HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably

Physiological Genomics

Volumn 43, Issue 9, 2011, Pages 506-516

  Kopp, Renate ^a   Köblitz, Louise ^a   Egg, Margit ^a   Pelster, Bernd ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Environmental adaptation; Hypoxia inducible factor; Hypoxic signaling; Metabolism; Muscle tissue; Ontogeny; Zebrafish

Indexed keywords

COMPLEMENTARY DNA; CYTOCHROME C OXIDASE; ERYTHROPOIETIN; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; MESSENGER RNA; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 2; SUCCINATE DEHYDROGENASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; VASCULOTROPIN 121; VASCULOTROPIN 165; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXERCISE; GENE EXPRESSION; HYPOXIA; IMMUNOBLOTTING; LARVA; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ZEBRA FISH;

ANIMALIA; DANIO RERIO;

EID: 79956315689     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00250.2010     Document Type: Article

References (79)

1. Adams V, Linke A, Krankel N, Erbs S, Gielen S, Mobius-Winkler S, Gummert J.F, Mohr F.W, Schuler G, Hambrecht R. Impact of regular physical activity on the NAD(P)H oxidase and angiotensin receptor system in patients with coronary artery disease. Circulation 111: 555-562, 2005.
2. Alpadi K, Magupalli V.G, Käppel S, Köblitz L, Schwarz K, Seigel G.M, Sung C.H, Schmitz F. RIBEYE Recruits Munc119, a mammalian or-tholog of the Caenorhabditis elegans Protein unc119, to synaptic ribbons of photoreceptor synapses. J Biol Chem 283: 26461-26467, 2008.
3. Ameln H, Gustafsson T, Sundberg C.J, Okamoto K, Jansson E, Poellinger L, Makino Y. Physiological activation of hypoxia inducible factor-1 in human skeletal muscle. FASEB J 19: 1009-1011, 2005.
4. Bagatto B, Pelster B, Burggren W.W. Growth and metabolism of larval zebrafish: effects of swim training. J Exp Biol 204: 4335-4343, 2001.
5. Bassel-Duby R, Olson E.N. Signaling pathways in skeletal muscle remodeling. Ann Rev Biochem 6: 19-37, 2006.
6. Bilton R.L, Booker G.W. The subtle side to hypoxia inducible factor (HIFα) regulation. Eur J Biochem 270: 791-798, 2003.
7. Carroll VA, Ashcroft M. Role of hypoxia-inducible factor (HIF)-1α versus HIF-2α in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res 66: 6264-6270, 2006.
8. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analyt Biochem 162: 156-159, 1987.
9. Christiansen J.S, Jobling M. The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise. Can J Zool 68: 2185-2191, 1990.
10. Davison W. The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol 117A: 67-75, 1997.
11. Egginton S. Temperature and angiogenesis: the possible role of mechanical factors in capillary growth. Comp Biochem Physiol 132A: 773-787, 2002.
12. Ehrnborg C, Lange K.H.W, Dall R, Christiansen J.S, Lundberg P.A, Baxter R.C, Boroujerdi M.A, Bengtsson B.A, Healey M.L, Pentecost C, Longobardi S, Napoli R, Rosen T. The growth hormone/insulin-like growth factor-I axis hormones and bone markers in elite athletes in response to a maximum exercise test. J Clin Endocrinol Metab 88: 394-401, 2003.
13. Eldar A, Elowitz M.B. Functional roles for noise in genetic circuits. Nature 467: 167-173, 2010.
14. Freyssenet D. Energy sensing and regulation of gene expression in skeletal muscle. J Appl Physiol 102: 529-540, 2007.
15. Gallaugher P.E, Thorarensen H, Kiessling A, Farrell A.P. Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in Chinook salmon (On-corhynchus tshawytscha) during critical speed swimming. J Exp Biol 204: 2861-2872, 2001.
16. Gassmann M, Tissot van Patot M, Soliz J. The neuronal control of hypoxic ventilation erythropoietin and sexual dimorphism. Ann NY Acad Sci 1177: 151-161, 2009.
17. Gong B, Liang D, Chew T.G, Ge R. Characterization of the zebrafish vascular endothelial growth factor A gene: comparison with vegf-A genes in mammals and Fugu. Biochim Biophys Acta 1676: 33-40, 2004.
18. Greenbaum D, Colangelo C, Williams K, Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4: 117, 2003.
19. Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg C.J. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol Heart Circ Physiol 276: H679-H685, 1999.
20. Hamilton M.T, Booth F.W. Skeletal muscle adaptation to exercise: a century of progress. J Appl Physiol 88: 327-331, 2000.
21. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-785, 2007.
22. Heidbreder M, Fröhlich F, Jöhren O, Dendorfer A, Quadri F, Do-miniak P. Hypoxia rapidly activates HIF-3a mRNA expression. FASEB J 17: 1541-1543, 2003.
23. Hochachka P.W, Somero G.N. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. New York: Oxford University Press, 2002, p. 1-466.
24. Hoppeler H, Howald H, Conley K.E, Lindstedt S.L, Claassen H, Vock P, Weibel E.R. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59: 320-327, 1985.
25. Hoppeler H, Vogt M, Weibel E.R, Flück M. Response of skeletal muscle mitochondria to hypoxia. Exp Physiol 88: 109-119, 2003.
26. Jaakkola P, Mole D.R, Tian Y.M, Wilson M.I, Gielbert J, Gaskell S.J, Kriegsheim Av Hebestreit H.F, Mukherji M, Schofield CJ, Maxwell P.H, Pugh C.W, Ratcliffe P.J. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472, 2001.
27. Jacob E, Drexel M, Schwerte T, Pelster B. The influence of hypoxia and of hypoxemia on the development of cardiac activity in zebrafish larvae. Am J Physiol Regul Integr Comp Physiol 283: R911-R917, 2002.
28. Joyner M.J, Tschakovsky M.E. Nitric oxide and physiologic vasodilation in human limbs: where do we go from here? Appl Physiol Nutr Metab 28: 475-490, 2003.
29. Kaelin J, Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402, 2008.
30. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70: 1469-1480, 2006.
31. Kopp R, Schwerte T, Egg M, Sandbichler A.M, Egger B, Pelster B. 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, 2010.
32. Law S.H.W, Wu R.S.S, Ng P.K.S, Yu R.M.K, Kong R.Y.C. 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, 2006.
33. Loboda A, Jozkowicz A, Dulak J. HIF-1 and HIF-2 transcription factors - similar but not identical. Mol Cells 29: 435-442, 2010.
34. Lundby C, Gassmann M, Pilegaard H. Regular endurance training reduces the exercise induced HIF-1α and HIF-2α mRNA expression in human skeletal muscle in normoxic conditions. Eur J Appl Physiol 96: 363-369, 2006.
35. Marques I.J, Leito J.T.D, Spaink H.P, Testerink J, Jaspers R.T, Witte F, van den Berg S, Bagowski C.P. Transcriptome analysis of the response to chronic constant hypoxia in zebrafish hearts. J Comp Physiol [B] 178: 77-92, 2008.
36. Martin C.C, Tang P, Barnardo G, Krone P.H. Expression of the chaperonin 10 gene during zebrafish development. Cell Stress Chaperones 6: 38-43, 2001.
37. Mason S.D, Howlett R.A, Kim M.J, Olfert I.M, Hogan M.C, McNulty W, Hickey R.P, Wagner P.D, Kahn C.R, Giordano F.J, Johnson R.S. Loss of skeletal muscle HIF-1α results in altered exercise endurance. PLoS Biol 2: e288, 2004.
38. Mason S.D, Rundqvist H, Papandreou I, Duh R, McNulty W.J, Howlett R.A, Olfert I.M, Sundberg C.J, Denko N.C, Poellinger L, Johnson R.S. HIF-1α in endurance training: suppression of oxidative metabolism. Am J Physiol Regul Integr Comp Physiol 293: R2059-R2069, 2007.
39. Maynard M.A, Evans A.J, Hosomi T, Hara S, Jewett M.A.S, Ohh M. Human HIF-3α4 is a dominant-negative regulator of HIF-1 and is down-regulated in renal cell carcinoma. FASEB J 19: 1396-1406, 2005.
40. McClelland G.B, Craig P.M, Dhekney K, Dipardo S. Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol 577: 739-751, 2006.
41. McCurley A.T, Callard G.V. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9: 102, 2008.
42. Milkiewicz M, Doyle J.L, Fudalewski T, Ispanovic E, Aghasi M, Haas T.L. HIF-1alpha and HIF-2alpha play a central role in stretch-induced but not shear-stress-induced angiogenesis in rat skeletal muscle. J Physiol 583: 753-766, 2007.
43. Naryzhny SN. Blue Dry Western: simple, economic, informative, and fast way of immunodetection. Analyt Biochem 392: 90-95, 2009.
44. Nikinmaa M, Rees B.B. Oxygen-dependent gene expression in fish. Am J Physiol Regul Integr Comp Physiol 288: R1079-R1090, 2005.
45. O'Hagan K.A, Cocchiglia S, Zhdanov A.V, Tambuwala M.M, Cummins E.P, Monfared M, Agbor T.A, Garvey J.F, Papkovsky D.B, Taylor C.T, Allan B.B. PGC-1α is coupled to HIF-1α-dependent gene expression by increasing mitochondrial oxygen consumption in skeletal muscle cells. Proc Natl Acad Sci USA 106: 2188-2193, 2009.
46. Ookawara T, Suzuk K, Haga S, Ha S, Chung K.S, Toshinai K, Hamaoka T, Katsumura T, Takemasa T, Mizuno M, Hitomi Y, Suzuki K, Ohno H. Transcription regulation of gene expression in human skeletal muscle in response to endurance training. Res Commun Mol Pathol Pharmacol 111: 41-54, 2002.
47. Pascal L, True L, Campbell D, Deutsch E, Risk M, Coleman I, Eichner L, Nelson P, Liu A. Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate. BMC Genomics 9: 246, 2008.
48. Patel S.A, Simon M.C. Biology of hypoxia-inducible factor-2a in development and disease. Cell Death Differ 15: 628-634, 2008.
49. Pelster B, Sänger A.M, Siegele M, Schwerte T. Influence of swim training on cardiac activity, tissue capillarization, and mitochondrial density in muscle tissue of zebrafish larvae. Am J Physiol Regul Integr Comp Physiol 285: R339-R347, 2003.
50. Pette D. Plasticity in skeletal, cardiac, and smooth muscle historical perspectives: plasticity of mammalian skeletal muscle. J Appl Physiol 90: 1119-1124, 2001.
51. Pette D, Staron R.S. Transitions of muscle fiber phenotypic plasticity. Histochem Cell Biol 115: 359-372, 2001.
52. Pisani D.F, Dechesne C.A. Skeletal muscle HIF-1α expression is dependent on muscle fiber type. J Gen Physiol 126: 173-178, 2005.
53. Plaut I. Effects of fin size on swimming performance, swimming behaviour and routine activity of zebrafish Danio rerio. J Exp Biol 203: 813-820, 2000.
54. Plaut I, Gordon M.S. Swimming metabolism of wild-type and cloned zebrafish Brachydanio rerio. J Exp Biol 194: 209-223, 1994.
55. Poliseno L, Salmena L, Zhang J, Carver B, Haveman W.J, Pandolfi P.P. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465: 1033-1038, 2010.
56. Prior B.M, Yang H.T, Terjung R.L. What makes vessels grow with exercise training? J Appl Physiol 97: 1119-1128, 2004.
57. Rainer J, Sanchez-Cabo F, Stocker G, Sturn A, Trajanoski Z. CARMAweb: comprehensive R- and bioconductor-based web service for microarray data analysis. Nucleic Acids Res 34: W498-W503, 2006.
58. Rankin E.B, Biju M.P, Liu Q, Unger T.L, Rha J, Johnson R.S, Simon M.C, Keith B, Haase V.H. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 117: 1068-1077, 2007.
59. Ratcliffe P.J. HIF-1 and HIF-2: working alone or together in hypoxia? J Clin Invest 117: 862-865, 2007.
60. Richardson R.S, Newcomer S.C, Noyszewski E.A. Skeletal muscle intra-cellular PO2 assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol 91: 2679-2685, 2001.
61. Richardson R.S, Noyszewski E.A, Kendrick K.F, Leigh J.S, Wagner P.D. Myoglobin O2 desaturation during exercise evidence of limited O2 transport. J Clin Invest 96: 1916-1926, 1995.
62. Sänger A.M. Effects of training on axial muscle of two cyprinid species: Chondrostoma nasus (L.) and Leuciscus cephalus (L.). J Fish Biol 40: 637-646, 1992.
63. Sänger A.M. The so-called tonic muscle fibre in cyprinid axial muscle: their morphology and response to endurance exercise training. J Fish Biol 50: 487-497, 1997.
64. Sänger A.M, Pötscher U. Endurance exercise training affects fast white axial muscle in the cyprinid species Chalcalburnus chalcoides mento (Agassiz, 1832), Cyprinidae, Teleostei. BAM 10: 297-300, 2001.
65. Sänger A.M, Stoiber W. Muscle fiber diversity and plasticity. Fish Physiol 18: 187-250, 2001.
66. Schmitz F, Königstorfer A, Südhof T.C. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857-872, 2000.
67. Schwerte T, Überbacher D, Pelster B. Non-invasive imaging of blood cell concentration and blood distribution in hypoxic incubated zebrafish in vivo (Danio rerio). J Exp Biol 206: 1299-1307, 2003.
68. Semenza G.L. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 64: 993-998, 2002.
69. Semenza G.L. Oxygen homeostasis. WIREs Sys Biol Med 2: 336-361, 2010.
70. Semenza G.L. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24: 97-106, 2009.
71. Tanaka T, Wiesener M, Bernhardt W, Eckardt K.U, Warnecke C. The human HIF (hypoxia-inducible factor)-3a gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 424: 143-151, 2009.
72. Timmons J.A, Larsson O, Jansson E, Fischer H, Gustafsson T, Green-haff P.L, Ridden J, Rachman J, Peyrard-Janvid M, Wahlestedt C, Sundberg C.J. Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy. FASEB J 19: 750-760, 2005.
73. Ton C, Stamatiou D, Liew C.C. Gene expression profile of zebrafish exposed to hypoxia during development. Physiol Genomics 13: 97-106, 2003.
74. Uchida T, Rossignol F, Matthay M.A, Mounier R, Couette S, Clottes E, Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1a and HIF-2α expression in lung epithelial cells: implication of natural antisense HIF-1α. J Biol Chem 279: 14871- 14878, 2004.
75. van der Meer D.L.M, van den Thillart G.E.E.J, Witte F, de Bakker M.A.G, Besser J, Richardson M.K, Spaink H.P, Leito J.T.D, Bagowski C.P. Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am J Physiol Regul Integr Comp Physiol 289: R1512-R1519, 2005.
76. van der Meulen T, Schipper H, van den Boogaart J.G.M, Huising M.O, Kranenbarg S, van Leeuwen J.L. Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 291: R1040-R1048, 2006.
77. Vock R, Weibel E.R, Hoppeler H, Ordway G, Weber J.M, Taylor C.R. Design of the oxygen and substrate pathways. V. Structural basis of vascular substrate supply to muscle cells. J Exp Biol 199: 1675-1688, 1996.
78. Warnecke C, Zaborowska Z, Kurreck J, Erdmann VA, Frei U, Wiesener M, Eckardt K.U. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha; and HIF-2alpha; (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha; target gene in Hep3B and Kelly cells. FASEB J 18: 1462-1464, 2004.
79. Weibel E.R, Taylor CR, Weber J.M, Vock R, Roberts TJ, Hoppeler H. Design of the oxygen and substrate pathways VII. Different structural limits for oxygen and substrate supply to muscle mitochondria. J Exp Biol 199: 1699-1709, 1996.