Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1

Biochemical Journal

Volumn 405, Issue 1, 2007, Pages 1-9

  Semenza, Gregg L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytochrome c oxidase (COX); Hypoxia inducible factor 1 (HIF 1); Mitochondrial respiratory chain; Oxidative phosphorylation; Reactive oxygen species (ROS); Tricarboxylic acid cycle

Indexed keywords

CYTOCHROME C OXIDASE (COX); HYPOXIA-INDUCIBLE FACTOR-1 (HIF-1); MITOCHONDRIAL RESPIRATORY CHAIN; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES (ROS); TRICARBOXYLIC ACID CYCLE;

CARBOXYLIC ACIDS; ENZYME ACTIVITY; GENE ENCODING; PHOSPHORYLATION; RESPIRATORY MECHANICS; TRANSCRIPTION FACTORS;

BIODIVERSITY;

ACETYL COENZYME A; CYCLOOXYGENASE 4; CYTOCHROME C OXIDASE; CYTOCHROME OXIDASE 4 1; CYTOCHROME OXIDASE 4 2; ENDOPEPTIDASE LA; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE REDUCTASE; HYPOXIA INDUCIBLE FACTOR 1; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 5; MITOCHONDRIAL ENZYME; OXYGEN; PROTEIN SUBUNIT; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 1; PYRUVATE KINASE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRICARBOXYLIC ACID; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ADAPTATION; CELL METABOLISM; CITRIC ACID CYCLE; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ENZYME SUBUNIT; EUKARYOTE; HUMAN; MAMMAL CELL; METAZOON; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SURVIVAL; YEAST CELL;

CELL RESPIRATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOLYSIS; HOMEOSTASIS; HYPOXIA-INDUCIBLE FACTOR 1; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; OXYGEN; PROTEIN KINASES;

EUKARYOTA; MAMMALIA; METAZOA;

EID: 34347227058     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070389     Document Type: Review

References (109)

1. Falkowski, P. G. (2006) Tracing oxygen's imprint on Earth's metabolic evolution. Science 311, 1724-1725
2. Manalo, D. J., Rowan, A., Lavoie, T., Natarajan, L., Kelly, B. D., Ye, S. Q., Garcia, J. G. and Semenza, G. L. (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105, 659-669
3. Elvidge, G. P., Glenny, L., Appelhoff, R. J., Ratcliffe, P. J., Ragoussis, J. and Gleadle, J. M. (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1α, HIF-2α, and other pathways. J Biol. Chem. 281, 15215-15226
4. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12, 149-162
5. Ryan, H. E., Lo, J. and Johnson, R. S. (1998) HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17, 3005-3015
6. Carmeliet, P., Dor, Y., Herbert, J. M., Fukumura, D., Brusselmans, K., Dewerchin, M., Neeman, M., Bono, F., Abramovitch, R., Maxwell, P. et al. (1998) Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 394, 485-490
7. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A. 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
8. Bishop, T., Lau, K. W., Epstein, A. C., Kim, S. K., Jiang, M., O'Rourke, D., Pugh, C. W., Gleadle, J. M., Taylor, M. S., Hodgkin, J. and Ratcliffe, P. J. (2004) Genetic analysis of pathways regulated by the von Hippel-Lindau tumor suppressor in Caenorhabditis elegans. PLoS Biol. 2, e289
9. 2 tension. Am. J. Physiol. 271, C1172-C1180
10. Salceda, S. and Caro, J. (1997) Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642-22647
11. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 7987-7992
12. Jewell, U. R., Kvietikova, I., Scheid, A., Bauer, C., Wenger, R. H. and Gassmann, M. (2001) Induction of HIF-1α in response to hypoxia is instantaneous. FASEB J. 15, 1312-1314
13. Bruick, R. K. and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340
14. 2 sensing. Science 292, 464-468
15. 2-regulated prolyl hydroxylation. Science 292, 468-472
16. Yu, F., White, S. B., Zhao, Q. and Lee, F. S. (2001) HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. U.S.A. 98, 9630-9635
17. 2 sensing. J. Biol. Chem. 275, 25130-25138
18. 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
19. Mansfield, K. D., Guzy, R. D., Pan, Y., Young, R. M., Cash, T. P., Schumacker, P. T. and Simon, M. C. (2005) Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-α activation. Cell Metab. 1, 393-399
20. Hagen, T., Taylor, C. T., Lam, F. and Moncada, S. (2003) Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF-1α. Science 302, 1975-1978
21. Mahon, P. C., Hirota, K. and Semenza, G. L. (2001) FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15, 2675-2686
22. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L. and Bruick, R. K. (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471
23. McNeill, L. A., Hewitson, K. S., Claridge, T. D., Seibel, J. F., Horsfall, L. E. and Schofield, C. J. (2002) Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the β-carbon of asparagine-803. Biochem. J. 367, 571-575
24. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J. and Whitelaw, M. L. (2002) Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295, 858-861
25. Seagroves, T. N., Ryan, H. E., Lu, H., Wouters, B. G., Knapp, M., Thibault, P., Laderoute, K. and Johnson, R. S. (2001) Transcription factor HIF-1 is a necessary mediator ot the Pasteur effect in mammalian cells. Mol. Cell. Biol. 21, 3436-3444
26. Cramer, T., Yamanishi, Y., Clausen, B. E., Forster, I., Pawlinski, R., Mackman, N., Haase, V. H., Jaenisch, R., Corr, M., Nizet, V. et al. (2003) HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112, 645-657
27. Dang, C. V. and Semenza, G. L. (1999) Oncogenic alterations of metabolism. Trends Biochem. Sci. 24, 68-72
28. Discher, D. J., Bishopric, N. H., Wu, X., Peterson, C. A. and Webster, K. A. (1998) Hypoxia regulates β-enolase and pyruvate kinase-M promoters by modulating Sp1/Sp3 binding to a conserved GC element. J. Biol. Chem. 273, 26087-26093
29. Almeida, A., Moncada, S. and Bolaños, J. P. (2004) Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2- kinase pathway. Nat. Cell Biol. 6, 45-51
30. Webster, K. A., Gunning, P., Hardeman, E., Wallace, D. C. and Kedes, L. (1990) Coordinate reciprocal trends in glycolytic and mitochondrial transcript accumulations during the in vitro differentiation of human myoblasts. J. Cell. Physiol. 142, 566-573
31. Kim, J.-W., Tchernyshyov, I., Semenza, G. L. and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185
32. Papandreou, I., Cairns, R. A., Fontana, L., Lim, A. L. and Denko, N. C. (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 3, 187-197
33. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinizawa-Itoh, K., Nakashima, R., Yaono, R. and Yoshikawa, S. (1995) The whole structure of the 13-subunit oxidized COX at 2 Å. Science 272, 1136-1144
34. Napiwotzki, J. and Kadenbach, B. (1998) Extramitochondrial ATP/ADP ratios regulate COX activity via binding to the cytosolic domain of subunit IV. Biol. Chem. 379, 335-339
35. Burke, P. V. and Poyton, R. O. (1998) Structure/function of oxygen-regulated isoforms in COX. J. Exp. Biol. 201, 1163-1175
36. Lowry, C. V. and Zitomer, R. S. (1984) Oxygen regulation of anaerobic and aerobic genes mediated by a common factor in yeast. Proc. Natl. Acad. Sci. U.S.A. 81, 6129-6133
37. Forsburg, S. L. and Guarente, L. (1989) Communication between mitochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Ann. Rev. Cell Biol. 5, 153-180
38. Kwast, K. E., Burke, P. V. and Poyton, R. O. (1998) Oxygen sensing and the transcriptional regulation of oxygen-responsive genes in yeast. J. Exp. Biol. 201, 1177-1195
39. Waterland, R. A., Basu, A., Chance, B. and Poyton, R. O. (1991) The isoforms of yeast COX alter the in vivo kinetic properties of the holoenzyme. J. Biol. Chem. 266, 4180-4186
40. Allen, L. A., Zhao, X.-J., Caughey, W. and Poyton, R. O. (1995) Isoforms of yeast COX subunit V affect the binuclear reaction center and alter the kinetics of interaction with the isoforms of yeast cytochrome c. J. Biol. Chem. 270, 110-118
41. Hutteman, M., Kadenbach, B. and Grossman, L. I. (2001) Mammalian subunit IV isoforms of COX. Gene 267, 111-123
42. Fukuda, R., Zhang, H., Kim, J.-w., Shimoda, L. A., Dang, C. V. and Semenza, G. L. (2007) Regulation of COX subunit composition by HIF-1: a mechanism for optimizing the efficiency of respiration in hypoxic cells. Cell 129, 111-122
43. Kelly, B. D., Hackett, S. F., Hirota, K., Oshima, Y., Cai, Z., Berg-Dixon, S., Rowan, A., Yan, Z., Campochiaro, P. A. and Semenza, G. L. (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ. Res. 93, 1074-1081
44. Prabhakar, N. R., Peng, Y. J., Yuan, G. and Kumar, G. K. (2006) Reactive oxygen species facilitate oxygen sensing. Novartis Found. Symp. 272, 95-99
45. -/- mice. Nat Genet. 35, 331-340
46. Krishnamurthy, P., Ross, D. D., Nakanishi, T., Bailey-Dell, K., Zhou, S., Mercer, K. E., Sarkadi, B., Sorrentino, B. P. and Schuetz, J. D. (2004) The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol. Chem. 279, 24218-24225
47. 1B-adrenergic receptor gene promoter region and hypoxia regulatory elements in vascular smooth muscle. Proc. Natl. Acad. Sci. U.S.A. 94, 9487-9492
48. Cormier-Regard, S., Nguyen, S. V. and Claycomb, W. C. (1998) Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273, 17787-17792
49. Chun, Y. S., Hyun, J. Y., Kwak, Y. G., Kim, I. S., Choi, E., Kim, M. S. and Park, J. W. (2003) Hypoxic activation of the atrial natriuretic peptide gene promoter through direct and indirect actions of hypoxia-inducible factor-1. Biochem. J. 370, 149-157
50. Wykoff, C. C., Pugh, C. W., Maxwell, P. H., Harris, A. L. and Ratcliffe, P. J. (2000) Identification of novel hypoxia dependent and independent target genes of the von Hippel-Lindau (VHL) tumor suppressor by mRNA differential expression profiling. Oncogene 19, 6297-6305
51. 2 integrin gene expression. Proc. Natl. Acad. Sci. U.S.A. 101, 10440-10445
52. Mukhopadhyay, C. K., Mazumder, B. and Fox, P. L. (2000) Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. J. Biol. Chem. 275, 21048-21054
53. Pennacchietti, S., Michieli, P., Galluzzo, M., Mazzone, M., Giordano, S. and Comoglio, P. M. (2003) Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 3, 347-361
54. Higgins, D. F., Biju, M. P., Akai, Y., Wutz, A., Johnson, R. S. and Haase, V. H. (2004) Hypoxic induction of Ctgf is directly mediated by HIF-1. Am. J. Physiol. 287, F1223-F1232
55. Kaidi, A., Qualtrough, D., Williams, A. C. and Paraskeva, C. (2006) Direct transcriptional up-regulation of cyclooxygenase-2 by hypoxia-inducible factor (HIF)-1 promotes colorectal tumor cell survival and enhances HIF-1 transcriptional activity during hypoxia. Cancer Res. 66, 6683-6691
56. Fradette, C. and du Souich, P. (2003) Hypoxia-inducible factor-1 and activator protein-1 modulate the upregulation of CYP3A6 induced by hypoxia. Br. J. Pharmacol. 140, 1146-1154
57. Schioppa, T., Uranchimeg, B., Saccani, A., Biswas, S. K., Doni, A., Rapisarda, A., Bernasconi, S., Saccani, S., Nebuloni, M., Vago, L., Mantovani, A. et al. (2003) Regulation of the chemokine receptor CXCR4 by hypoxia. J. Exp. Med. 198, 1391-1402
58. Staller, P., Sulitkova, J., Lisztwan, J., Moch, H., Oakeley, E. J. and Krek, W. (2003) Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumor suppressor pVHL. Nature 425, 307-311
59. Zagzag, D., Krishnamachary, B., Yee, H., Okuyama, H., Chiriboga, L., Ali, M. A., Melamed, J. and Semenza, G. L. (2005) Stromal cell-derived factor-1α and CXCR4 expression in hemangioblastoma and clear cell-renal cell carcinoma: von Hippel-Lindau loss-of-function induces expression of a ligand and its receptor. Cancer Res. 65, 6178-6188
60. Miyazaki, K., Kawamoto, T., Tanimoto, K., Nishiyama, M., Honda, H. and Kato, Y. (2002) Identification of functional hypoxia response elements in the promoter region of the DEC1 and DEC2 genes. J. Biol. Chem. 277, 47014-47021
61. Synnestvedt, K., Furuta, G. T., Comerford, K. M., Louis, N., Karhausen, J., Eltzschig, H. K., Hansen, K. R., Thompson, L. F. and Colgan, S. P. (2002) Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J. Clin. Invest. 110, 993-1002
62. LeCouter, J., Kowalski, J., Foster, J., Hass, P., Zhang, Z., Dillard-Telm, L., Frantz, G., Rangell, L., DeGuzman, L., Keller, G. A. et al. (2001) Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412, 877-884
63. Sanchez-Eisner, T., Botella, L. M., Velasco, B., Langa, C. and Bernabeu, C. (2002) Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-β pathways. J. Biol. Chem. 277, 43799-43808
64. Hu, J., Discher, D. J., Bishopric, N. H. and Webster, K. A. (1998) Hypoxia regulates expression of the endothelin-1 gene through a proximal hypoxia-inducible factor-1 binding site on the antisense strand. Biochem. Biophys. Res. Commun. 245, 894-899
65. Semenza, G. L., Jiang, B. H., Leung, S. W., Passantino, R., Concordet, J. P., Maire, P. and Giallongo, A. (1996) 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
66. Coulet, F., Nadaud, S., Agrapart, M. and Soubrier, F. (2003) Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J. Biol. Chem. 278, 46230-46240
67. Semenza, G. L. and Wang, G. L. (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454
68. Jiang, B.-H., Rue, E., Wang, G. L., Roe, R. and Semenza, G. L. (1996) Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271, 17771-17778
69. Oikawa, M., Abe, M., Kurosawa, H., Hida, W., Shirato, K. and Sato, Y. (2001) Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem. Biophys. Res. Commun. 289, 39-43
70. Wood, S. M., Wiesener, M. S., Yeates, K. M., Okada, N., Pugh, C. W., Maxwell, P. H. and Ratcliffe, P. J. (1998) Selection and analysis of a mutant cell line defective in the hypoxia-inducible factor-1 α-subunit (HIF-1 α). Characterization of HIF-1 α-dependent and -independent hypoxia-inducible gene expression. J. Biol. Chem. 273, 8360-8368
71. Graven, K. K., Yu, Q., Pan, D., Roncarati, J. S. and Farber, H. W. (1999) Identification of an oxygen responsive enhancer element in the glyceraldehyde-3-phosphate dehydrogenase gene. Biochim. Biophys. Acta 1447, 208-218
72. Lu, S., Gu, X., Hoestje, S. and Epner, D. E. (2002) Identification of an additional hypoxia responsive element in the glyceraldehyde-3-phosphate dehydrogenase gene promoter. Biochim. Biophys. Acta 1574, 152-156
73. Paris, S., Denis, H., Delaive, E., Dieu, M., Dumont, V., Ninane, N., Raes, M. and Michiels, C. (2005) Up-regulation of 94-kDa glucose-regulated protein by hypoxia-inducible factor-1 in human endothelial cells in response to hypoxia. FEBS Lett. 579, 105-114
74. Lee, P. J., Jiang, B. H., Chin, B. Y., Iyer, N. V., Alam, J., Semenza, G. L. and Choi, A. M. (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375-5381
75. Pescador, N., Cuevas, Y., Naranjo, S., Alcaide, M., Villar, D., Landazuri, M. O. and Del Peso, L. (2005) Identification of a functional hypoxia-responsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem. J. 390, 189-197
76. Metzen, E., Stiehl, D. P., Doege, K., Marxsen, J. H., Hellwig-Burgel, T. and Jelkmann, W. (2005) Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: identification of a functional hypoxia-responsive element. Biochem. J. 387, 711-717
77. Lee, M. J., Kim, J. Y., Suk, K. and Park, J. H. (2004) Identification of the hypoxia-inducible factor 1a-responsive HGTD-P gene as a mediator in the mitochondrial apoptotic pathway. Mol. Cell. Biol. 24, 3918-3927
78. Lofstedt, T., Jogi, A., Sigvardsson, M., Gradin, K., Poellinger, L., Pahlman, S. and Axelson, H. (2004) Induction of ID2 expression by hypoxia-inducible factor-1: a role in dedifferentiation of hypoxic neuroblastoma cells. J. Biol. Chem. 279, 39223-39231
79. Furuta, G. T., Turner, J. R., Taylor, C. T., Hershberg, R. M., Comerford, K., Narravula, S., Podolsky, D. K. and Colgan, S. P. (2001) Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193, 1027-1034
80. Lee, S. Y., Madan, A., Furuta, G. T., Colgan, S. P. and Sibley, E. (2002) Lactase gene transcription is activated in response to hypoxia in intestinal epithelial cells. Mol. Genet. Metab. 75, 65-69
81. Grosfeld, A., Andre, J., Hauguel-De Mouzon, S., Berra, E., Pouyssegur, J. and Guerre-Millo, M. (2002) Hypoxia-inducible factor 1 transactivates the human leptin gene promoter. J. Biol. Chem. 277, 42953-42957
82. Petrella, B. L., Lohi, J. and Brinckerhoff, C. E. (2005) Identification of membrane type-1 matrix metalloproteinase as a target of hypoxia-inducible factor-2α in von Hippel-Lindau renal cell carcinoma. Oncogene 24, 1043-1052
83. Reynolds, P. R., Mucenski, M. L., Le Cras, T. D., Nichols, W. C. and Whitsett, J. A. (2004) Midkine is regulated by hypoxia and causes pulmonary vascular remodeling. J. Biol. Chem. 279, 37124-37132
84. Ullah, M. S., Davies, A. J. and Halestrap, A. P. (2006) The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1α-dependent mechanism. J. Biol. Chem. 281, 9030-9037
85. Comerford, K. M., Wallace, T. J., Karhausen, J., Louis, N. A., Montalto, M. C. and Colgan, S. P. (2002) Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 62, 3387-3394
86. Piret, J. P., Minet, E., Cosse, J. P., Ninane, N., Debacq, C., Raes, M. and Michiels, C. (2005) Hypoxia-inducible factor-1-dependent overexpression of myeloid cell factor-1 protects hypoxic cells against tert-butyl hydroperoxide-induced apoptosis. J. Biol. Chem. 280, 9336-9344
87. Melillo, G., Musso, T., Sica, A., Taylor, L. S., Cox, G. W. and Varesio, L. (1995) A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182, 1683-1693
88. Bruick, R. K. (2000) Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. U.S.A. 97, 9082-9087
89. Kim, J. Y., Ahn, H. J., Ryu, J. H., Suk, K. and Park, J. H. (2004) BH3-only protein Noxa is a mediator of hypoxic cell death induced by hypoxia-inducible factor 1α. J. Exp. Med. 199, 113-124
90. Choi, J., Park, S., Kang, G., Liu, J. and Youn, H. (2004) Nur77 activated by hypoxia-inducible factor-1α overproduces proopiomelanocortin in von Hippel-Lindau-mutated renal cell carcinoma. Cancer Res. 64, 35-39
91. Bhattacharya, S., Michels, C. L., Leung, M. K., Arany, Z. P., Kung, A. L. and Livingston, D. M. (1999) Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev. 13, 64-75
92. Firth, J. D., Ebert, B. L., Pugh, C. W. and Ratcliffe, P. J. (1994) Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl. Acad. Sci. U.S.A. 91, 6496-6500
93. Minchenko, A., Leshchinsky, I., Opentanova, I., Sang, N., Srinivas, V., Armstead, V. and Caro, J. (2002) Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J. Biol. Chem. 277, 6183-6187
94. Fukasawa, M., Tsuchiya, T., Takayama, E., Shinomaya, N., Uyeda, K., Sakakibara, R. and Seki, S. (2004) Identification and characterization of the hypoxia-responsive element of the human placental 6-phosphofructo-2-kinase/ fructose-2,6-bisphosphatase gene. J. Biochem. (Tokyo) 136, 273-277
95. Minchenko, O., Opentanova, I. and Caro, J. (2003) Hypoxic regulation of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene family (PFKFB-1-4) expression in vivo. FEBS Lett. 554, 264-270
96. Kietzmann, T., Roth, U. and Jungermann, K. (1999) Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes. Blood 94, 4177-4185
97. Takahashi, Y., Takahashi, S., Shiga, Y., Yoshimi, T. and Miura, T. (2000) Hypoxic induction of prolyl 4-hydroxylase α(I) in cultured cells. J. Biol. Chem. 275, 14139-14146
98. Miki, N., Ikuta, M. and Matsui, T. (2004) Hypoxia-induced activation of the retinoic acid receptor-related orphan receptor α4 gene by an interaction between hypoxia-inducible factor-1 and Sp1 J. Biol. Chem. 279, 15025-15031
99. Chauvet, C., Bois-Joyeux, B., Berra, E., Pouyssegur, J. and Danan, J. L. (2004) The gene encoding human retinoic acid-receptor-related orphan receptor α is a target for hypoxia-inducible factor 1. Biochem. J. 384, 79-85
100. Amano, H., Maruyama, K., Naka, M. and Tanaka, T. (2003) Target validation in hypoxia-induced vascular remodeling using transcriptome/metabolome analysis. Pharmacogenomics J. 3, 183-188
101. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P. and Gurtner, G. C. (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-864
102. Nishi, H., Nakada, T., Kyo, S., Inoue, M., Shay, J. W. and Isaka, K. (2004) Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol. Cell. Biol. 24, 6076-6083
103. Rolfs, A., Kvietikova, I., Gassmann, M. and Wenger, R. H. (1997) Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J. Biol. Chem. 272, 20055-20062
104. Lok, C. N. and Ponka, P. (1999) Identification of a hypoxia response element in the transferrin receptor gene. J. Biol. Chem. 274, 24147-24152
105. Tacchini, L., Fusar-Poli, D., Bernelli-Zazzera, A. and Cairo, G. (2002) Transferrin receptor gene expression and transferrin-bound iron uptake are increased during postischemic rat liver reperfusion. Hepatology 36, 103-111
106. Caniggia, I., Mostachfi, H., Winter, J., Gassmann, M., Lye, S. J., Kuliszewski, M. and Post, M. (2000) Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGF-β3. J. Clin. Invest. 105, 577-587
107. Forsythe, J. A., Jiang, B.-H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613
108. Gerber, H. P., Condorelli, F., Park, J. and Ferrara, N. (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272, 23659-23667
109. Okuyama, H., Krishnamachary, B., Zhou, Y. F., Nagasawa, H., Bosch-Marce, M. and Semenza, G. L. (2006) Expression of vascular endothelial growth factor receptor 1 in bone marrow-derived mesenchymal cells is dependent on hypoxia-inducible factor 1. J. Biol. Chem. 281, 15554-15563