Multiplicity of hypoxia-inducible transcription factors and their connection to the circadian clock in the zebrafish

Physiological and Biochemical Zoology

Volumn 88, Issue 2, 2015, Pages 137-145

  Pelster, Bernd ^a   Egg, Margit ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCADIAN RHYTHM; COEVOLUTION; ENVIRONMENTAL STRESS; FISH; GENE EXPRESSION; GERM CELL; HYPOXIA; MORTALITY; POPULATION GENETICS; PROTEIN; RNA; SIGNALING;

ANIMALIA; DANIO RERIO; MAMMALIA; VERTEBRATA;

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOPROTEIN; MESSENGER RNA; ZEBRAFISH PROTEIN;

ANIMAL; CIRCADIAN RHYTHM; GENETICS; LARVA; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LARVA; PROTEIN ISOFORMS; RNA, MESSENGER; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84988822564     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/679751     Document Type: Article

References (104)

1. Ameln H., T. Gustafsson, C.J. Sundberg, K. Okamoto, E. Jansson, L. Poellinger, and Y. Makino. 2005. Physiological activation of hypoxia inducible factor-1 in human skeletal muscle. FASEB J 19:1009–1011.
2. Bass J. 2012. Circadian topology of metabolism. Nature 491: 348–356.
3. Benita Y., H. Kikuchi, A.D. Smith, M.Q. Zhang, D.C. Chung, and R.J. Xavier. 2009. An integrative genomics approach identifies hypoxia inducible factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37:4587–4602.
4. Bersten D.C., A.E. Sullivan, D.J. Peet, and M.L. Whitelaw. 2013. bHLH-PAS proteins in cancer. Nat Rev Cancer 13: 827–841.
5. Bosco G., A. Ionadi, S. Panico, F. Faralli, R. Gagliardi, P. Data, and J.P. Mortola. 2003. Effects of hypoxia on the circadian patterns in men. High Alt Med Biol 4:305–318.
6. Bozek K., A. Relogio, S.M. Kielbasa, M. Heine, C. Dame, A. Kramer, and H. Herzel. 2009. Regulation of clock-controlled genes in mammals. PLoS ONE 4:e4882.
7. Burggren W.W. and A.W. Pinder. 1991. Ontogeny of cardiovascular and respiratory physiology in lower vertebrates. Annu Rev Physiol 53:107–135.
8. Carrero P., K. Okamoto, P. Coumailleau, S. O’Brien, H. Tanaka, and L. Poellinger. 2000. Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1a. Mol Cell Biol 20:402–415.
9. Chilov D., T. Hofer, C. Bauer, R.H. Wenger, and M. Gassmann. 2001. Hypoxia affects expression of circadian genes PER1 and CLOCK in mouse brain. FASEB J 15:2613–2622.
10. Compernolle V., K. Brusselmans, T. Acker, P. Hoet, M. Tjwa, H. Beck, S. Plaisance, et al. 2002. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8:702–710.
11. Coste O., M. Beaumont, D. Batejat, P.V. Beers, and Y. Touitou. 2004. Prolonged mild hypoxia modifies human circadian core body temperature and may be associated with sleep disturbances. Chronobiol Int 21:419–433.
12. Doherty C.J. and S.A. Kay. 2010. Circadian control of global gene expression patterns. Annu Rev Genet 44:419–444.
13. Eckel-Mahan K. and P. Sassone-Corsi. 2013. Metabolism and the circadian clock converge. Physiol Rev 93:107–135.
14. Eckel-Mahan K.L., V.R. Patel, R.P. Mohney, K.S. Vignola, P. Baldi, and P. Sassone-Corsi. 2012. Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 109:5541–5546.
15. Edgar R.S., E.W. Green, Y. Zhao, G. van Ooijen, M. Olmedo, X. Qin, Y. Xu, et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464.
16. Egg M., L. Köblitz, J. Hirayama, T. Schwerte, C. Folterbauer, A. Kurz, B. Fiechtner, M. Möst, W. Salvenmoser, P. Sassone-Corsi, and B. Pelster. 2013. Linking oxygen to time: the bidirectional interaction between the hypoxic signaling pathway and the circadian clock. Chronobiol Int 30:510–529.
17. Egg M., M. Paulitsch, Y. Ennemoser, A. Wüstenhagen, T. Schwerte, A.M. Sandbichler, B. Fiechtner, L. Köblitz, C. Prem, and B. Pelster. 2014. Chronodisruption increases cardiovascular risk in zebrafish via reduced clearance of senescent erythrocytes. Chronobiol Int 31:680–689.
18. Ema M., K. Hirota, J. Mimura, H. Abe, J. Yodoi, K. Sogawa, L. Poellinger, and Y. Fujii-Kuriyama. 1999. Molecular mechanisms of transcription activation by HLF and HIF1α in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 18:1905–1914.
19. Fink T., A. Kazlauskas, L. Poellinger, P. Ebbesen, and V. Zachar. 2002. Identification of a tightly regulated hypoxia-response element in the promoter of human plasminogen activator inhibitor-1. Blood 99:2077–2083.
20. Forristal C.E., K.L. Wright, N.A. Hanley, R.O.C. Oreffo, and F.D. Houghton. 2010. Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139:85–97.
21. Freyssenet D. 2007. Energy sensing and regulation of gene expression in skeletal muscle. J Appl Physiol 102:529–540.
22. Fujita S., Y. Koyama, M. Higashimoto, K. Ono, T. Ono, K. Watanabe, N. Yoshimoto, et al. 2010. Regulation of circadian rhythm of human vascular endothelial growth factor by circadian rhythm of hypoxia inducible factor-1: implication for clinical use as anti-angiogenic therapy. Ann Cancer Res Ther 18:28–36.
23. Ghorbel M.T., J.M. Coulson, and D. Murphy. 2003. Cross-talk between hypoxic and circadian pathways: cooperative roles for hypoxia-inducible factor 1a and CLOCK in transcriptional activation of the vasopressin gene. Mol Cell Neurosci 22:396–404.
24. Gustafsson T., A. Puntschart, L. Kaijser, E. Jansson, and C.J. Sundberg. 1999. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol 276:H679–H685.
25. Hara S., J. Hamada, C. Kobayashi, Y. Kondo, and N. Imura. 2001. Expression and characterization of hypoxia-inducible factor (HIF)-3α in human kidney: suppression of HIF-mediated gene expression by HIF-3α. Biochem Biophys Res Commun 287:808–813.
26. Heikkilä M., A. Pasanen, K. Kivirikko, and J. Myllyharju. 2011. Roles of the human hypoxia-inducible factor (HIF)-3a variants in the hypoxia response. Cell Mol Life Sci 68:3885–3901.
27. Hirayama J., S. Cho, and P. Sassone-Corsi. 2007. Circadian control by the reduction/oxidation pathway: catalase represses light-dependent clock gene expression in the zebrafish. Proc Natl Acad Sci 104:15747–15752.
28. Hogenesch J.B., Y. Gu, S. Jain, and C.A. Bradfield. 1998. The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc Natl Acad Sci USA 95:5474–5479.
29. Hu C.-J., L.-Y. Wang, L.A. Chodosh, B. Keith, and C. Simom. 2003. Differential roles of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in hypoxic gene regulation. Mol Cell Biol 23:9361–9374.
30. Husa M., R. Liu-Bryan, and R. Terkeltaub. 2010. Shifting HIFs in osteoarthritis. Nat Med 16:641–644.
31. Idda M.L., C. Bertolucci, D. Vallone, Y. Gothilf, F.J. Sanchez-Vazquez, and N.S. Foulkes. 2012. Circadian clocks: lessons from fish. Prog Brain Res 199:41–57.
32. Iyer N.V., L.E. Kotch, F. Agani, S.W. Leung, E. Laughner, R.H. Wenger, M. Gassmann, J.D. Gearhart, A.M. Lawler, A.Y. Yu, and G.L. Semenza. 1998. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor1α. Genes Develop 12:149–162.
33. Jacob E., M. Drexel, T. Schwerte, and B. Pelster. 2002. The influence of hypoxia and of hypoxemia on the development of cardiac activity in zebrafish larvae. Am J Physiol 283: R911–R917.
34. Jensen L.D., Z. Cao, M. Nakamura, Y. Yang, L. Bräutigam, P. Andersson, Y. Zhang, E. Wahlberg, T. Länne, K. Hosaka, and Y. Cao. 2012. Opposing effects of circadian clock genes Bmal1 and Period2 in regulation of VEGF-dependent angiogenesis in developing zebrafish. Cell Rep 2:231–241.
35. Kaelin J. and P.J. Ratcliffe. 2008. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402.
36. Kajimura S., K. Aida, and C. Duan. 2006. Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Mol Cell Biol 26:1142–1155.
37. Keith B. and M.C. Simon. 2007. Hypoxia-inducible factors, stem cells, and cancer. Cell 129:465–472.
38. Kimura H., A. Weisz, T. Ogura, Y. Hitomi, Y. Kurashima, K. Hashimoto, F. D’Acquisto, M. Makuuchi, and H. Esumi. 2001. Identification of hypoxia-inducible factor 1 ancillary sequence and its function in vascular endothelial growth factor gene induction by hypoxia and nitric oxide. J Biol Chem 276: 2292–2298.
39. Kopp R., L. Köblitz, M. Egg, and B. Pelster. 2011. HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably. Physiol Genomics 43:506–516.
40. Kopp R., T. Schwerte, M. Egg, A.M. Sandbichler, B. Egger, and B. Pelster. 2010. Chronic reduction in cardiac output induces hypoxic signaling in larval zebrafish even at a time when convective oxygen transport is not required. Physiol Genomics 42A:8–23.
41. Kotch L.E., N.V. Iyer, E. Laughner, and G.L. Semenza. 1999. Defective vascularization of HIF-1a-null embryos is not associated with vegf deficiency but with mesenchymal cell death. Dev Biol 209:254–267.
42. Lai J.C.C., I. Kakuta, H.O.L. Mok, J.L. Rummer, and D. Randall. 2006. Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. J Exp Biol 209:2734–2738.
43. Law S.H.W., R.S.S. Wu, P.K.S. Ng, R.M.K. Yu, and R.Y.C. Kong. 2006. Cloning and expression analysis of two distinct HIF-alpha isoforms—gcHIF-1alpha and gcHIF-4alpha— from the hypoxia-tolerant grass carp, Ctenopharyngodon idellus.BMC Mol Biol 7:15.
44. Lee P., K. Goishi, A.J. Davidson, R. Mannix, L.I. Zon, and M. Klagsbrun. 2002. Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc Natl Acad Sci USA 99:10470–10475.
45. Loenarz C., M.L. Coleman, A. Boleininger, B. Schierwater, P.W.H. Holland, P.J. Ratcliffe, and C.J. Schofield. 2011. The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal,Trichoplax adhaerens.EMBO Rep 12:63–70.
46. Loudon A.S.I. 2012. Circadian biology: a 2.5 billion year old clock. Curr Biol 22:R570–R571.
47. Lundby C., M. Gassmann, and H. Pilegaard. 2006. Regular endurance training reduces the exercise induced HIF-1a and HIF-2a mRNA expression in human skeletal muscle in normoxic conditions. Eur J Appl Physiol 96:363–369.
48. Maltepe E., J.V. Schmidt, D. Baunoch, C.A. Bradfield, and M.C. Simon. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403–407.
49. Maynard M.A., A.J. Evans, T. Hosomi, S. Hara, M.A.S. Jewett, and M. Ohh. 2005. Human HIF-3α4 is a dominant-negative regulator of HIF-1 and is down-regulated in renal cell carcinoma. FASEB J 19:1396–1406.
50. Maynard M.A., H. Qi, J. Chung, E.H.L. Lee, Y. Kondo, S. Hara, R.C. Conaway, J.W. Conaway, and M. Ohh. 2003. Multiple splice variants of the human HIF-3α locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 278:11032–11040.
51. Montminy M.R., K.A. Sevarino, J.A. Wagner, G. Mandel, and R.H. Goodman. 1986. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci USA 83:6682–6686.
52. Mortola J.P. 2007. Hypoxia and circadian patterns. Respir Physiol Neurobiol 158:274–279.
53. Munoz E., M. Brewer, and R. Baler. 2002. Circadian transcription: thinking outside the E-box. J Biol Chem 277: 36009–36017.
54. Nikinmaa M. and B.B. Rees. 2005. Oxygen-dependent gene expression in fish. Am J Physiol 288:R1079–R1090.
55. O’Neill J.S. and A.B. Reddy. 2011. Circadian clocks in human red blood cells. Nature 469:498–504.
56. O’Neill J.S., G. van Ooijen, L.E. Dixon, C. Troein, F. Corellou, F.-Y. Bouget, A.B. Reddy, and A.J. Millar. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–558.
57. Padilla P.A. and M.B. Roth. 2001. Oxygen deprivation causes suspended animation in the zebrafish embryo. Proc Natl Acad Sci USA 98:7331–7335.
58. Pasanen A., M. Heikkilä, K. Rautavuoma, M. Hirsilä, K.I. Kivirikko, and J. Myllyharju. 2010. Hypoxia-inducible factor (HIF)-3α is subject to extensive alternative splicing in human tissues and cancer cells and is regulated by HIF-1 but not HIF-2. Int J Biochem Cell Biol 42:1189–1200.
59. Peek C.B., A.H. Affinati, K.M. Ramsey, H.Y. Kuo, W. Yu, L.A. Sena, O. Ilkayeva, et al. 2013. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342. doi:10.1126/science.1243417.
60. Pelster B. 1999. Environmental influences on the development of the cardiac system in fish and amphibians. Comp Biochem Physiol A 124:407–412.
61. Pelster B. and B. Bagatto. 2010. Respiration. Pp. 290–309 in S.F. Perry, M. Ekker, A.P. Farrell, and C.J. Brauner, eds. Zebrafish. Academic Press, Amsterdam.
62. Pelster B. and W.W. Burggren. 1996. Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio). Circ Res 79:358–362.
63. Prabhakar N.R. and G.L. Semenza. 2012. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev 92:967–1003.
64. Rahman M. and P. Thomas. 2007. Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1α and HIF-2α, in a hypoxia-tolerant marine teleost, Atlantic croaker(Micropogonias undulatus). Gene 396:273–282.
65. Randall D. 1982. The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100:275–288.
66. Rey G. and A.B. Reddy. 2013. Rhythmic respiration. Science 342:570–571.
67. Richards J.G. 2009. Metabolic and molecular responses of fish to hypoxia. Pages 443–485 in J.G. Richards, A.P. Farrell, and C.J. Brauner, eds. Hypoxia. Elsevier, Amsterdam.
68. Rimoldi S., G. Terova, P. Ceccuzzi, S. Marelli, M. Antonini, and M. Saroglia. 2012. HIF-1a mRNA levels in Eurasian perch (Perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep 39:4009–4015.
69. Rissanen E., H.K. Tranberg, and M. Nikinmaa. 2006. Oxygen availability regulates metabolism and gene expression in trout hepatocyte cultures. Am J Physiol 291:R1507–R1515.
70. Rojas D.A., D.A. Perez-Munizaga, L. Centanin, M. Antonelli, P. Wappner, M.L. Allende, and A.E. Reyes. 2007. Cloning of hif-1α and hif-2α and mRNA expression pattern during development in zebrafish. Gene Expr Patterns 7:339–345.
71. Rombough P. and H. Drader. 2009. Hemoglobin enhances oxygen uptake in larval zebrafish (Danio rerio) but only under conditions of extreme hypoxia. J Exp Biol 212:778–784.
72. Rytkönen K.T., A. Akbarzadeh, H.K. Miandare, H. Kamei, C. Duan, E.H. Leder, T.A. Williams, and M. Nikinmaa. 2013. Subfunctionalization of cyprinid hypoxia-inducible factors for roles in development and oxygen sensing. Evolution 67: 873–882.
73. Rytkönen K.T., J.M. Prokkola, V. Salonen, and M. Nikinmaa. 2014. Transcriptional divergence of the duplicated hypoxia-inducible factor alpha genes in zebrafish. Gene 541:60–66.
74. Rytkönen K.T. and J.F. Storz. 2011. Evolutionary origins of oxygen sensing in animals. EMBO Rep 12:3–4.
75. Rytkönen K.T., T.A. Williams, G.M. Renshaw, C.R. Primmer, and M. Nikinmaa. 2011. Molecular evolution of the metazoan PHD-HIF oxygen-sensing system. Mol Biol Evol 28: 1913–1926.
76. Santhakumar K., E.C. Judson, P.M. Elks, S. McKee, S. Elworthy, E. van Rooijen, S.S. Walmsley, S. Renshaw, S.S. Cross, and F.J. van Eeden. 2012. A zebrafish model to study and therapeutically manipulate hypoxia signaling in tumorigenesis. Cancer Res 72:4017–4027.
77. Schödel J., S. Oikonomopoulos, J. Ragoussis, C.W. Pugh, P.J. Ratcliffe, and D.R. Mole. 2011. High-resolution genomewide mapping of HIF-binding sites by ChIP-seq. Blood 117: e207–e217.
78. Seifert E.L. and J.P. Mortola. 2002. Circadian pattern of ventilation during prolonged hypoxia in conscious rats. Respir Physiol Neurobiol 133:23–34.
79. Semenza G.L. 2001. HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 13:167–171.
80. Semenza G.L. 2003. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3:721–732.
81. Semenza G.L. 2009. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24:97–106.
82. Semenza G.L. 2010a. HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20:51–56.
83. Semenza G.L. 2010b. Oxygen homeostasis. WIREs Syst Biol Med 2: 336–361.
84. Semenza G.L. 2012. Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408.
85. Semenza G.L. 2014. Hypoxia-inducible factor 1 and cardiovascular disease. Annu Rev Physiol 76:39–56.
86. Semenza G.L. and G.L. Wang. 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.
87. Shams I., A. Avivi, and E. Nevo. 2004. Hypoxic stress tolerance of the blind subterranean mole rat: expression of erythropoietin and hypoxia-inducible factor 1a. Proc Natl Acad Sci USA 101:9698–9703.
88. Shams I., E. Nevo, and A. Avivi. 2005. Ontogenetic expression of erythropoietin and hypoxia-inducible factor-1 alpha genes in subterranean blind mole rats. FASEB J 19:307–309.
89. Shen R.J., X.Y. Jiang, J.W. Pu, and S.M. Zou. 2010. HIF-1a and -2a genes in a hypoxia-sensitive teleost species Megalobrama amblycephala: cDNA cloning, expression and different responses to hypoxia. Comp Biochem Physiol B 157:273–280.
90. Sherman H. and O. Froy. 2008. Expression of human β-defensin 1 is regulated via c-Myc and the biological clock. Mol Immunol 45:3163–3167.
91. Soitamo A.J., C.M.I. Rabergh, M. Gassmann, L. Sistonen, and M. Nikinmaa. 2001. Characterization of a hypoxia-inducible factor (HIF-1a) from rainbow trout. J Biol Chem 276: 19699–19705.
92. Sollid J., E. Rissanen, H. Tranberg, T. Thorstensen, K. Vuori, M. Nikinmaa, and G.E. Nilsson. 2006. HIF-1 and iNOS levels in crucian carp gills during hypoxia-induced transformation. J Comp Physiol B 176:359–369.
93. Takahata S., K. Sogawa, A. Kobayashi, M. Ema, J. Mimura, N. Ozaki, and Y. Fujii-Kuriyama. 1998. Transcriptionally active heterodimer formation of an Arnt-like PAS protein, Arnt3, with HIF-1a, HLF, and clock. Biochem Biophys Res Commun 248:789–794.
94. Taniguchi C.M., E.C. Finger, A.J. Krieg, C. Wu, A.N. Diep, E.L. LaGory, K. Wei, et al. 2013. Cross-talk between hypoxia and insulin signaling through Phd3 regulates hepatic glucose and lipid metabolism and ameliorates diabetes. Nat Med 19:1325–1330.
95. Terova G., S. Rimoldi, S. Cora, G. Bernardini, R. Gornati, and M. Saroglia. 2008. Acute and chronic hypoxia affects HIF-1a mRNA levels in sea bass (Dicentrarchus labrax).Aquaculture 279:150–159.
96. Touitou Y., O. Coste, G. Dispersyn, and L. Pain. 2010. Disruption of the circadian system by environmental factors: effects of hypoxia, magnetic fields and general anesthetics agents. Adv Drug Deliv Rev 62:928–945.
97. van Ginneken V. and G. van den Thillart. 2009. Metabolic depression in fish measured by direct calorimetry: a review. Thermochim Acta 483:1–7.
98. Vatine G., D. Vallone, L. Appelbaum, P. Mracek, Z. Ben-Moshe, K. Lahiri, Y. Gothilf, and N.S. Foulkes. 2009. Light directs zebrafish period2 expression via conserved D and E boxes. PLoS Biol 7:e1000223.
99. Vatine G., D. Vallone, Y. Gothilf, and N.S. Foulkes. 2011. It’s time to swim! zebrafish and the circadian clock. FEBS Lett 585:1485–1494.
100. Wenger R.H., D.P. Stiehl, and G. Camenisch. 2005. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005:re12.
101. Xia X. and A. Kung. 2009. Preferential binding of HIF-1 to transcriptionally active loci determines cell-type specific response to hypoxia. Genome Biol 10:R113.
102. Zhang P., L. Lu, Q. Yao, Y. Li, J. Zhou, Y. Liu, and C. Duan. 2012. Molecular, functional, and gene expression analysis of zebrafish hypoxia-inducible factor-3a. Am J Physiol 303: R1165–R1174.
103. Zhang P., Q. Yao, L. Lu, Y. Li, P.J. Chen, and C. Duan. 2014. Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep 6:1110–1121.
104. Zhang R., N.F. Lahens, H.I. Ballance, M.E. Hughes, and J.B. Hogenesch. 2014. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci 111:16219–16224.