NADPH oxidase-mitochondria axis-derived ROS mediate arsenite-induced HIF-1α stabilization by inhibiting prolyl hydroxylases activity

Toxicology Letters

Volumn 224, Issue 2, 2014, Pages 165-174

  Li, Ying Na ^a   Xi, Miao Miao ^b   Guo, Yu ^b   Hai, Chun Xu ^b   Yang, Wei Lin ^a   Qin, Xu Jun ^b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Arsenic; Mitochondria; NADPH oxidase; Prolyl hydroxylases (PHDs); Reactive oxygen species (ROS)

Indexed keywords

ARSENIC; ARSENIC TRIOXIDE; DIPHENYLIODONIUM SALT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYDROXYLATION; LIVER CELL; MITOCHONDRION; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVERSE TRANSCRIPTION; WESTERN BLOTTING;

EID: 84888109789     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.10.029     Document Type: Article

References (58)

1. Ahluwalia A., Tarnawski A.S. Critical role of hypoxia sensor - HIF-1α in VEGF gene activation. Implications for angiogenesis and tissue injury healing. Curr. Med. Chem. 2012, 19:90-97.
2. Carpenter R.L., Jiang Y., Jing Y., He J., Rojanasakul Y., Liu L.Z., Jiang B.H. Arsenite induces cell transformation by reactive oxygen species, AKT, ERK1/2, and p70S6K1. Biochem. Biophys. Res. Commun. 2011, 414:533-538.
3. Cavadas M.A., Nguyen L.K., Cheong A. Hypoxia-inducible factor (HIF) network: insights from mathematical models. Cell Commun. Signal. 2013, 11:42.
4. Cheng G., Zielonka J., McAllister D.M., Mackinnon A.C., Joseph J., Dwinell M.B., Kalyanaraman B. Mitochondria-targeted vitamin E analogs inhibit breast cancer cell energy metabolism and promote cell death. BMC Cancer 2013, 13:285.
5. Cooper K.L., Liu K.J., Hudson L.G. Enhanced ROS production and redox signaling with combined arsenite and UVA exposure: contribution of NADPH oxidase. Free Radic. Biol. Med. 2009, 47:381-388.
6. Corcoran A., O'Connor J.J. Hypoxia-inducible factor signalling mechanisms in the central nervous system. Acta Physiol. (Oxf.) 2013, 208:298-310.
7. Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic. Biol. Med. 2011, 51:1289-1301.
8. Doughan A.K., Harrison D.G., Dikalov S.I. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 2008, 102:488-496.
9. Edwards D.H., Li Y., Ellinsworth D.C., Griffith T.M. The effect of inorganic arsenic on endothelium-dependent relaxation: role of NADPH oxidase and hydrogen peroxide. Toxicology 2013, 306:50-58.
10. Evans C.E., Branco-Price C., Johnson R.S. HIF-mediated endothelial response during cancer progression. Int. J. Hematol. 2012, 95:471-477.
11. Figueira T.R., Barros M.H., Camargo A.A., Castilho R.F., Ferreira J.C., Kowaltowski A.J., Sluse F.E., Souza-Pinto N.C., Vercesi A.E. Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid. Redox. Signal. 2013, 18:2029-2074.
12. Greer S.N., Metcalf J.L., Wang Y., Ohh M. The updated biology of hypoxia-inducible factor. EMBO J. 2012, 31:2448-2460.
13. Guo L., Li L., Wang W., Pan Z., Zhou Q., Wu Z. Mitochondrial reactive oxygen species mediates nicotine-induced hypoxia-inducible factor-1α expression in human non-small cell lung cancer cells. Biochim. Biophys. Acta 2012, 1822:852-861.
14. Hartwig A. Metal interaction with redox regulation: an integrating concept in metal carcinogenesis?. Free Radic. Biol. Med. 2013, 55:63-72.
15. Hawkins B.J., Madesh M., Kirkpatrick C.J., Fisher A.B. Superoxide flux in endothelial cells via the chloride channel-3 mediates intracellular signaling. Mol. Biol. Cell 2007, 18:2002-2012.
16. Hu Y., Liu J., Huang H. Recent agents targeting HIF-1α for cancer therapy. J. Cell Biochem. 2013, 114:498-509.
17. Hubaux R., Becker-Santos D.D., Enfield K.S., Rowbotham D., Lam S., Lam W.L., Martinez V.D. Molecular features in arsenic-induced lung tumors. Mol. Cancer 2013, 12:20.
18. IARC A Review of Human Carcinogens: Arsenic, Metals, Fibres, and Dusts 2012, World Health Organization Press, Lyon.
19. Irwin D.C., McCord J.M., Nozik-Grayck E., Beckly G., Foreman B., Sullivan T., White M.T., Crossno J.J., Bailey D., Flores S.C., Majka S., Klemm D., van Patot M.C. A potential role for reactive oxygen species and the HIF-1α-VEGF pathway in hypoxia-induced pulmonary vascular leak. Free Radic. Biol. Med. 2009, 47:55-61.
20. Jokilehto T., Jaakkola P.M. The role of HIF prolyl hydroxylases in tumour growth. J. Cell Mol. Med. 2010, 14:758-770.
21. Jomova K., Jenisova Z., Feszterova M., Baros S., Liska J., Hudecova D., Rhodes C.J., Valko M. Arsenic: toxicity, oxidative stress and human disease. J. Appl. Toxicol. 2011, 31:95-107.
22. Keith B., Johnson R.S., Simon M.C. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 2012, 12:9-22.
23. Khan S.A., Nanduri J., Yuan G., Kinsman B., Kumar G.K., Joseph J., Kalyanaraman B., Prabhakar N.R. NADPH oxidase 2 mediates intermittent hypoxia-induced mitochondrial complex I inhibition: relevance to blood pressure changes in rats. Antioxid. Redox. Signal. 2011, 14:533-542.
24. Kitchin K.T., Conolly R. Arsenic-induced carcinogenesis - oxidative stress as a possible mode of action and future research needs for more biologically based risk assessment. Chem. Res. Toxicol. 2010, 23:327-335.
25. Kobliakov V.A. Mechanisms of tumor promotion by reactive oxygen species. Biochemistry (Moscow) 2010, 75:675-685.
26. Kuiper C., Molenaar I.G., Dachs G.U., Currie M.J., Sykes P.H., Vissers M.C. Low ascorbate levels are associated with increased hypoxia-inducible factor-1 activity and an aggressive tumor phenotype in endometrial cancer. Cancer Res. 2010, 70:5749-5758.
27. Lappin T., Masson N. Two antioxidants are better than one. Blood 2011, 117:5276-5277.
28. Lee J.C., Son Y.O., Pratheeshkumar P., Shi X. Oxidative stress and metal carcinogenesis. Free Radic. Biol. Med. 2012, 53:742-757.
29. Ling M., Li Y., Xu Y., Pang Y., Shen L., Jiang R., Zhao Y., Yang X., Zhang J., Zhou J., Wang X., Liu Q. Regulation of miRNA-21 by reactive oxygen species-activated ERK/NF-kappaB in arsenite-induced cell transformation. Free Radic. Biol. Med. 2012, 52:1508-1518.
30. Linster C.L., Van Schaftingen E. Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J. 2007, 274:1-22.
31. Liu L.Z., Jiang Y., Carpenter R.L., Jing Y., Peiper S.C., Jiang B.H. Role and mechanism of arsenic in regulating angiogenesis. PLoS One 2011, 6:e20858.
32. Meng D., Mei A., Liu J., Kang X., Shi X., Qian R., Chen S. NADPH oxidase 4 mediates insulin-stimulated HIF-1α and VEGF expression, and angiogenesis in vitro. PLoS One 2012, 7:e48393.
33. Naranmandura H., Xu S., Sawata T., Hao W.H., Liu H., Bu N., Ogra Y., Lou Y.J., Suzuki N. Mitochondria are the main target organelle for trivalent monomethylarsonous acid (MMA(III))-induced cytotoxicity. Chem. Res. Toxicol. 2011, 24:1094-1103.
34. Niecknig H., Tug S., Reyes B.D., Kirsch M., Fandrey J., Berchner-Pfannschmidt U. Role of reactive oxygen species in the regulation of HIF-1 by prolyl hydroxylase 2 under mild hypoxia. Free Radic. Res. 2012, 46:705-717.
35. Page E.L., Chan D.A., Giaccia A.J., Levine M., Richard D.E. Hypoxia-inducible factor-1α stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol. Biol. Cell 2008, 19:86-94.
36. Patten D.A., Lafleur V.N., Robitaille G.A., Chan D.A., Giaccia A.J., Richard D.E. Hypoxia-inducible factor-1 activation in nonhypoxic conditions: the essential role of mitochondrial-derived reactive oxygen species. Mol. Biol. Cell 2010, 21:3247-3257.
37. Pi J., Diwan B.A., Sun Y., Liu J., Qu W., He Y., Styblo M., Waalkes M.P. Arsenic-induced malignant transformation of human keratinocytes: involvement of Nrf2. Free Radic. Biol. Med. 2008, 45:651-658.
38. Queliconi B.B., Wojtovich A.P., Nadtochiy S.M., Kowaltowski A.J., Brookes P.S. Redox regulation of the mitochondrial K(ATP) channel in cardioprotection. Biochim. Biophys. Acta 2011, 1813:1309-1315.
39. Shimojo Y., Akimoto M., Hisanaga T., Tanaka T., Tajima Y., Honma Y., Takenaga K. Attenuation of reactive oxygen species by antioxidants suppresses hypoxia-induced epithelial-mesenchymal transition and metastasis of pancreatic cancer cells. Clin. Exp. Metastasis 2013, 30:143-154.
40. Smith T.G., Talbot N.P. Prolyl hydroxylases and therapeutics. Antioxid. Redox. Signal. 2010, 12:431-433.
41. Straub A.C., Clark K.A., Ross M.A., Chandra A.G., Li S., Gao X., Pagano P.J., Stolz D.B., Barchowsky A. Arsenic-stimulated liver sinusoidal capillarization in mice requires NADPH oxidase-generated superoxide. J. Clin. Invest. 2008, 118:3980-3989.
42. Tang C.M., Yu J. Hypoxia-inducible factor-1 as a therapeutic target in cancer. J. Gastroenterol. Hepatol. 2013, 28:401-405.
43. Tokar E.J., Diwan B.A., Ward J.M., Delker D.A., Waalkes M.P. Carcinogenic effects of "whole-life" exposure to inorganic arsenic in CD1 mice. Toxicol. Sci. 2011, 119:73-83.
44. Tseng H.Y., Liu Z.M., Huang H.S. NADPH oxidase-produced superoxide mediates EGFR transactivation by c-Src in arsenic trioxide-stimulated human keratinocytes. Arch. Toxicol. 2012, 86:935-945.
45. Vissers M.C., Gunningham S.P., Morrison M.J., Dachs G.U., Currie M.J. Modulation of hypoxia-inducible factor-1α in cultured primary cells by intracellular ascorbate. Free Radic. Biol. Med. 2007, 42:765-772.
46. Wang Y., Xu Y., Wang H., Xue P., Li X., Li B., Zheng Q., Sun G. Arsenic induces mitochondria-dependent apoptosis by reactive oxygen species generation rather than glutathione depletion in Chang human hepatocytes. Arch. Toxicol. 2009, 83:899-908.
47. Wang L., Son Y.O., Ding S., Wang X., Hitron J.A., Budhraja A., Lee J.C., Lin Q., Poyil P., Zhang Z., Luo J., Shi X. Ethanol enhances tumor angiogenesis in vitro induced by low-dose arsenic in colon cancer cells through hypoxia-inducible factor 1α pathway. Toxicol. Sci. 2012, 130:269-280.
48. Wang X., Mandal A.K., Saito H., Pulliam J.F., Lee E.Y., Ke Z.J., Lu J., Ding S., Li L., Shelton B.J., Tucker T., Evers B.M., Zhang Z., Shi X. Arsenic and chromium in drinking water promote tumorigenesis in a mouse colitis-associated colorectal cancer model and the potential mechanism is ROS-mediated Wnt/beta-catenin signaling pathway. Toxicol. Appl. Pharmacol. 2012, 262:11-21.
49. Wang F., Zhou X., Liu W., Sun X., Chen C., Hudson L.G., Jian Liu K. Arsenite-induced ROS/RNS generation causes zinc loss and inhibits the activity of poly(ADP-ribose) polymerase-1. Free Radic. Biol. Med. 2013, 61C:249-256.
50. Washko P.W., Hartzell W.O., Levine M. Ascorbic acid analysis using high-performance liquid chromatography with coulometric electrochemical detection. Anal. Biochem. 1989, 181:276-282.
51. Xu Y., Li Y., Pang Y., Ling M., Shen L., Jiang R., Zhao Y., Zhou J., Wang X., Liu Q. Blockade of p53 by HIF-2α, but not HIF-1α, is involved in arsenite-induced malignant transformation of human bronchial epithelial cells. Arch. Toxicol. 2012, 86:947-959.
52. Yan L., Colandrea V.J., Hale J.J. Prolyl hydroxylase domain-containing protein inhibitors as stabilizers of hypoxia-inducible factor: small molecule-based therapeutics for anemia. Expert Opin. Ther. Pat. 2010, 20:1219-1245.
53. Yang Y., Karakhanova S., Werner J., Bazhin A.V. Reactive oxygen species in cancer biology and anticancer therapy. Curr. Med. Chem. 2013, 20:3677-3692.
54. Yang Y., Sun M., Wang L., Jiao B. HIFs, angiogenesis, and cancer. J. Cell Biochem. 2013, 114:967-974.
55. Zepeda A.B., Pessoa A., Castillo R.L., Figueroa C.A., Pulgar V.M., Farias J.G. Cellular and molecular mechanisms in the hypoxic tissue: role of HIF-1 and ROS. Cell Biochem. Funct. 2013, 31:451-459.
56. Zhang Z., Wang X., Cheng S., Sun L., Son Y.O., Yao H., Li W., Budhraja A., Li L., Shelton B.J., Tucker T., Arnold S.M., Shi X. Reactive oxygen species mediate arsenic induced cell transformation and tumorigenesis through Wnt/beta-catenin pathway in human colorectal adenocarcinoma DLD1 cells. Toxicol. Appl. Pharmacol. 2011, 256:114-121.
57. Zhao F., Severson P., Pacheco S., Futscher B.W., Klimecki W.T. Arsenic exposure induces the Warburg effect in cultured human cells. Toxicol. Appl. Pharmacol. 2013, 271:72-77.
58. Zinkevich N.S., Gutterman D.D. ROS-induced ROS release in vascular biology: redox-redox signaling. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H647-H653.