Molec. Med. 7(8) August:345-350, 2001.
3. Welsh S.J., Koh M.Y., Powis G.: The hypoxic inducible stress response as a target for cancer drug discovery. Semin. Oncol. 33(4):486-97, 2006.
4. Sainson R.C., Harris A.L. Hypoxia-regulated differentiation: let's step it up a Notch. Trends Mol. Med. 12(4):141-3, 2006.
5. Subarsky P., Hill R.P.: The hypoxic tumour microenvironment and metastatic progression. Clin. Exp. Metastasis 20(3):237-250, 2003.
6. Brown J.M., Wilson W.R.: Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4(6):437-447, 2004.
7. Dale G.N., Yu-Dong Z.: Natural Product-Based Inhibitors of Hypoxia-Inducible Factor-1 (HIF-1). Curr. Drug Targets 7:355-369, 2006.
8. Graeber T.G., Osmanian C., Jacks T., et al.: Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379(6560):88-91, 1996.
9. Maxwell P.H., Pugh C.W., Ratcliffe P.J.: The pVHL-HIF-1 system. A key mediator of oxygen homeostasis. Adv. Exp. Med. Biol. 502:365-376, 2001.
10. Wenger R.H.: Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J 16:1151-1162, 2002.
11. Maxwell P.H., Ratcliffe P.J.: Oxygen sensors and angiogenesis. Semin. Cell Dev. Biol. 13:29-37, 2002.
12. Kung AL, Zabludoff SD, France DS, et al.: Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway. Cancer Cell. 6(1):33-43, 2004.
13. Ryan H.E., Poloni M., McNulty W., et al.: Hypoxia-inducible factor-1alpha is a positive factor in solid tumour growth. Cancer Res. 60:4010-4015, 2000.
14. Semenza G.L., Shimoda L.A., Prabhakar N.R.: Regulation of gene expression by HIF-1.Novartis Found Symp. 272:2-8, 2006.
15. Schumacker P.T.: Hypoxia-inducible factor-1 (HIF-1). Crit. Care Med. 33(12 Suppl):S423-5, 2005.
16. Acker H.: The oxygen sensing signal cascade under the influence of reactive oxygen species. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360(1464):2201-10, 2005.
17. Jiang H., Guo R., Powell-Coffman J.A.: The Caenorhabditis elegans HIF-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc. Natl. Acad. Sci. USA 98:7916-7921, 2001.
18. Chavez J.C., Baranova O., Lin J., Pichiule P.: The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci. 126(37):9471-81, 2006.
19. Hogenesch J.B., Gu Y.Z., Moran S.M., et al.: The basic helix-loop-helix-PAS protein MOP9 is a brain-specific heterodimeric partner of circadian and hypoxia factors. J. Neurosci. 20:RC83, 2000.
20. Pouyssegur J., Dayan F., Mazure N.M.: Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441(7092):437-43, 2006.
21. O'Rourke J.F., Tian Y.M., Ratcliffe P.J., Pugh C.W.: Oxygen-regulated and transactivating domains in endothelial PAS protein 1: comparison with hypoxia-inducible factor-1α. J. Biol. Chem. 274:2060-2071: 1999.
22. Lando D., Pongratz I., Poellinger L., Whitelaw M.L.: A redox mechanism controls differential DNA binding activities of hypoxia-inducible factor (HIF) 1α and the HIF-like factor. J. Biol. Chem. 275:4618-4627, 2000.
23. Talks K.L., Turley H., Gatter K.C., et al.: The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumourassociated macrophages. Am. J. Pathol. 157:411-421, 2000.
24. Wiesener M.S., Jurgensen J.S., Rosenberger C., et al.: Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J 17: 271-273, 2003.
25. Maynard M.A., Qi H., Chung J., et al.: Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J. Biol. Chem. 278:11032-11040, 2003.
26. Makino Y., Kanopka A., Wilson W.J., Tanaka H., Poellinger L.: Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxiainducible factor-3alpha locus. J. Biol. Chem. 277: 32405-32408, 2002.
27. Semenza G.L., Jiang B.H., Leung S.W., 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. 271:32529-32537, 1996.
28. Hammond E.M., Giaccia A.J.: Hypoxia-inducible factor-1 and p53: friends, acquaintances, or strangersa Clin. Cancer Res. 12(17):5007-9, 2006.
29. Zhang W., Tsuchiya T., Yasukochi Y.: Transitional change in interaction between HIF-1 and HNF-4 in response to hypoxia. J. Hum. Genet. 44:293-299, 1999.
30. Kietzmann T., Samoylenko A., Roth U., et al. Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibition-1 gene expression by insulin in primary rat hepatocytes. Blood 101:907-914, 2003.
31. Fukuda R., Hirota K., Fan F., Jung Y.D., Ellis L.M., Semenza G.L.: Insulin-like growth factor 1 induces hypoxia-inducible factor 1 mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 277: 38205-38211, 2002.
32. Gorlach A., Diebold I., Schini-Kerth V.B., et al.: Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ. Res. 89:47-54, 2001.
33. Richard D.E., Berra E., Pouyssegur J.: Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1 alpha in vascular smooth muscle cells. J. Biol. Chem. 275:26765-26771, 2000.
34. Stiehl D.P., Jelkmann W., Wenger R.H., et al.: Normoxic induction of the hypoxia-inducible factor 1 alpha by insulin and interlukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett. 512:157-162, 2002.
35. Hirota K., Fukuda R., Takabuchi S., et al.: Induction of hypoxia-inducible factor 1 activity by muscarinic acetylcholine receptor signaling. J. Biol. Chem. 279:41521-41528, 2004.
36. Yuan G., Naduri J., Bhasker C.R., et al.: Ca2+/calmodulin kinase-dependent activation of hypoxia inducible factor 1 transcritional activity in cells subjected to intermittent hypoxia. J. Biol. Chem. 280:4321-4328, 2005.
37. Gao N., Jiang B.H., Leonard S.S., et al.: p38 Signaling-mediated hypoxia-inducible factor by Cr(VI) in DU145 human prostate carcinoma cells. J. Biol. Chem. 277:45042-45048, 2002.
38. Duyndam M.C., Hulscher T.M., Fontijn D., et al.: Induction of vascular endothelial grown factor expression and hypoxia-inducible factor 1 alpha protein by the oxidative stress arsenite. J. Biol. Chem. 276:48066-48076, 2001.
39. Kim C.H., Cho Y.S., Chum Y.S., et al.: Early expression of myocardial HIF-1alpha in response to mechanical stress: regulation by stretch-activated channels and the phosphatidylinositol 3-kinase signaling pathway. Circ. Res. 90:E25-E33, 2002.
40. Kietzmann T., Gorlach A.: Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression. Semin. Cell. Dev. Biol. 16:474-486, 2005.
41. Gross J., Rheinlander C., Fuch J., et al.: Expression of hypoxia-inducible factor-1 in the cochlea of newborn rats. Hear. Res. 183:73-83, 2003.
42. Heidbreder M., Frohlich F., Johren O., et al.: Hypoxia rapidly activates HIF-1 alpha mRNA expression. FASEB J. 17:1541-1543, 2003.
43. Kaelin W.G.: The von Hippel-Lindau tumor suppressor protein: roles in cancer and oxygen sensing. Cold Spring Harb. Symp. Quant. Biol. 70:159-66, 2005.
44. Min J.H., Yang H., Ivan M., et al.: Structure and HIF-1apha-pVHL complex: hydroxyproline recognition in signaling. Science 296:1886-1889, 2002.
45. Ivan M., Kondo K., Yang H., et al: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468, 2001.
46. Carrero P., Okamoto K., Coumailleau P., O'Brien S., Tanaka H., Poellinger L.: Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxiainducible factor 1alpha. Mol. Cell. Biol. 20:402-15, 2000.
47. Kaelin W.G. Jr.: Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2:673-682, 2002.
48. Berra E., Ginouves A., Pouyssegur J.: The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep. 7(1):41-5, 2006.
49. Görlach A., Diebold I., Schini-Kerth V.B., et al.: Thrombin activates the hypoxiainducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ. Res. 89:47-54, 2001.
50. Knowles H.J., Raval R.R., Harris A.L., Ratcliffe P.J.: Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res. 63:1764-8, 2003.
51. Hirsila M., Koivunen P., Gunzler V., Kivirikko K.I., Myllyharju J.: Characterization of the human prolyl 4-hydroxylases that modif. the hypoxia-inducible factor. J. Biol. Chem. 278:30772-80, 2003.
52. Welsh S.J., Bellamy W.T., Briehl M.M., Powis G.: The redox protein thioredoxin-1 (Trx-1) increases hypoxia-inducible factor 1alpha protein expression: Trx-1 overexpression results in increased vascular endothelial growth factor production and enhanced tumour angiogenesis. Cancer Res. 62:5089-95, 2002.
53. Liu Q., Berchner-Pfannschmidt U., Moller U., et al.: A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc. Natl. Acad. Sci. USA 101:4302-7, 2004.
54. Yang Z.Z., Zhang A.Y., Yi F.X., Li P.L., Zou A.P.: Redox regulation of HIF-1alpha levels and HO-1 expression in renal medullary interstitial cells. Am. J. Physiol. Renal Physiol. 284:F1207-15, 2003.
55. Chandel N.S., McClintock D.S., Feliciano C.E., et al.: Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275:25130-8, 2000.
56. Jung Y., Isaacs J.S., Lee S., Trepel J., Liu Z.G., Neckers L.: Hypoxiainducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent uclear factor kappa beta activation. Biochem. J. 370:1011-7, 2003.
57. Wyatt C.N., Buckler K.J.: The effect of mitochondrial inhibitors on membrane currents in isolated neonatal rat carotid body type I cells. J. Physiol. 556:175-91, 2004.
58. Michelakis E.D., Hampl V., Nsair A., et al.: Diversity in mitochondrial function explains differences in vascular oxygen sensing. Circ. Res. 90:1307-15, 2002.
59. Hool L.C., Arthur P.G.: Decreasing cellular hydrogen peroxide with catalase mimics the effects of hypoxia on the sensitivity of the Ltype Ca2+ channel to beta-adrenergic receptor stimulation in cardiac myocytes. Circ. Res. 91:601-9, 2002.
60. Carriere A., Fernandez Y., Rigoulet M., Penicaud L., Casteilla L.: Inhibition of preadipocyte proliferation by mitochondrial reactive oxygen species. FEBS Lett. 550:163-7, 2003.
61. Chandel N.S., McClintock D.S., Feliciano C.E., et al.: Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275:25130-8, 2000.
62. Takahashi M. A., Asada K.: Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch. Biochem. Biophys. 226:558-566, 1983.
63. Hadad J.J., Land S.C.: A non-hypoxic, ROS-sensitive pathway mediates TNF-alpha-dependent regulation of HIF-1 apha. FEBS Lett. 505:269-274, 2001.
64. Mateo J., Garcia-Ledea M., Cadenas S., Hernández C., Moncada S.: Regulation of hypoxia-inducible factor-1 apha by nitric oxide throught mitochondria-dependent and independent pathways. Biochem. J. 376:537-544, 2003.
65. Hagen T., Taylor C.T., Lam F., Moncada S.: Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIFlapha. Science 302:1975-1978, 2003.
66. Rota C., Fann Y.C., Mason R.P.: Phenoxyl free radical formation during the oxidation of the fluorescent dye 2′,7′-dichlorofluorescein by horseradish peroxidase. Possible consequences for oxidative stress measurements. J. Biol. Chem. 274:28161-8, 1999.
67. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T.: Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95:11715-20, 1998.
68. Chandel N.S., Schumacker P.T., Arch R.H.: Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J. Biol. Chem. 276:42728-36, 2001.
69. Hagen T., Taylor C.T., Lam F., Moncada S.: Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302:1975-8, 2003.
70. Searle G.J., Hartness M.E., Hoareau R., Peers C., Kemp P.J.: Lack of contribution of mitochondrial electron transport to acute O2 sensing in model airway chemoreceptors. Biochem. Biophys. Res. Commun. 291:332-7, 2002.
71. Vaux E.C., Metzen E., Yeates K.M., Ratcliffe P.J.: Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98:296-302, 2001.
72. Srinivas V., Leshchinsky I., Sang N., King M.P., Minchenko A., Caro J.: Oxygen sensing and HIF-1 activation does not require an active mitochondrial respiratory chain electron-transfer pathway. J. Biol. Chem. 276:21995-8, 2001.
73. Park J.H., Kim T.Y., Jong H.S., et al.: Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1alpha in gastric cancer cells. Clin. Cancer Res. 9:433-40, 2003.
74. Williams K.J., Parker C.A., Stratford I.J.: Exogenous and endogenous markers of tumour oxygenation status: definitive markers of tumour hypoxiaα Adv. Exp. Med. Biol. 566:285-94, 2005.
75. Giatromanolaki A., Harris A.L.: Tumour hypoxia, hypoxia signalling pathways and hypoxia inducible factor expression in human cancer. Anticancer Res. 21:4317-4324, 2001.
76. Bos R., Zhong H., Hanrahan C.F., et al.: Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J. Natl. Cancer Inst. 93:309-314, 2001.
77. Zagzag D., Zhong H., Scalzitti J.M., Laughner E., Simons J.W., Semenza G.L.: Expression of hypoxia-inducible factor 1α in human brain tumours: association with angiogenesis, invasion, and progression. Cancer 88:2606-2618, 2000.
78. Maxwell P.H., Dachs G.U., Gleadle J.M., et al.: Hypoxia-inducible factor-1 modulates gene expression in solid tumours and influences both angiogenesis and tumour growth. Proc. Natl. Acad. Sci. USA 94:8104-8109, 1997.
79. Seagroves T.N., Ryan H.E., Lu H., et al.: Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol. Cell. Biol. 21:3436-3444, 2001.
80. Hicks K.O., Pruijn F.B., Sturman J.R. Denny W.A., Wilson W.R.: Multicellular resistance to tirapazamine is due to restricted extravascular transport in HT29 multicellular layer cultures: A pharmacokinetic/ pharmacodynamic study. Cancer Res. 63:5970-5977, 2003.
81. Nagle D.G., Zhou Y.D., Mora F.D., Mohammed K.A., Kim Y.P. Mechanism targeted discovery of antitumour marine natural products. Curr. Med. Chem. 11(13):1725-1756, 2004.
82. Bussink J., Kaanders J. H. A. M., van der Kogel A. J.: Tumour hypoxia at the micro-regional level: clinical relevance and predictive value of exdogenous and endogenous hypoxic cell markers. Radiother. Oncol. 67:3-15, 2003.