Hypoxia-inducible factor-1 activation in nonhypoxic conditions: The essential role of mitochondrial-derived reactive oxygen species

Molecular Biology of the Cell

Volumn 21, Issue 18, 2010, Pages 3247-3257

  Patten, David A ^a   Lafleur, Véronique N ^a   Robitaille, Geneviève A ^a   Chan, Denise A ^b   Giaccia, Amato J ^b   Richard, Darren E ^a  

^a Université Laval   (Canada)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; ANTIOXIDANT; HYPOXIA INDUCIBLE FACTOR 1; MITOCHONDRIAL PROTEIN; PROTEIN P22; PROTEIN SKQ1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; MALE; MITOCHONDRION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TARGETING; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX III; HYPOXIA-INDUCIBLE FACTOR 1; MALE; METHACRYLATES; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; POLYENES; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; THIAZOLES;

EID: 77956713136     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-01-0025     Document Type: Article

References (75)

1. Aldieri, E., Riganti, C., Polimeni, M., Gazzano, E., Lussiana, C., Campia, I., and Ghigo, D. (2008). Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr. Drug Metab. 9, 686-696.
2. Ambasta, R. K., Kumar, P., Griendling, K. K., Schmidt, H. H., Busse, R., and Brandes, R. P. (2004). Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279, 45935-45941.
3. Andreyev, A. Y., Kushnareva, Y. E., and Starkov, A. A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry 70, 200-214.
4. Antonenko, Y. N., et al. (2008). Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry 73, 1273-1287.
5. Babior, B.M. (2004). NADPH oxidase. Curr. Opin. Immunol. 16, 42-47.
6. Baumer, A. T., Ten Freyhaus, H., Sauer, H., Wartenberg, M., Kappert, K., Schnabel, P., Konkol, C., Hescheler, J., Vantler, M., and Rosenkranz, S. (2008). Phosphatidylinositol 3-kinase-dependent membrane recruitment of Rac-1 and p47phox is critical for alpha-platelet-derived growth factor receptor-induced production of reactive oxygen species. J. Biol. Chem. 283, 7864-7876.
7. Bell, E. L., Klimova, T. A., Eisenbart, J., Moraes, C. T., Murphy, M. P., Budinger, G. R., and Chandel, N. S. (2007). The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol. 177, 1029-1036.
8. Brunelle, J. K., Bell, E. L., Quesada, N. M., Vercauteren, K., Tiranti, V., Zeviani, M., Scarpulla, R. C., and Chandel, N. S. (2005). Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 1, 409-414.
9. Cai, H., Li, Z., Dikalov, S., Holland, S. M., Hwang, J., Jo, H., Dudley, S. C., Jr., and Harrison, D. G. (2002). NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II. J. Biol. Chem. 277, 48311-48317.
10. Chan, D. A., Sutphin, P. D., Denko, N. C., and Giaccia, A. J. (2002). Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1alpha. J. Biol. Chem. 277, 40112-40117.
11. Chan, D. A., Sutphin, P. D., Yen, S. E., and Giaccia, A. J. (2005). Coordinate regulation of the oxygen-dependent degradation domains of hypoxia-inducible factor 1 alpha. Mol. Cell. Biol. 25, 6415-6426.
12. 2 sensing. J. Biol. Chem. 275, 25130-25138.
13. Chou, M. M., and Blenis, J. (1996). The 70 kDa S6 kinase complexes with and is activated by the Rho family G proteins Cdc42 and Rac1. Cell 85, 573-583.
14. Cockman, M. E., Masson, N., Mole, D. R., Jaakkola, P., Chang, G. W., Clifford, S. C., Maher, E. R., Pugh, C. W., Ratcliffe, P. J., and Maxwell, P. H. (2000). Hypoxia inducible factor-alpha binding and ubiquitylation by the von hippellindau tumor suppressor protein. J. Biol. Chem. 275, 25733-25741.
15. Corley, K. M., Taylor, C. J., and Lilly, B. (2005). Hypoxia-inducible factor 1alpha modulates adhesion, migration, and FAK phosphorylation in vascular smooth muscle cells. J. Cell. Biochem. 96, 971-985.
16. Dery, M. A., Michaud, M. D., and Richard, D. E. (2005). Hypoxia-inducible factor 1, regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell Biol. 37, 535-540.
17. Deshpande, S. S., Angkeow, P., Huang, J., Ozaki, M., and Irani, K. (2000). Rac1 inhibits TNF-alpha-induced endothelial cell apoptosis: dual regulation by reactive oxygen species. FASEB J. 14, 1705-1714.
18. Diebold, I., Djordjevic, T., Hess, J., and Gorlach, A. (2008). Rac-1 promotes pulmonary artery smooth muscle cell proliferation by upregulation of plasminogen activator inhibitor-1, role of NFkappaB-dependent hypoxia-inducible factor-1alpha transcription. Thromb. Haemost. 100, 1021-1028.
19. Diebold, I., Flugel, D., Becht, S., Belaiba, R. S., Bonello, S., Hess, J., Kietzmann, T., and Gorlach, A. (2010). The hypoxia-inducible Factor-2alpha is stabilized by oxidative stress involving NOX4. Antioxid. Redox Signal. 13, 425-436.
20. Doughan, A. K., Harrison, D. G., and Dikalov, S. I. (2008). Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 102, 488-496.
21. Epstein, A. C., et al. (2001). C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54.
22. Felty, Q., Xiong, W. C., Sun, D., Sarkar, S., Singh, K. P., Parkash, J., and Roy, D. (2005). Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry 44, 6900-6909.
23. Garrido, A. M., and Griendling, K. K. (2009). NADPH oxidases and angiotensin II receptor signaling. Mol. Cell. Endocrinol. 302, 148-158.
24. Gerthoffer, W. T. (2007). Mechanisms of vascular smooth muscle cell migration. Circ. Res. 100, 607-621.
25. Gorlach, A., Berchner-Pfannschmidt, U., Wotzlaw, C., Cool, R. H., Fandrey, J., Acker, H., Jungermann, K., and Kietzmann, T. (2003). Reactive oxygen species modulate HIF-1 mediated PAI-1 expression: involvement of the GTPase Rac1. Thromb. Haemost. 89, 926-935.
26. Griendling, K. K., Sorescu, D., and Ushio-Fukai, M. (2000). NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86, 494-501.
27. Guo, J., Chen, H., Ho, J., Mancini, J., Sontag, T., Laporte, S. A., Richard, D. E., and Lebrun, J. J. (2009). TGFbeta-induced GRK2 expression attenuates AngII-regulated vascular smooth muscle cell proliferation and migration. Cell Signal. 21, 899-905.
28. Guzy, R. D., Hoyos, B., Robin, E., Chen, H., Liu, L., Mansfield, K. D., Simon, M. C., Hammerling, U., and Schumacker, P. T. (2005). Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 1, 401-408.
29. Hanna, I. R., Hilenski, L. L., Dikalova, A., Taniyama, Y., Dikalov, S., Lyle, A., Quinn, M. T., Lassegue, B., and Griendling, K. K. (2004). Functional association of nox1 with p22phox in vascular smooth muscle cells. Free Radic. Biol. Med. 37, 1542-1549.
30. Heumuller, S., Wind, S., Barbosa-Sicard, E., Schmidt, H. H., Busse, R., Schroder, K., and Brandes, R. P. (2008). Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51, 211-217.
31. Hirota, K., and Semenza, G. L. (2001). Rac1 activity is required for the activation of hypoxia-inducible factor 1. J. Biol. Chem. 276, 21166-21172.
32. Hutchinson, D. S., Csikasz, R. I., Yamamoto, D. L., Shabalina, I. G., Wikstrom, P., Wilcke, M., and Bengtsson, T. (2007). Diphenylene iodonium stimulates glucose uptake in skeletal muscle cells through mitochondrial complex I inhibition and activation of AMP-activated protein kinase. Cell Signal. 19, 1610-1620.
33. 2 sensing. Science 292, 464-468.
34. Kaelin, W. G., Jr., and Ratcliffe, P. J. (2008). Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402.
35. Kaibuchi, K., Kuroda, S., and Amano, M. (1999). Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68, 459-486.
36. Kim, J., et al. (2008). Hypoxia-induced IL-18 increases hypoxia-inducible factor-1alpha expression through a Rac1-dependent NF-kappaB pathway. Mol. Biol. Cell 19, 433-444.
37. Kimura, S., Zhang, G. X., Nishiyama, A., Shokoji, T., Yao, L., Fan, Y. Y., Rahman, M., and Abe, Y. (2005a). Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45, 438-444.
38. Kimura, S., Zhang, G. X., Nishiyama, A., Shokoji, T., Yao, L., Fan, Y. Y., Rahman, M., Suzuki, T., Maeta, H., and Abe, Y. (2005b). Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 45, 860-866.
39. Lambert, C. M., Roy, M., Robitaille, G. A., Richard, D. E., and Bonnet, S. (2010) HIF-1 inhibition decreases systemic vascular remodeling diseases by promoting apoptosis through a hexokinase2-dependent mechanism. Cardiovasc. Res. (in press). Epub ahead of print. doi: 10.1093/cvr/cvq152.
40. Lassegue, B., and Griendling, K.K. (2010). NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb. Vasc. Biol. 653-661.
41. Laughner, E., Taghavi, P., Chiles, K., Mahon, P. C., and Semenza, G. L. (2001). HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21, 3995-4004.
42. Lauzier, M. C., Page, E. L., Michaud, M. D., and Richard, D. E. (2007). Differential regulation of hypoxia-inducible factor-1 through receptor tyrosine kinase transactivation in vascular smooth muscle cells. Endocrinology 148, 4023-4031.
43. Lee, S. B., Bae, I. H., Bae, Y. S., and Um, H. D. (2006). Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J. Biol. Chem. 281, 36228-36235.
44. Li, Y., and Trush, M. A. (1998). Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem. Biophys. Res. Commun. 253, 295-299.
45. Liliental, J., Moon, S. Y., Lesche, R., Mamillapalli, R., Li, D., Zheng, Y., Sun, H., and Wu, H. (2000). Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr. Biol. 10, 401-404.
46. Lyle, A. N., and Griendling, K. K. (2006). Modulation of vascular smooth muscle signaling by reactive oxygen species. Physiology 21, 269-280.
47. Masson, N., Willam, C., Maxwell, P. H., Pugh, C. W., and Ratcliffe, P. J. (2001). Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 20, 5197-5206.
48. Michaud, M. D., Robitaille, G. A., Gratton, J. P., and Richard, D. E. (2009). Sphingosine-1-phosphate: a novel nonhypoxic activator of hypoxia-inducible factor-1 in vascular cells. Arterioscler. Thromb. Vasc. Biol. 29, 902-908.
49. Modlinger, P., et al. (2006). RNA silencing in vivo reveals role of p22phox in rat angiotensin slow pressor response. Hypertension 47, 238-244.
50. Nozoe, M., Hirooka, Y., Koga, Y., Araki, S., Konno, S., Kishi, T., Ide, T., and Sunagawa, K. (2008). Mitochondria-derived reactive oxygen species mediate sympathoexcitation induced by angiotensin II in the rostral ventrolateral medulla. J. Hypertens. 26, 2176-2184.
51. Osada-Oka, M., Ikeda, T., Akiba, S., and Sato, T. (2008). Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1alpha-dependent expression of thrombospondin-1. J. Cell. Biochem. 104, 1918-1926.
52. Owens, G. K., Loeb, A., Gordon, D., and Thompson, M. M. (1986). Expression of smooth muscle-specific alpha-isoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation. J. Cell Biol. 102, 343-352.
53. Page, E. L., Chan, D. A., Giaccia, A. J., Levine, M., and Richard, D. E. (2008). Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol. Biol. Cell 19, 86-94.
54. Page, E. L., Robitaille, G. A., Pouyssegur, J., and Richard, D. E. (2002). Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J. Biol. Chem. 277, 48403-48409.
55. Queval, G., and Noctor, G. (2007). A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: Application to redox profiling during Arabidopsis rosette development. Anal. Biochem. 363, 58-69.
56. Rhee, S. G. (2006). Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883.
57. Richard, D. E., Berra, E., Gothie, E., Roux, D., and Pouyssegur, J. (1999). p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274, 32631-32638.
58. Richard, D. E., Berra, E., and Pouyssegur, J. (2000). Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J. Biol. Chem. 26765-26771.
59. Robinson, K. M., Janes, M. S., and Beckman, J. S. (2008). The selective detection of mitochondrial superoxide by live cell imaging. Nat. Protoc. 3, 941-947.
60. San Martin, A., and Griendling, K. K. (2010). Redox control of vascular smooth muscle migration. Antioxid. Redox Signal. 12, 625-640.
61. Sanjuan-Pla, A., Cervera, A. M., Apostolova, N., Garcia-Bou, R., Victor, V. M., Murphy, M. P., and McCreath, K. J. (2005). A targeted antioxidant reveals the importance of mitochondrial reactive oxygen species in the hypoxic signaling of HIF-1alpha. FEBS Lett. 579, 2669-2674.
62. Schofield, C. J., and Ratcliffe, P. J. (2004). Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354.
63. Semenza, G. L. (2003). Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732.
64. Skulachev, V. P., et al. (2009). An attempt to prevent senescence: a mitochondrial approach. Biochim. Biophys. Acta 1787, 437-461.
65. Smith, R. A., et al. (2008). Mitochondria-targeted antioxidants in the treatment of disease. Ann. NY Acad. Sci. 1147, 105-111.
66. Sorescu, D., Somers, M. J., Lassegue, B., Grant, S., Harrison, D. G., and Griendling, K. K. (2001). Electron spin resonance characterization of the NAD(P)H oxidase in vascular smooth muscle cells. Free Radic. Biol. Med. 30, 603-612.
67. Sun, H., King, A. J., Diaz, H. B., and Marshall, M. S. (2000). Regulation of the protein kinase Raf-1 by oncogenic Ras through phosphatidylinositol 3-kinase, Cdc42/Rac and Pak. Curr. Biol. 10, 281-284.
68. ten Freyhaus, H., Huntgeburth, M., Wingler, K., Schnitker, J., Baumer, A. T., Vantler, M., Bekhite, M. M., Wartenberg, M., Sauer, H., and Rosenkranz, S. (2006). Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc. Res. 71, 331-341.
69. Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344.
70. Ushio-Fukai, M., Zafari, A. M., Fukui, T., Ishizaka, N., and Griendling, K. K. (1996). p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J. Biol. Chem. 271, 23317-23321.
71. Varela, D., Simon, F., Riveros, A., Jorgensen, F., and Stutzin, A. (2004). NAD(P)H oxidase-derived H(2)O(2) signals chloride channel activation in cell volume regulation and cell proliferation. J. Biol. Chem. 279, 13301-13304.
72. Xi, X. P., Graf, K., Goetze, S., Fleck, E., Hsueh, W. A., and Law, R. E. (1999). Central role of the MAPK pathway in ang II-mediated DNA synthesis and migration in rat vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 19, 73-82.
73. Yoshida, K., Kirito, K., Yongzhen, H., Ozawa, K., Kaushansky, K., and Komatsu, N. (2008). Thrombopoietin (TPO) regulates HIF-1alpha levels through generation of mitochondrial reactive oxygen species. Int. J. Hematol. 88, 43-51.
74. 2 in angiotensin II-induced vascular hypertrophy. Hypertension 32, 488-495.
75. Zhang, G. X., Lu, X. M., Kimura, S., and Nishiyama, A. (2007). Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation. Cardiovasc. Res. 76, 204-212.