HIF-independent regulation of thioredoxin reductase 1 contributes to the high levels of reactive oxygen species induced by hypoxia

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Naranjo Suarez, Salvador ^a,b   Carlson, Bradley A ^a   Tsuji, Petra A ^a,c   Yoo, Min Hyuk ^a   Gladyshev, Vadim N ^d   Hatfield, Dolph L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c TOWSON UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; MESSENGER RNA; OXYGENASE INHIBITOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE INHIBITOR; REACTIVE OXYGEN METABOLITE; THIOREDOXIN REDUCTASE 1; UNCLASSIFIED DRUG; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TXNRD1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE EXPRESSION REGULATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; ANIMAL; ANOXIA; CELL STRAIN 3T3; GENETICS; METABOLISM;

3T3 CELLS; ANIMALS; ANOXIA; DOWN-REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; PROTEIN STABILITY; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; THIOREDOXIN REDUCTASE 1;

EID: 84856837495     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030470     Document Type: Article

References (40)

1. Semenza GL, (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551-578.
2. Seta KA, Spicer Z, Yuan Y, Lu G, Millhorn DE, (2002) Responding to hypoxia: lessons from a model cell line. Sci STKE 146: RE11.
3. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
4. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
5. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, et al. (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275: 25130-25138.
6. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, et al. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408.
7. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, et al. (2005) Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 1: 409-414.
8. Hoffman DL, Salter JD, Brookes PS, (2007) Response of mitochondrial reactive oxygen species generation to steady-state oxygen tension: implications for hypoxic cell signaling. Am J Physiol Heart Circ Physiol 292: H101-108.
9. Srinivas V, Leshchinsky I, Sang N, King MP, Minchenko A, et al. (2001) Oxygen sensing and HIF-1 activation does not require an active mitochondrialrespiratory chain electron-transfer pathway. J Biol Chem 276: 21995-21998.
10. Vaux EC, Metzen E, Yeates KM, Ratcliffe PJ, (2001) Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98: 296-302.
11. Chua YL, Dufour E, Dassa EP, Rustin P, Jacobs HT, et al. (2010) Stabilization of hypoxia-inducible factor-1alpha protein in hypoxia occurs independently of mitochondrial reactive oxygen species production. J Biol Chem 285: 31277-31284.
12. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E, (2004) Oxidative stress and cell signalling. Curr Med Chem 11: 1163-1182.
13. Banning A, Deubel S, Kluth D, Zhou Z, Brigelius-Flohe R, (2005) The GI-GPx gene is a target for Nrf2. Mol Cell Biol 25: 4914-4923.
14. Fu T, Okano Y, Nozawa Y, (1992) Differential pathways (phospholipase C and phospholipase D) of bradykinin-induced biphasic 1,2-diacylglycerol formation in non-transformed and K-ras-transformed NIH-3T3 fibroblasts. Involvement of intracellular Ca2+ oscillations in phosphatidylcholine breakdown. Biochem J 283 (Pt 2): 347-354.
15. Chen B, Cepko CL, (2009) HDAC4 regulates neuronal survival in normal and diseased retinas. Science 323: 256-259.
16. Yoo MH, Xu XM, Carlson BA, Gladyshev VN, Hatfield DL, (2006) Thioredoxin reductase 1 deficiency reverses tumor phenotype and tumorigenicity of lung carcinoma cells. J Biol Chem 281: 13005-13008.
17. Yoo MH, Xu XM, Turanov AA, Carlson BA, Gladyshev VN, et al. (2007) A new strategy for assessing selenoprotein function: siRNA knockdown/knock-in targeting the 3′-UTR. RNA 13: 921-929.
18. Irons R, Tsuji PA, Carlson BA, Ouyang P, Yoo MH, et al. (2010) Deficiency in the 15-kDa selenoprotein inhibits tumorigenicity and metastasis of colon cancer cells. Cancer Prev Res (Phila) 3: 630-639.
19. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613.
20. Cormier-Regard S, Nguyen SV, Claycomb WC, (1998) Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J Biol Chem 273: 17787-17792.
21. Garayoa M, Martinez A, Lee S, Pio R, An WG, et al. (2000) Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol Endocrinol 14: 848-862.
22. Warnecke C, Griethe W, Weidemann A, Jurgensen JS, Willam C, et al. (2003) Activation of the hypoxia-inducible factor-pathway and stimulation of angiogenesis by application of prolyl hydroxylase inhibitors. FASEB J 17: 1186-1188.
23. Yoo MH, Gu X, Xu XM, Kim JY, Carlson BA, et al. (2010) Delineating the role of glutathione peroxidase 4 in protecting cells against lipid hydroperoxide damage and in Alzheimer's disease. Antioxid Redox Signal 12: 819-827.
24. Du J, Daniels DH, Asbury C, Venkataraman S, Liu J, et al. (2006) Mitochondrial production of reactive oxygen species mediate dicumarol-induced cytotoxicity in cancer cells. J Biol Chem 281: 37416-37426.
25. Wenger RH, Stiehl DP, Camenisch G, (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005: re12.
26. Peyssonnaux C, Zinkernagel AS, Schuepbach RA, Rankin E, Vaulont S, et al. (2007) Regulation of iron homeostasis by the hypoxia-inducible transcription factors (HIFs). J Clin Invest 117: 1926-1932.
27. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, et al. (2009) HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J Clin Invest 119: 1159-1166.
28. Biaglow JE, Miller RA, (2005) The thioredoxin reductase/thioredoxin system: novel redox targets for cancer therapy. Cancer Biol Ther 4: 6-13.
29. Rigoulet M, Yoboue ED, Devin A, (2011) Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. Antioxid Redox Signal 14: 459-468.
30. Lopez-Barneo J, Pardal R, Ortega-Saenz P, (2001) Cellular mechanism of oxygen sensing. Annu Rev Physiol 63: 259-287.
31. Liu Q, Berchner-Pfannschmidt U, Moller U, Brecht M, Wotzlaw C, et al. (2004) A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci U S A 101: 4302-4307.
32. Zulueta JJ, Yu FS, Hertig IA, Thannickal VJ, Hassoun PM, (1995) Release of hydrogen peroxide in response to hypoxia-reoxygenation: role of an NAD(P)H oxidase-like enzyme in endothelial cell plasma membrane. Am J Respir Cell Mol Biol 12: 41-49.
33. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, et al. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95: 11715-11720.
34. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, et al. (2005) Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 1: 393-399.
35. Maija Hirsila, Peppi Koivunen, Volkmar Gn, Kari IKivirikko, Myllyharju J, (2003) Characterization of the Human Prolyl 4-Hydroxylases That Modify the Hypoxia-inducible Factor*. J Biol Chem 278: 30772-30780.
36. Powis G, Montfort WR, (2001) Properties and biological activities of thioredoxins. Annu Rev Pharmacol Toxicol 41: 261-295.
37. Hammond EM, Denko NC, Dorie MJ, Abraham RT, Giaccia AJ, (2002) Hypoxia links ATR and p53 through replication arrest. Mol Cell Biol 22: 1834-1843.
38. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, et al. (2003) Hypoxia-Inducible Factor 1 Is Essential for Cell Cycle Arrest during Hypoxia. Mol Cell Biol 23: 359-369.
39. Ushio-Fukai M, (2006) Redox signaling in angiogenesis: role of NADPH oxidase. Cardiovasc Res 71: 226-235.
40. Miller TW, Isenberg JS, Roberts DD, (2009) Molecular regulation of tumor angiogenesis and perfusion via redox signaling. Chem Rev 109: 3099-3124.