Hypoxic but not anoxic stabilization of HIF-1α requires mitochondrial reactive oxygen species

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 283, Issue 5 27-5, 2002, Pages

  Schroedl, Clara ^a   McClintock, David S ^a   Budinger, G R Scott ^a   Chandel, Navdeep S ^a  

^a Divisions of Critical Care   (United States)

Author keywords

Complex I; Rho zero; Rotenone

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; RHO FACTOR; ROTENONE;

ANOXIA; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; HUMAN; HUMAN CELL; HYDROXYLATION; HYPOXIA; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY;

EID: 0036838358     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00014.2002     Document Type: Article

References (38)

1. Agani FH, Pichiule P, Chavez JC, and LaManna JC. The role of mitochondria in the regulation of hypoxia-inducible factor 1 expression during hypoxia. J Biol Chem 275: 35863-35867, 2000.
2. Aragones J, Jones DR, Martin S, San Juan MA, Alfranca A, Vidal F, Vara A, Merida I, and Landazuri MO. Evidence for the involvement of diacylglycerol kinase in the activation of hypoxia-inducible transcription factor 1 by low oxygen tension. J Biol Chem 276: 10548-10555, 2001.
3. Au HC, Seo BB, Matsuno-Yagi A, Yagi T, and Scheffler IE. The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria. Proc Natl Acad Sci USA 96: 4354-4359, 1999.
4. Bruick RK and McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340, 2001.
5. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, and Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95: 5015-5019, 1998.
6. 2 sensing. J Biol Chem 275: 25130-25138, 2000.
7. Chandel NS, Vander Heiden MG, Thompson CB, and Schumacker PT. Redox regulation of p53 during hypoxia. Oncogene 19: 3840-3848, 2000.
8. DeFrancesco L, Werntz D, and Scheffler IE. Conditionally lethal mutations in chinese hamster cells. Characterization of a cell line with a possible defect in the Krebs cycle. J Cell Physiol 85: 293-305, 1975.
9. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, and Ratcliffe PJ. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54, 2001.
10. Gleadle JM, Ebert BL, and Ratcliffe PJ. Diphenylene iodonium inhibits the induction of erythropoietin and other mammalian genes by hypoxia. Implications for the mechanism of oxygen sensing. Eur J Biochem 234: 92-99, 1995.
11. Gleadle JM and Ratcliffe PJ. Induction of hypoxia-inducible factor-1, erythropoietin, vascular endothelial growth factor, and glucose transporter-1 by hypoxia: Evidence against a regulatory role for Src kinase. Blood 89: 503-509, 1997.
12. Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, and Busse R. 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.
13. Haddad JJ and Land SC. A non-hypoxic, ROS-sensitive pathway mediates TNF-alpha-dependent regulation of HIF-1alpha. FEBS Lett 505: 269-274, 2001.
14. Hirota K and Semenza GL. Rac1 activity is required for the activation of hypoxia-inducible factor 1. J Biol Chem 276: 21166-21172, 2001.
15. 2 sensing. Science 292: 464-468, 2001.
16. 2-regulated prolyl hydroxylation. Science 292: 468-472, 2001.
17. Jamieson D, Chance B, Cadenas E, and Boveris A. The relation of free radical production to hyperoxia. Annu Rev Physiol 48: 703-719, 1986.
18. 2 tension. Am J Physiol Cell Physiol 271: C1172-C1180, 1996.
19. 2 and ATP. Am J Physiol Cell Physiol 250: C663-C675, 1986.
20. Killilea DW, Hester R, Balczon R, Babal P, and Gillespie MN. Free radical production in hypoxic pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 279: L408-L412, 2000.
21. King MP and Attardi G. Isolation of human cell lines lacking mitochondrial DNA. Methods Enzymol 264: 304-313, 1996.
22. Leach RM, Hill HM, Snetkov VA, Robertson TP, and Ward JP. Divergent roles of glycolysis and the mitochondrial electron transport chain in hypoxic pulmonary vasoconstriction of the rat: Identity of the hypoxic sensor. J Physiol 536: 211-224, 2001.
23. Liu Q, Kuppusamy P, Sham JS, Shimoda LA, Zweier JL, and Sylvester JT. Increased production of reactive oxygen species (ROS) by pulmonary arterial smooth muscle is required for hypoxic pulmonary vasoconstriction (HPV). Am J Respir Crit Care Med 163: A395, 2001.
24. Mahadev K, Zilbering A, Zhu L, and Goldstein BJ. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade J. Biol Chem 276: 21938-21942, 2001.
25. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, and Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
26. McClintock DS, Santore MT, Lee VY, Brunelle J, Scott Budinger GR, Zong W-X, Thompson CB, Hay N, and Chandel NS. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation induced cell death. Mol Cell Biol 22: 94-104, 2002.
27. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, Pavletich N, Chau V, and Kaelin WG. Ubiquitination of hypoxia-inducible factor requires direct binding to the betadomain of the von Hippel-Lindau protein. Nat Cell Biol 2: 423-427, 2000.
28. Richard DE, Berra E, and Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem 275: 26765-26771, 2000.
29. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551-578, 1999.
30. Seo BB, Kitajima-Ihara T, Chan EK, Scheffler IE, Matsuno-Yagi A, and Yagi T. Molecular remedy of complex I defects: Rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc Natl Acad Sci USA 95: 9167-9171, 1999.
31. Srinivas V, Leshchinsky I, Sang N, King MP, Minchenko A, and Caro J. Oxygen sensing and HIF-1 activation does not require an active mitochondrial respiratory chain electron-transfer pathway. J Biol Chem 276: 21995-21998, 2001.
32. Vaux EC, Metzen E, Yeates KM, and Ratcliffe PJ. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98: 296-302, 2001.
33. 2 tension. Proc Natl Acad Sci USA 92: 5510-5514, 1995.
34. Waypa GB, Chandel NS, and Schumacker PT. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ Res 88: 1259-1266, 2001.
35. Williams KJ, Telfer BA, Airley RE, Peters HP, Sheridan MR, van der Kogel AJ, Harris AL, and Stratford IJ. A protective role for HIF-1 in response to redox manipulation and glucose deprivation: Implications for tumorigenesis. Oncogene 21: 282-290, 2002.
36. Wilson DF, Rumsey WL, Green TJ, and Vanderkooi JM. The oxygen dependence of mitochondrial oxidative phosphorylation measured by a new optical method for measuring oxygen concentration. J Biol Chem 263: 2712-2718, 1988.
37. Wood JG, Johnson JS, Mattioli LF, and Gonzalez NC. Systemic hypoxia promotes leukocyte-endothelial adherence via reactive oxidant generation. J Appl Physiol 87: 1734-1740, 1999.
38. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, Simons JW, and Semenza GL. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: Implications for tumor angiogenesis and therapeutics. Cancer Res 60: 1541-1545, 2000.