HIF-1α response to hypoxia is functionally separated from the glucocorticoid stress response in the in vitro regenerating human skeletal muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 6, 2010, Pages

  Pirkmajer, Sergej ^a   Filipovic, Dragana ^b   Mars, Tomaz ^a   Mis, Katarina ^a   Grubic, Zoran ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

11 hydroxysteroid dehydrogenases; Antisense version of hypoxia inducible factor; Glucocorticoid receptors; Hypoxia inducible factor ; Vascular endothelial growth factor

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN; HIF1A PROTEIN, HUMAN; INTERLEUKIN 6; SMALL INTERFERING RNA;

ARTICLE; CELL PROLIFERATION; DOWN REGULATION; DRUG EFFECT; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IN VITRO STUDY; MUSCLE REGENERATION; MYOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; STRESS; ANALYSIS OF VARIANCE; ANOXIA; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; REGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANOXIA; BLOTTING, WESTERN; CELLS, CULTURED; DEXAMETHASONE; GLUCOCORTICOIDS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERLEUKIN-6; MUSCLE, SKELETAL; MYOBLASTS; RECEPTORS, GLUCOCORTICOID; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING;

EID: 78649851593     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00133.2010     Document Type: Article

References (56)

1. Abdallah BM, Beck-Nielsen H, Gaster M. Increased expression of 11beta-hydroxysteroid dehydrogenase type 1 in type 2 diabetic myotubes. Eur J Clin Invest 35: 627-634, 2005.
2. Albiston AL, Obeyesekere VR, Smith RE, Krozowski ZS. Cloning and tissue distribution of the human 11 beta-hydroxysteroid dehydrogenase type 2 enzyme. Mol Cell Endocrinol 105: R11-R17, 1994.
3. Ameln H, Gustafsson T, Sundberg CJ, 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. Askanas V, Kwan H, Alvarez RB, Engel WK, Kobayashi T, Martinuzzi A, Hawkins EF. De novo neuromuscular junction formation on human muscle fibers cultured in monolayer and innervated by foetal rat spinal cord: ultrastructural and ultrastructural-cytochemical studies. J Neurocyto 16: 523-537, 1987.
5. Austin L, Burgess AW. Stimulation of myoblast proliferation in culture by leukaemia inhibitory factor and other cytokines. J Neurol Sci 101: 193-197, 1991.
6. Austin L, Bower J, Kurek J, Vakakis N. Effects of leukaemia inhibitory factor and other cytokines on murine and human myoblast proliferation. J Neurol Sci 112: 185-191, 1992.
7. Baeza-Raja B, Munoz-Canoves P. p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: role of interleukin-6. Mol Biol Cell 15: 2013-2026, 2004.
8. Baker ME. Co-evolution of steroidogenic and steroid-inactivating enzymes and adrenal and sex steroid receptors. Mol Cell Endocrinol 215: 55-62, 2004.
9. Bischoff R. The satellite cell and muscle regeneration. In: Myology, edited by Engel AG and Franzini-Armstrong C. New York, NY: McGraw Hill, 1994. p. 97-118.
10. Cantini M, Massimino ML, Rapizzi E, Rossini K, Catani C, Dalla Libera L, Carraro U. Human satellite cell proliferation in vitro is regulated by autocrine secretion of IL-6 stimulated by a soluble factor(s) released by activated monocytes. Biochem Biophys Res Commun 216: 49-53, 1995.
11. Chang Y, Goldberg VM, Caplan AI. Toxic effects of gentamicin on marrow-derived human mesenchymal stem cells. Clin Orthop Relat Res 452: 242-249, 2006. (Pubitemid 44690676)
12. Chargé SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84: 209-238, 2004.
13. 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, Ratcliffe PJC. Elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54, 2001.
14. Frede S, Stockmann C, Winning S, Freitag P, Fandrey J. Hypoxia-inducible factor (HIF) 1alpha accumulation and HIF target gene expression are impaired after induction of endotoxin tolerance. J Immunol 182: 6470-6476, 2009.
15. Fruchter O, Kino T, Zoumakis E, Alesci S, De Martino M, Chrousos G, Hochberg Z. The human glucocorticoid receptor (GR) isoform β differentially suppresses GRα-induced transactivation stimulated by synthetic glucocorticoids. J Clin Endocrinol Metab 90: 3505-3509, 2005.
16. Gao L, Mejías R, Echevarría M, López-Barneo J. Induction of the glucose-6-phosphate dehydrogenase gene expression by chronic hypoxia in PC12 cells. FEBS Lett 569: 256-260, 2004.
17. Goetz IE, Moklebust R, Warren CJ. Effects of some antibiotics on the growth of human diploid skin fibroblasts in cell culture. In Vitro 15: 114-119, 1979.
18. Greenberger S, Boscolo E, Adini I, Mulliken JB, Bischoff J. Corticosteroid suppression of VEGF-A in infantile hemangioma-derived stem cells. N Engl J Med 362: 1005-1013, 2010.
19. Grubic Z, Komel R, Walker WF, Miranda AF. Myoblast fusion and innervation with rat motor nerve alter distribution of acetylcholinesterase and its mRNA in cultures of human muscle. Neuron 14: 317-327, 1995.
20. Hampton-Smith RJ, Peet DJ. From polyps to people: a highly familiar response to hypoxia. Ann NY Acad Sci 1177: 19-29, 2009.
21. Higgins DF, Biju MP, Akai Y, Wutz A, Johnson RS, Haase VH. Hypoxic induction of CTGF is directly mediated by HIF-1. Am J Physiol Renal Physiol 287: F1223-F1232, 2004.
22. Jang C, Obeyesekere VR, Dilley RJ, Krozowski Z, Inder WJ, Alford FP. Altered activity of 11beta-hydroxysteroid dehydrogenase types 1 and 2 in skeletal muscle confers metabolic protection in subjects with type 2 diabetes. J Clin Endocrinol Metab 92: 3314-3320, 2007.
23. Leonard MO, Godson C, Brady HR, Taylor CT. Potentiation of glucocorticoid activity in hypoxia through induction of the glucocorticoid receptor. J Immunol 174: 2250-2257, 2005.
24. Lin ZY, Chuang WL, Chuang YH. Amphotericin B up-regulates angiogenic genes in hepatocellular carcinoma cell lines. Eur J Clin Invest 39: 239-245, 2009.
25. Loboda A, Jozkowicz A, Dulak J. HIF-1 and HIF-2 transcription factors-similar but not identical. Mol Cells 29: 435-442 2010.
26. Lundby C, Calbet JAL, Robach P. The response of human skeletal muscle tissue to hypoxia. Cell Mol Life Sci 66: 3615-3623, 2009.
27. Mars T, King MP, Miranda AF, Walker WF, Mis K, Grubic Z. Functional innervation of cultured human skeletal muscle proceeds by two modes with regard to agrin effects. Neuroscience 118: 87-97, 2003.
28. Maxwell PH, Salnikow K. HIF-1: an oxygen and metal responsive transcription factor. Cancer Biol Ther 3: 29-35, 2004.
29. Melo MR, Faria CD, Melo KC, Reboucas NA, Longui CA. Real-time PCR quantitation of glucocorticoid receptor alpha isoform (Abstract). BMC Mol Biol 5: 19, 2004.
30. Mounier R, Pedersen BK, Plomgaard P. Muscle-specific expression of hypoxia-inducible factor in human skeletal muscle. Exp Physiol 95: 899-907, 2010.
31. Mounier R, Pialoux V, Schmitt L, Richalet JP, Robach P, Coudert J, Clottes E, Fellmann N. Effects of acute hypoxia tests on blood markers in high-level endurance athletes. Eur J Appl Physiol 106: 713-720, 2009.
32. Neckers LM. aHIF: the missing link between HIF-1 and VHL? J Natl Cancer Inst 91: 106-107, 1999.
33. Oakley RH, Webster JC, Sar M, Parker CR Jr, Cidlowski JA. Expression and subcellular distribution of the beta-isoform of the human glucocorticoid receptor. Endocrinology 138: 5028-5038, 1997.
34. Pisani DF, Dechesne CA. Skeletal muscle HIF-1alpha expression is dependent on muscle fiber type. J Gen Physiol 126: 173-178, 2005.
35. Prelovsek O, Mars T, Jevsek M, Podbregar M, Grubic Z. High dexamethasone concentration prevents stimulatory effects of TNF-α and LPS on IL-6 secretion from the precursors of human muscle regeneration. Am J Physiol Regul Integr Comp Physiol 291: R1651-R1656, 2006.
36. Pujols L, Mullol J, Roca-Ferrer J, Torrego A, Xaubet A, Cidlowski JA, Picado C. Expression of glucocorticoid receptor α- and β-isoforms in human cells and tissues. Am J Physiol Cell Physiol 283: C1324-C1331, 2002.
37. Rey S, Semenza GL. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86: 236-242, 2010.
38. Richmond KN, Shonat RD, Lynch RM, Johnson PC. Critical PO2 of skeletal muscle in vivo. Am J Physiol Heart Circ Physiol 277: H1831-H1840, 1999.
39. Rossignol F, de Laplanche E, Mounier R, Bonnefont J, Cayre A, Godinot C, Simonnet H, Clottes E. Natural antisense transcripts of HIF-1alpha are conserved in rodents. Gene 339: 121-130, 2004.
40. Rossignol F, Vaché C, Clottes E. Natural antisense transcripts of hypoxia-inducible factor 1alpha are detected in different normal and tumour human tissues. Gene 299: 135-140, 2002.
41. Schafer TW, Pascale A, Shimonaski G, Came PE. Evaluation of gentamicin for use in virology and tissue culture. Appl Microbiol 23: 565-570, 1972.
42. Schimmer BP, Parker KL. Adrenocorticotropic hormone; adrenocortical steroids and their synthetic analogs; inhibitors of the synthesis and actions of adrenocortical hormones. In: Goodman & Gilman's The Pharmacological Basis of Therapeutics, edited by Brunton LL, Lazo JS, and Parker LL. New York, NY: McGraw-Hill, 2006, p. 1587-1612.
43. Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763, 1994.
44. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, Bauer C, Gassmann M, Candinas D. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 15: 2445-2453, 2001.
45. Tanaka T, Wiesener M, Bernhardt W, Eckardt KU, Warnecke C. The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 424: 143-151, 2009.
46. Uchida T, Rossignol F, Matthay MA, Mounier R, Couette S, Clottes E, Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem 279: 14871-14878, 2004.
47. Walls EV, Kay JE. Inhibition of proliferation of a murine myeloma cell line and mitogen-stimulated B lymphocytes by the antibiotic amphotericin B (Fungizone). Immunology 47: 115-121, 1982.
48. Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90: 4304-4308, 1993.
49. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270: 1230-1237, 1995.
50. Webster KA. Regulation of glycolytic enzyme RNA transcriptional rates by oxygen availability in skeletal muscle cells. Mol Cell Biochem 77: 19-28, 1987.
51. Webster KA. Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia. J Exp Biol 206: 2911-2922, 2003.
52. Wenger RH, Rolfs A, Spielmann P, Zimmermann DR, Gassmann M. Mouse hypoxia-inducible factor-1alpha is encoded by two different mRNA isoforms: expression from a tissue-specific and a housekeeping-type promoter. Blood 91: 3471-3480, 1998.
53. Whorwood CB, Donovan SJ, Wood PJ, Phillips DI. Regulation of glucocorticoid receptor alpha and beta isoforms and type I 11beta-hydroxysteroid dehydrogenase expression in human skeletal muscle cells: a key role in the pathogenesis of insulin resistance? J Clin Endocrinol Metab 86: 2296-2308, 2001.
54. Yun Z, Lin Q, Giaccia AJ. Adaptive myogenesis under hypoxia. Mol Cell Biol 25: 3040-3055, 2005.
55. Zhang H, Qian DZ, Tan YS, Lee K, Gao P, Ren YR, Rey S, Hammers H, Chang D, Pili R, Dang CV, Liu JO, Semenza GL. Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth. Proc Natl Acad Sci USA 105: 19579-19586, 2008.
56. Zoll J, Ponsot E, Dufour S, Doutreleau S, Ventura-Clapier R, Vogt M, Hoppeler H, Ruddy Richard R, Flück M. Exercise training in normobaric hypoxia in endurance runners. III. Muscular adjustments of selected gene transcripts. J Appl Physiol 100: 1258-1266, 2006.