Hypoxia and HIF-1 suppress SERCA2a expression in embryonic cardiac myocytes through two interdependent hypoxia response elements

Journal of Molecular and Cellular Cardiology

Volumn 50, Issue 6, 2011, Pages 1008-1016

  Ronkainen, Veli Pekka ^a,b   Skoumal, Reka ^a   Tavi, Pasi ^b  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Calcium cycling; Excitation contraction coupling; Gene expression; Gene promoter; Sarcoplasmic reticulum

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL HYPOXIA; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; GLUCOSE METABOLISM; HEART MUSCLE CELL; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; SEQUENCE HOMOLOGY; UPREGULATION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CALCIUM; CELL HYPOXIA; CELLS, CULTURED; CYTOSOL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; HERPES SIMPLEX VIRUS PROTEIN VMW65; HYPOXIA-INDUCIBLE FACTOR 1; MICE; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; OXYGEN; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; RESPONSE ELEMENTS; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 79955658960     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.02.017     Document Type: Article

References (63)

1. Bers D.M. Cardiac excitation-contraction coupling. Nature Jan. 10 2002, 415(6868):198-205.
2. Diaz M.E., Graham H.K., O'Neill S.C., Trafford A.W., Eisner D.A. The control of sarcoplasmic reticulum Ca content in cardiac muscle. Cell Calcium Sep-Oct. 2005, 38(3-4):391-396.
3. Piacentino V., Weber C.R., Chen X.W., Weisser-Thomas J., Margulies K.B., Bers D.M., et al. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res Apr. 4 2003, 92(6):651-658.
4. 2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovasc Res Jan. 15 2008, 77(2):265-273.
5. Hasenfuss G., Pieske B. Calcium cycling in congestive heart failure. J Mol Cell Cardiol Aug. 2002, 34(8):951-969.
6. Gwathmey J.K., Copelas L., Mackinnon R., Schoen F.J., Feldman M.D., Grossman W., et al. Abnormal intracellular calcium handling in myocardium from patients with end-stage heart-failure. Circ Res Jul. 1987, 61(1):70-76.
7. 2+-ATPase gene expression in the human ventricle during end-stage heart failure. J Clin Invest Jan. 1990, 85(1):305-309.
8. Arai M., Alpert N.R., Maclennan D.H., Barton P., Periasamy M. Alterations in sarcoplasmic-reticulum gene-expression in human heart-failure - a possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ Res Feb. 1993, 72(2):463-469.
9. del Monte F., Harding S.E., Schmidt U., Matsui T., Kang Z.B., Dec G.W., et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation Dec. 7 1999, 100(23):2308-2311.
10. Miyamoto M.I., del Monte F., Schmidt U., DiSalvo T.S., Kang Z.B., Matsui T., et al. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc Natl Acad Sci USA Jan. 18 2000, 97(2):793-798.
11. Niwano K., Arai M., Koitabashi N., Watanabe A., Ikeda Y., Miyoshi H., et al. Lentiviral vector-mediated SERCA2 gene transfer protects against heart failure and left ventricular remodeling after myocardial infarction in rats. Mol Ther Jun. 2008, 16(6):1026-1032.
12. Rapila R., Korhonen T., Tavi P. Excitation-contraction coupling of the mouse embryonic cardiomyocyte. J Gen Physiol Oct. 2008, 132(4):397-405.
13. Korhonen T., Rapila R., Tavi P. Mathematical model of mouse embryonic cardiomyocyte excitation-contraction coupling. J Gen Physiol Oct. 2008, 132(4):407-419.
14. 2+ oscillations, a potential pacemaking mechanism in early embryonic heart cells. J Gen Physiol Aug. 2007, 130(2):133-144.
15. Mesaeli N., Nakamura K., Zvaritch E., Dickie P., Dziak E., Krause K.H., et al. Calreticulin is essential for cardiac development. J Cell Biol Mar. 8 1999, 144(5):857-868.
16. Takeshima H., Komazaki S., Hirose K., Nishi M., Noda T., Lino M. Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2. EMBO J Jun. 15 1998, 17(12):3309-3316.
17. (2+)-ATPase (SERCA2) gene promoter. J Mol Cell Cardiol Oct. 1996, 28(10):2139-2150.
18. 2+- ATPase (SERCA2) gene promoter activity is decreased in response to severe left ventricular pressure-overload hypertrophy in rat hearts. J Mol Cell Cardiol Apr. 1999, 31(4):919-926.
19. Sharma S., Taegtmeyer H., Adrogue J., Razeghi P., Sen S., Ngumbela K., et al. Dynamic changes of gene expression in hypoxia-induced right ventricular hypertrophy. Am J Physiol Heart Circ Physiol Mar. 2004, 286(3):H1185-H1192.
20. Okazaki K., Maltepe E. Oxygen, epigenetics and stem cell fate. Regen Med Jan. 2006, 1(1):71-83.
21. Dunwoodie S.L. The role of hypoxia in development of the mammalian embryo. Dev Cell Dec. 2009, 17(6):755-773.
22. 2+ exchanger are antithetically regulated during mouse cardiac development and in hypo/hyperthyroidism. J Mol Cell Cardiol Mar. 2000, 32(3):453-464.
23. Semenza G.L. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology Aug. 2004, 19:176-182.
24. Krishnan J., Ahuja P., Bodenmann S., Knapik D., Perriard E., Krek W., et al. Essential role of developmentally activated hypoxia-inducible factor 1 alpha for cardiac morphogenesis and function. Circ Res Nov. 7 2008, 103(10):1139-1146.
25. Camenisch G., Stroka D.M., Gassmann M., Wenger R.H. Attenuation of HIF-1 DNA-binding activity limits hypoxia-inducible endothelin-1 expression. Pflügers Arch Eur J Physiol Nov. 2001, 443(2):240-249.
26. Huang L.E., Gu J., Schau M., Bunn H.F. Regulation of hypoxia-inducible factor 1 alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA Jul. 7 1998, 95(14):7987-7992.
27. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science Apr. 20 2001, 292(5516):468-472.
28. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science Apr. 20 2001, 292(5516):464-468.
29. Narravula S., Colgan S.P. Hypoxia-inducible factor 1-mediated inhibition of peroxisome proliferator-activated receptor alpha expression during hypoxia. J Immunol Jun. 15 2001, 166(12):7543-7548.
30. Mazure N.M., Chauvet C., Bois-Joyeux B., Bernard M.A., Nacer-Cherif H., Danan J.L. Repression of alpha-fetoprotein gene expression under hypoxic conditions in human hepatoma cells: characterization of a negative hypoxia response element that mediates opposite effects of hypoxia inducible factor-1 and c-Myc. Cancer Res Feb. 15 2002, 62(4):1158-1165.
31. Erler J.T., Cawthorne C.J., Williams K.J., Koritzinsky M., Wouters B.G., Wilson C., et al. Hypoxia-mediated down-regulation of bid and bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol Cell Biol Apr. 2004, 24(7):2875-2889.
32. Chen K.F., Lai Y.Y., Sun H.S., Tsai S.J. Transcriptional repression of human cad gene by hypoxia inducible factor-1 alpha. Nucleic Acids Res 2005, 33(16):5190-5198.
33. Eltzschig H.K., Abdulla P., Hoffman E., Hamilton K.E., Daniels D., Schonfeld C., et al. HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J Exp Med Dec. 5 2005, 202(11):1493-1505.
34. Morote-Garcia J.C., Rosenberger P., Kuhlicke J., Eltzschig H.K. HIF-1-dependent repression of adenosine kinase attenuates hypoxia-induced vascular leak. Blood Jun. 15 2008, 111(12):5571-5580.
35. Zheng W., Kuhlicke J., Jackel K., Eltzschig H.K., Singh A., Sjoblom M., et al. Hypoxia inducible factor-1 (HIF-1)-mediated repression of cystic fibrosis transmembrane conductance regulator (CFTR) in the intestinal epithelium. FASEB J Jan. 2009, 23(1):204-213.
36. Lee KJ, Lee KY, Lee YM. Downregulation of a tumor suppressor RECK by hypoxia through recruitment of HDAC1 and HIF-1alpha to reverse HRE site in the promoter. Biochim Biophys Acta. May 2010;1803(5):608-16.
37. Wen W, Ding J, Sun W, Wu K, Ning B, Gong W, et al. Suppression of cyclin D1 by hypoxia-inducible factor-1 via direct mechanism inhibits the proliferation and 5-fluorouracil-induced apoptosis of A549 cells. Cancer Res. Mar 1 2010;70(5):2010-9.
38. Bekeredjian R, Walton CB, MacCannell KA, Ecker J, Kruse F, Outten JT, et al. Conditional HIF-1alpha expression produces a reversible cardiomyopathy. PLoS One. 5(7): e11693.
39. Ronkainen V.P., Ronkainen J.J., Hanninen S.L., Leskinen H., Ruas J.L., Pereira T., et al. Hypoxia inducible factor regulates the cardiac expression and secretion of apelin. FASEB J Jun. 2007, 21(8):1821-1830.
40. Vlasblom R., Muller A., Musters R.J., Zuidwijk M.J., Van Hardeveld C., Paulus W.J., et al. Contractile arrest reveals calcium-dependent stimulation of SERCA2a mRNA expression in cultured ventricular cardiomyocytes. Cardiovasc Res Aug. 15 2004, 63(3):537-544.
41. 2+ releases enable rapid heart rates in developing cardiomyocytes. J Physiol Lond May 1 2010, 588(9):1407-1417.
42. Meynier A., Razik H., Cordelet C., Gregoire S., Demaison L. Involvement of oxygen free radicals in the respiratory uncoupling induced by free calcium and ADP-magnesium in isolated cardiac mitochondria: comparing reoxygenation in cultured cardiomyocytes. Mol Cell Biochem Jan. 2003, 243(1-2):55-64.
43. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Investig Mar. 2005, 115(3):500-508.
44. Sabri A., Hughie H.H., Lucchesi P.A. Regulation of hypertrophic and apoptotic signaling pathways by reactive oxygen species in cardiac myocytes. Antioxid Redox Signal Dec. 2003, 5(6):731-740.
45. Korhonen T., Rapila R., Ronkainen V.P., Koivumaki J.T., Tavi P. Local Ca2+ releases enable rapid heart rates in developing cardiomyocytes. J Physiol. May 1 2010;588(Pt 9):1407-17.
46. 2+ homeostasis and cardiomyocyte function. J Biol Chem Dec. 1 2000, 275(48):38073-38080.
47. Andersson K.B., Birkeland J.A., Finsen A.V., Louch W.E., Sjaastad I., Wang Y., et al. Moderate heart dysfunction in mice with inducible cardiomyocyte-specific excision of the Serca2 gene. J Mol Cell Cardiol Aug. 2009, 47(2):180-187.
48. 2+ signaling mechanism in cardiac myocytes. Proc Natl Acad Sci USA Nov. 23 2004, 101(47):16683-16688.
49. MacLennan D.H., Kranias E.G. Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol Jul. 2003, 4(7):566-577.
50. Frazer K.A., Pachter L., Poliakov A., Rubin E.M., Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res Jul. 1 2004, 32(Web Server issue):W273-W279.
51. Gorr T.A., Cahn J.D., Yamagata H., Bunn H.F. Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent. J Biol Chem Aug. 20 2004, 279(34):36038-36047.
52. 2+- ATPase isoform 2 (SERCA2) gene. J Biol Chem Jan. 22 1999, 274(4):2556-2562.
53. Louch W.E., Hougen K., Mork H.K., Swift F., Aronsen J.M., Sjaastad I., et al. Sodium accumulation promotes diastolic dysfunction in end-stage heart failure following Serca2 knockout. J Physiol. Feb 1 2010;588(Pt 3):465-78.
54. Hajjar R.J., Kang J.X., Gwathmey J.K., Rosenzweig A. Physiological effects of adenoviral gene transfer of sarcoplasmic reticulum calcium ATPase in isolated rat myocytes. Circulation Jan. 21 1997, 95(2):423-429.
55. 2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest Jul. 15 1997, 100(2):380-389.
56. 2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ Res Dec. 14-28 1998, 83(12):1205-1214.
57. Maack C., O'Rourke B. Excitation-contraction coupling and mitochondrial energetics. Basic Res Cardiol Sep. 2007, 102(5):369-392.
58. +-ATPase in guinea-pig cardiac ventricular muscle. J Physiol Dec. 15 1994, 481(Pt 3):647-662.
59. Bers D.M. Excitation-contraction coupling and cardiac contractile force 2001, Kluwer Academic Publishers, Dordrecht Boston. 2nd ed.
60. Feldman A.M., Weinberg E.O., Ray P.E., Lorell B.H. Selective changes in cardiac gene expression during compensated hypertrophy and the transition to cardiac decompensation in rats with chronic aortic banding. Circ Res Jul. 1993, 73(1):184-192.
61. (2+)-pump ATPase in congestive heart failure due to myocardial infarction. Mol Cell Biochem Oct-Nov. 1996, 163-164. 285-90.
62. Loots G.G., Ovcharenko I., Pachter L., Dubchak I., Rubin E.M. rVista for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res May 2002, 12(5):832-839.
63. Briggs L.E., Takeda M., Cuadra A.E., Wakimoto H., Marks M.H., Walker A.J., et al. Perinatal loss of Nkx2-5 results in rapid conduction and contraction defects. Circ Res Sep. 12 2008, 103(6):580-590.