Hypoxic Regulation of Hand1 Controls the Fetal-Neonatal Switch in Cardiac Metabolism

PLoS Biology

Volumn 11, Issue 9, 2013, Pages

  Breckenridge, Ross A ^a,b   Piotrowska, Izabela ^a   Ng, Keat Eng ^a   Ragan, Timothy J ^a   West, James A ^c   Kotecha, Surendra ^a   Towers, Norma ^a   Bennett, Michael ^a   Kienesberger, Petra C ^d   Smolenski, Ryszard T ^e   Siddall, Hillary K ^b   Offer, John L ^a   Mocanu, Mihaela M ^b   Yelon, Derek M ^b   Dyck, Jason R B ^d   Griffin, Jules L ^c   Abramov, Andrey Y ^f   Gould, Alex P ^a   Mohun, Timothy J ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF ALBERTA   (Canada)

^e MEDICAL UNIVERSITY OF GDANSK   (Poland)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HAND1 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; FETUS; GENE; GLYCOLYSIS; HAND1 GENE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE METABOLISM; HYPOXIA; LIPID OXIDATION; MITOCHONDRION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN SENSING; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE; ENERGY METABOLISM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIPID METABOLISM; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MYOCARDIAL ISCHEMIA; MYOCARDIUM; MYOCYTES, CARDIAC; OXYGEN; OXYGEN CONSUMPTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84884550495     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001666     Document Type: Article

References (55)

1. Eltzschig HK, Eckle T, (2011) Ischemia and reperfusion-from mechanism to translation. Nat Med 17: 1391-1401.
2. Lopaschuk GD, Spafford MA, Marsh DR, (1991) Glycolysis is predominant source of myocardial ATP production immediately after birth. Am J Physiol 261: H1698-1705.
3. Lopaschuk GD, Jaswal JS, (2010) Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J Cardiovasc Pharmacol 56: 130-140.
4. Sheldon CA, Friedman WF, Sybers HD, (1976) Scanning electron microscopy of fetal and neonatal lamb cardiac cells. J Mol Cell Cardiol 8: 853-862.
5. Fisher DJ, Heymann MA, Rudolph AM, (1980) Myocardial oxygen and carbohydrate consumption in fetal lambs in utero and in adult sheep. Am J Physiol 238: H399-405.
6. Olivetti G, Anversa P, Loud AV, (1980) Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth, and sarcoplasmic alterations. Circ Res 46: 503-512.
7. Makinde AO, Kantor PF, Lopaschuk GD, (1998) Maturation of fatty acid and carbohydrate metabolism in the newborn heart. Mol Cell Biochem 188: 49-56.
8. Taegtmeyer H, Sen S, Vela D, (2010) Return to the fetal gene program: a suggested metabolic link to gene expression in the heart. Ann N Y Acad Sci 1188: 191-198.
9. Breckenridge RA, Zuberi Z, Gomes J, Orford R, Dupays L, et al. (2009) Overexpression of the transcription factor Hand1 causes predisposition towards arrhythmia in mice. J Mol Cell Cardiol 47: 133-141.
10. Firulli AB, McFadden DG, Lin Q, Srivastava D, Olson EN, (1998) Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat Genet 18: 266-270.
11. Riley P, Anson-Cartwright L, Cross JC, (1998) The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 18: 271-275.
12. Ritter O, Haase H, Schulte HD, Lange PE, Morano I, (1999) Remodeling of the hypertrophied human myocardium by cardiac bHLH transcription factors. J Cell Biochem 74: 551-561.
13. Cross JC, Flannery ML, Blanar MA, Steingrimsson E, Jenkins NA, et al. (1995) Hxt encodes a basic helix-loop-helix transcription factor that regulates trophoblast cell development. Development 121: 2513-2523.
14. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E, (2000) Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 14: 3191-3203.
15. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, et al. (2000) Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 105: 577-587.
16. Compernolle V, Brusselmans K, Franco D, Moorman A, Dewerchin M, et al. (2003) Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1alpha. Cardiovasc Res 60: 569-579.
17. Krishnan J, Ahuja P, Bodenmann S, Knapik D, Perriard E, et al. (2008) Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ Res 103: 1139-1146.
18. Lei L, Mason S, Liu D, Huang Y, Marks C, et al. (2008) Hypoxia-inducible factor-dependent degeneration, failure, and malignant transformation of the heart in the absence of the von Hippel-Lindau protein. Mol Cell Biol 28: 3790-3803.
19. Mohun TJ, Weninger WJ, (2011) Imaging heart development using high-resolution episcopic microscopy. Curr Opin Genet Dev 21 (5-2) (): 573-578.
20. Weninger WJ, Geyer SH, Mohun TJ, Rasskin-Gutman D, Matsui T, et al. (2006) High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology. Anat Embryol (Berl) 211: 213-221.
21. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, et al. (2001) Metabolic gene expression in fetal and failing human heart. Circulation 104: 2923-2931.
22. Rajabi M, Kassiotis C, Razeghi P, Taegtmeyer H, (2007) Return to the fetal gene program protects the stressed heart: a strong hypothesis. Heart Fail Rev 12: 331-343.
23. Yatscoff MA, Jaswal JS, Grant MR, Greenwood R, Lukat T, et al. (2008) Myocardial hypertrophy and the maturation of fatty acid oxidation in the newborn human heart. Pediatr Res 64: 643-647.
24. Cook GA, Edwards TL, Jansen MS, Bahouth SW, Wilcox HG, et al. (2001) Differential regulation of carnitine palmitoyltransferase-I gene isoforms (CPT-I alpha and CPT-I beta) in the rat heart. J Mol Cell Cardiol 33: 317-329.
25. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, et al. (2008) Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev 22: 1948-1961.
26. McFadden DG, Barbosa AC, Richardson JA, Schneider MD, Srivastava D, et al. (2005) The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development 132: 189-201.
27. Lopaschuk GD, McNeil GF, McVeigh JJ, (1989) Glucose oxidation is stimulated in reperfused ischemic hearts with the carnitine palmitoyltransferase 1 inhibitor, Etomoxir. Molecular and cellular biochemistry 88: 175-179.
28. Djouadi F, Bonnefont JP, Munnich A, Bastin J, (2003) Characterization of fatty acid oxidation in human muscle mitochondria and myoblasts. Molecular Genetics and Metabolism 78: 112-118.
29. Plun-Favreau H, Burchell VS, Holmstrom KM, Yao Z, Deas E, et al. (2012) HtrA2 deficiency causes mitochondrial uncoupling through the F(1)F(0)-ATP synthase and consequent ATP depletion. Cell death & disease 3: e335.
30. Siddall HK, Warrell CE, Yellon DM, Mocanu MM, (2008) Ischemia-reperfusion injury and cardioprotection: investigating PTEN, the phosphatase that negatively regulates PI3K, using a congenital model of PTEN haploinsufficiency. Basic Res Cardiol 103: 560-568.
31. Neubauer S, Horn M, Cramer M, Harre K, Newell JB, et al. (1997) Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 96: 2190-2196.
32. Neubauer S, (2007) The failing heart-an engine out of fuel. N Engl J Med 356: 1140-1151.
33. Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, et al. (2003) Defective brain development in mice lacking the Hif-1alpha gene in neural cells. Mol Cell Biol 23: 6739-6749.
34. Zolk O, Solbach TF, Eschenhagen T, Weidemann A, Fromm MF, (2008) Activation of negative regulators of the hypoxia-inducible factor (HIF) pathway in human end-stage heart failure. Biochem Biophys Res Commun 376: 315-320.
35. Giordano FJ, (2005) Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115: 500-508.
36. Hogberg H, Engblom L, Ekdahl A, Lidell V, Walum E, et al. (2006) Temperature dependence of O2 consumption; opposite effects of leptin and etomoxir on respiratory quotient in mice. Obesity (Silver Spring) 14: 673-682.
37. Lopaschuk GD, Wall SR, Olley PM, Davies NJ, (1988) Etomoxir, a carnitine palmitoyltransferase I inhibitor, protects hearts from fatty acid-induced ischemic injury independent of changes in long chain acylcarnitine. Circ Res 63: 1036-1043.
38. Bruder ED, Raff H, (2010) Cardiac and plasma lipid profiles in response to acute hypoxia in neonatal and young adult rats. Lipids Health Dis 9: 3.
39. Russell LK, Mansfield CM, Lehman JJ, Kovacs A, Courtois M, et al. (2004) Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res 94: 525-533.
40. Semenza GL, (2011) Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harb Symp Quant Biol 76: 347-353.
41. Neary MT, Mohun TJ, Breckenridge RA, (2013) A mouse model to study the link between hypoxia, long QT interval and sudden infant death syndrome. Disease Models & Mechanisms 6: 503-507.
42. Chen CH, Liu YF, Lee SD, Huang CY, Lee WC, et al. (2009) Altitude hypoxia increases glucose uptake in human heart. High Alt Med Biol 10: 83-86.
43. Holloway CJ, Montgomery HE, Murray AJ, Cochlin LE, Codreanu I, et al. (2011) Cardiac response to hypobaric hypoxia: persistent changes in cardiac mass, function, and energy metabolism after a trek to Mt. Everest Base Camp. Faseb J 25: 792-796.
44. Depre C, Vatner SF, (2005) Mechanisms of cell survival in myocardial hibernation. Trends in Cardiovascular Medicine 15: 101-110.
45. Depre C, Vanoverschelde JL, Gerber B, Borgers M, Melin JA, et al. (1997) Correlation of functional recovery with myocardial blood flow, glucose uptake, and morphologic features in patients with chronic left ventricular ischemic dysfunction undergoing coronary artery bypass grafting. The Journal of Thoracic and Cardiovascular Surgery 113: 371-378.
46. Bell RM, Mocanu MM, Yellon DM, (2011) Retrograde heart perfusion: the Langendorff technique of isolated heart perfusion. Journal of Molecular and Cellular Cardiology 50: 940-950.
47. Dyck JR, Cheng JF, Stanley WC, Barr R, Chandler MP, et al. (2004) Malonyl coenzyme a decarboxylase inhibition protects the ischemic heart by inhibiting fatty acid oxidation and stimulating glucose oxidation. Circ Res 94: e78-84.
48. Lopaschuk GD, (2004) Targets for modulation of fatty acid oxidation in the heart. Curr Opin Investig Drugs 5: 290-294.
49. Perman JC, Bostrom P, Lindbom M, Lidberg U, StAhlman M, et al. (2011) The VLDL receptor promotes lipotoxicity and increases mortality in mice following an acute myocardial infarction. J Clin Invest 121: 2625-2640.
50. Stancheva I, Collins AL, Van den Veyver IB, Zoghbi H, Meehan RR, (2003) A mutant form of MeCP2 protein associated with human Rett syndrome cannot be displaced from methylated DNA by notch in Xenopus embryos. Molecular Cell 12: 425-435.
51. Le Belle JE, Harris NG, Williams SR, Bhakoo KK, (2002) A comparison of cell and tissue extraction techniques using high-resolution 1H-NMR spectroscopy. NMR in Biomedicine 15: 37-44.
52. Dyck JR, Hopkins TA, Bonnet S, Michelakis ED, Young ME, et al. (2006) Absence of malonyl coenzyme A decarboxylase in mice increases cardiac glucose oxidation and protects the heart from ischemic injury. Circulation 114: 1721-1728.
53. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292: C125-136.
54. Smolenski RT, Lachno DR, Ledingham SJ, Yacoub MH, (1990) Determination of sixteen nucleotides, nucleosides and bases using high-performance liquid chromatography and its application to the study of purine metabolism in hearts for transplantation. Journal of Chromatography 527: 414-420.
55. Kodde IF, van der Stok J, Smolenski RT, de Jong JW, (2007) Metabolic and genetic regulation of cardiac energy substrate preference. Comp Biochem Phys A 146: 26-39.