Alteration of cardiac glucose metabolism in association to low birth weight: Experimental evidence in lambs with left ventricular hypertrophy

Metabolism: Clinical and Experimental

Volumn 62, Issue 11, 2013, Pages 1662-1672

  Wang, Kimberley C W ^a   Lim, Chin H ^a   McMillen, I Caroline ^a,b   Duffield, Jaime A ^a,b   Brooks, Doug A ^a   Morrison, Janna L ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Cardiac fatty acid metabolism; Cardiac glucose metabolism; Left ventricular hypertrophy; Low birth weight

Indexed keywords

ADENOSINE TRIPHOSPHATE; CCAAT ENHANCER BINDING PROTEIN BETA; CD36 ANTIGEN; FATTY ACID; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; GLYCOGEN; INSULIN; INSULIN RECEPTOR; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; PYRUVATE DEHYDROGENASE KINASE 4; RETINOID X RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY CONVERSION; ENERGY METABOLISM; FATTY ACID METABOLISM; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEART LEFT VENTRICLE HYPERTROPHY; INTRAUTERINE GROWTH RETARDATION; LAMB; LOW BIRTH WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIODIC ACID SCHIFF STAIN; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ABW; ACC; ACETYL COA CARBOXYLASE; ADENOSINE TRIPHOSPHATE; AKT; AKT SUBSTRATE 160; AS160; ATP; AVERAGE BIRTH WEIGHT; B2M; BETA-2-MICROGLOBULIN; C/EBPΒ; CARDIAC FATTY ACID METABOLISM; CARDIAC GLUCOSE METABOLISM; CARNITINE PALMITOYLTRANSFERASE-I; CCAAT/ENHANCER BINDING PROTEIN; CD36; CPT-I; FATP1; FATTY ACID TRANSLOCASE CD36; FATTY ACID TRANSPORTER PROTEIN 1; GLUCOSE TRANSPORTER; GLUT; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE; GS; GSK; HORMONE SENSITIVE LIPASE; HPRT; HSL; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE 1; INSULIN-RECEPTOR; IR; LBW; LEFT VENTRICULAR HYPERTROPHY; LOW BIRTH WEIGHT; MEAN NORMALISED EXPRESSION; MNE; PAS; PC; PDH; PDK-4; PEPTIDYLPROLYL ISOMERASE A; PERIODIC ACID-SCHIFF; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PGC-1; PGK; PHOSPHOGLYCERATE KINASE 1; PPAR; PPARΓ COACTIVATOR 1; PPIA; PROTEIN KINASE B; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE-4; RETINOID X RECEPTOR Α; RXRΑ; SD; STANDARD DEVIATION; TCA; TRICARBOXYLIC ACID; TYROSINE 3-MONOOXYGENASE; YWAHZ;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; FATTY ACIDS; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 4; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; HYPERTROPHY, LEFT VENTRICULAR; INFANT, LOW BIRTH WEIGHT; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, INSULIN; SHEEP;

EID: 84886384555     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.06.013     Document Type: Article

References (66)

1. M.A. Wood, and K.A. Ellenbogen Cardiac pacemakers from the patient's perspective Circulation 105 18 2002 2136 2138 (Pubitemid 34517154)
2. J.M. Huss, and D.P. Kelly Mitochondrial energy metabolism in heart failure: a question of balance J Clin Invest 115 3 2005 547 555 (Pubitemid 40322224)
3. S.C. Kolwicz Jr., and R. Tian Metabolic therapy at the crossroad: how to optimize myocardial substrate utilization? Trends Cardiovasc Med 19 6 2009 201 207
4. H. Taegtmeyer Switching metabolic genes to build a better heart Circulation 106 16 2002 2043 2045 (Pubitemid 35192807)
5. G.D. Lopaschuk, M.A. Spafford, and D.R. Marsh Glycolysis is predominant source of myocardial atp production immediately after birth Am J Physiol Heart Circ Physiol 261 1991 H1698 H1705
6. M. Saddik, and G.D. Lopaschuk Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts J Biol Chem 236 13 1991 8162 8170 (Pubitemid 21906491)
7. L.L. Chan, S.P. Sebert, and M.A. Hyatt Effect of maternal nutrient restriction from early to midgestation on cardiac function and metabolism after adolescent-onset obesity Am J Physiol Regul Integr Comp Physiol 296 5 2009 R1455 R1463
8. P.S. Tappia, M.S. Nijjar, and A. Mahay Phospholipid profile of developing heart of rats exposed to low-protein diet in pregnancy Am J Physiol Regul Integr Comp Physiol 289 5 2005 R1400 R1406
9. M.L. Langdown, M.J. Holness, and M.C. Sugden Early growth retardation induced by excessive exposure to glucocorticoids in utero selectively increases cardiac glut1 protein expression and akt/protein kinase b activity in adulthood J Endocrinol 169 1 2001 11 22 (Pubitemid 32273210)
10. M. Iemitsu, T. Miyauchi, and S. Maeda Cardiac hypertrophy by hypertension and exercise training exhibits different gene expression of enzymes in energy metabolism Hypertens Res 26 10 2003 829 837 (Pubitemid 37406952)
11. T. Kato, S. Niizuma, and Y. Inuzuka Analysis of metabolic remodeling in compensated left ventricular hypertrophy and heart failure Circ Heart Fail 3 3 2010 420 430
12. O.M. Hyyti, D. Ledee, and X.H. Ning Aging impairs myocardial fatty acid and ketone oxidation and modifies cardiac functional and metabolic responses to insulin in mice Am J Physiol Heart Circ Physiol 299 3 2010 H868 H875
13. L. Nascimben, J.S. Ingwall, and B.H. Lorell Mechanisms for increased glycolysis in the hypertrophied rat heart Hypertension 44 5 2004 662 667 (Pubitemid 39435236)
14. R. Tian, N. Musi, and J. D'Agostino Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy Circulation 104 14 2001 1664 1669 (Pubitemid 32947531)
15. M. Rajabi, C. Kassiotis, and P. Razeghi Return to the fetal gene program protects the stressed heart: a strong hypothesis Heart Fail Rev 12 3-4 2007 331 343 (Pubitemid 350176706)
16. S.C. Kolwicz Jr., and R. Tian Glucose metabolism and cardiac hypertrophy Cardiovasc Res 90 2 2011 194 201
17. M. van Bilsen, F.A. van Nieuwenhoven, and G.J. van der Vusse Metabolic remodelling of the failing heart: beneficial or detrimental? Cardiovasc Res 81 3 2009 420 428
18. I. Luptak, J.A. Balschi, and Y. Xing Decreased contractile and metabolic reserve in peroxisome proliferator-activated receptor-α-null hearts can be rescued by increasing glucose transport and utilization Circulation 112 15 2005 2339 2346 (Pubitemid 41464577)
19. J.S. Jaswal, W. Keung, and W. Wang Targeting fatty acid and carbohydrate oxidation - a novel therapeutic intervention in the ischemic and failing heart Biochim Biophys Acta 1813 7 2011 1333 1350
20. Q. Liu, J.C. Docherty, and J.C. Rendell High levels of fatty acids delay the recovery of intracellular ph and cardiac efficiency inpost-ischemic hearts by inhibiting glucose oxidation J Am Coll Cardiol 39 4 2002 718 725 (Pubitemid 34158171)
21. D.J. Barker, C. Osmond, and J. Golding Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease BMJ 298 6673 1989 564 567 (Pubitemid 19072097)
22. J. Rich-Edwards, M.J. Stampfer, and J.E. Manson Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976 BMJ 315 7105 1997 396 400 (Pubitemid 27346039)
23. S.S. Jonker, L. Zhang, and S. Louey Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart J Appl Physiol 102 2007 1130 1142 (Pubitemid 46377041)
24. E.A. Woodcock, and S.J. Matkovich Cardiomyocytes structure, function and associated pathologies Int J Biochem Cell Biol 37 9 2005 1746 1751 (Pubitemid 40961659)
25. K.C. Wang, L. Zhang, and I.C. McMillen Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb J Physiol 589 19 2011 4709 4722
26. J.A. Duffield, T. Vuocolo, and R. Tellam Intrauterine growth restriction and the sex specific programming of leptin and peroxisome proliferator-activated receptor gamma (ppargamma) mrna expression in visceral fat in the lamb Pediatr Res 66 1 2009 59 65
27. L. Danielson, I.C. McMillen, and J.L. Dyer Restriction of placental growth results in greater hypotensive response to alpha-adrenergic blockade in fetal sheep during late gestation J Physiol 563 Pt 2 2005 611 620 (Pubitemid 40360917)
28. J.L. Dyer, I.C. McMillen, and K.E. Warnes No evidence for an enhanced role of endothelial nitric oxide in the maintenance of arterial blood pressure in the iugr sheep fetus Placenta 30 8 2009 705 710
29. B.S. Muhlhausler, J.A. Duffield, and S.E. Ozanne The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle J Physiol 587 Pt 17 2009 4199 4211
30. K.C. Wang, D.A. Brooks, and K.L. Thornburg Activation of igf-2r stimulates cardiomyocyte hypertrophy in the late gestation sheep fetus J Physiol 590 Pt 21 2012 5425 5437
31. M. Passmore, M. Nataatmadja, and J.F. Fraser Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in ovis aries BMC Mol Biol 10 72 2009
32. P.S. Soo, J. Hiscock, and K.J. Botting Maternal undernutrition reduces p-glycoprotein in guinea pig placenta and developing brain in late gestation Reprod Toxicol 33 3 2012 374 381
33. K. Byrne, T. Vuocolo, and C. Gondro A gene network switch enhances the oxidative capacity of ovine skeletal muscle during late fetal development BMC Genomics 11 378 2010
34. S. Gentili, J.L. Morrison, and I.C. McMillen Intrauterine growth restriction and differential patterns of hepatic growth and expression of igf1, pck2, and hsdl1 mrna in the sheep fetus in late gestation Biol Reprod 80 6 2009 1121 1127
35. S.E. Nada, R.C. Thompson, and V. Padmanabhan Developmental programming: differential effects of prenatal testosterone excess on insulin target tissues Endocrinology 151 11 2010 5165 5173
36. E. Frey, F. Regenfelder, and P. Sussmann Adipogenic and myogenic gene expression in rotator cuff muscle of the sheep after tendon tear J Orthop Res 27 4 2009 504 509
37. J. Hellemans, G. Mortier, and A. De Paepe Qbase relative quantification framework and software for management and automated analysis of real-time quantitative pcr data Genome Biol 8 2 2007 R19
38. G. Schaart, R.P. Hesselink, and H.A. Keizer A modified pas stain combined with immunofluorescence for quantitative analyses of glycogen in muscle sections Histochem Cell Biol 122 2 2004 161 169 (Pubitemid 39222749)
39. R.V. Farese, M.P. Sajan, and M.L. Standaert Atypical protein kinase c in insulin action and insulin resistance Biochem Soc Trans 33 Pt 2 2005 350 353 (Pubitemid 40604370)
40. Allard MF, Schonekess BO, Henning SL, et al. Contribution of oxidative metabolism and glycolysis to atp production in hypertrophied hearts. Am J Physiol Heart Circ Physiol 1994;267(2 36-2): H742-50. (Pubitemid 24272494)
41. A. Akki, K. Smith, and A.M. Seymour Compensated cardiac hypertrophy is characterised by a decline in palmitate oxidation Mol Cell Biochem 311 1-2 2008 215 224
42. I. Friehs, A.M. Moran, and C. Stamm Impaired glucose transporter activity in pressure-overload hypertrophy is an early indicator of progression to failure Circulation 100 19 Suppl 1999 II-187 II-193
43. J.W. Kennedy, M.F. Hirshman, and E.V. Gervino Acute exercise induces glut4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes Diabetes 48 5 1999 1192 1197 (Pubitemid 29226370)
44. C.L. Antos, T.A. McKinsey, and N. Frey Activated glycogen synthase-3β suppresses cardiac hypertrophy in vivo Proc Natl Acad Sci U S A 99 2 2002 907 912 (Pubitemid 34106609)
45. C. Badorff, F.H. Seeger, and A.M. Zeiher Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation Circ Res 97 7 2005 645 654 (Pubitemid 41416333)
46. M.F. Allard, S.L. Henning, and R.B. Wambolt Glycogen metabolism in the aerobic hypertrophied rat heart Circulation 96 2 1997 676 682 (Pubitemid 27329450)
47. W.C. Stanley, G.D. Lopaschuk, and J.L. Hall Regulation of myocardial carbohydrate metabolism under normal and ischaemic conditions Cardiovasc Res 33 2 1997 243 257
48. G.D. Lopaschuk, J.R. Ussher, and C.D. Folmes Myocardial fatty acid metabolism in health and disease Physiol Rev 90 1 2010 207 258
49. C.P. Lydell, A. Chan, and R.B. Wambolt Pyruvate dehydrogenase and the regulation of glucose oxidation in hypertrophied rat hearts Cardiovasc Res 53 4 2002 841 851 (Pubitemid 34261022)
50. R.T. Mallet Pyruvate: metabolic protector of cardiac performance Proc Soc Exp Biol Med 223 2 2000 136 148 (Pubitemid 30339435)
51. N. Sorokina, J.M. O'Donnell, and R.D. McKinney Recruitment of compensatory pathways to sustain oxidative flux with reduced carnitine palmitoyltransferase i activity characterizes inefficiency in energy metabolism in hypertrophied hearts Circulation 115 15 2007 2033 2041 (Pubitemid 46625954)
52. F. Liang, F. Wang, and S. Zhang Peroxisome proliferator activated receptor (ppar)alpha agonists inhibit hypertrophy of neonatal rat cardiac myocytes Endocrinology 144 9 2003 4187 4194 (Pubitemid 37088775)
53. K. Yamamoto, R. Ohki, and R.T. Lee Peroxisome proliferator-activated receptor gamma activators inhibit cardiac hypertrophy in cardiac myocytes Circulation 104 14 2001 1670 1675 (Pubitemid 32947532)
54. M.E. Young, F.A. Laws, and G.W. Goodwin Reactivation of peroxisome proliferator-activated receptor alpha is associated with contractile dysfunction in hypertrophied rat heart J Biol Chem 276 48 2001 44390 44395
55. S.Z. Duan, C.Y. Ivashchenko, and M.W. Russell Cardiomyocyte-specific knockout and agonist of peroxisome proliferator-activated receptor-gamma both induce cardiac hypertrophy in mice Circ Res 97 4 2005 372 379 (Pubitemid 41216142)
56. B. Stratmann, and D. Tschoepe Sweet heart - contributions of metabolism in the development of heart failure in diabetes mellitus Exp Clin Endocrinol Diabetes 116 Suppl 1 2008 S40 S45
57. J. Luo, S. Wu, and J. Liu Conditional PPARγ knockout from cardiomyocytes of adult mice impairs myocardial fatty acid utilization and cardiac function Am J Transl Res 3 1 2010 61 72
58. P.M. Barger, and D.P. Kelly Ppar signaling in the control of cardiac energy metabolism Trends Cardiovasc Med 10 6 2000 238 245 (Pubitemid 32229879)
59. H. Degens, K.F. de Brouwer, and A.J. Gilde Cardiac fatty acid metabolism is preserved in the compensated hypertrophic rat heart Basic Res Cardiol 101 1 2006 17 26 (Pubitemid 43323428)
60. T. Miyamoto, Y. Takeishi, and S. Tazawa Fatty acid metabolism assessed by 125i-iodophenyl 9-methylpentadecanoic acid (9mpa) and expression of fatty acid utilization enzymes in volume-overloaded hearts Eur J Clin Invest 34 3 2004 176 181 (Pubitemid 38406631)
61. G.D. Lopaschuk, L.A. Witters, and T. Itoi Acetyl-CoA carboxylase involvement in the rapid maturation of fatty acid oxidation in the newborn rabbit heart J Biol Chem 269 41 1994 25871 25878 (Pubitemid 24336288)
62. J. Yang, and G. Holman Long-term metformin treatment stimulates cardiomyocyte glucose transport through an AMPK-dependent reduction in glut4 endocytosis Endocrinology 147 2006 2728 2736 (Pubitemid 43764609)
63. S.B. Jorgensen, J.N. Nielsen, and J.B. Birk The alpha2-5′amp- activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading Diabetes 53 2004 3074 3081 (Pubitemid 39564481)
64. J. Dyck, N. Kudo, and A. Barr Phosphorylation control of cardiac acetyl-coa carboxylase by camp-dependent protein kinase and 5′-amp activated protein kinase Eur J Biochem 262 1999 184 190 (Pubitemid 29242625)
65. H.C. Chiu, A. Kovacs, and D.A. Ford A novel mouse model of lipotoxic cardiomyopathy J Clin Invest 107 7 2001 813 822 (Pubitemid 32274034)
66. H.S. Leong, M. Grist, and H. Parsons Accelerated rates of glycolysis in the hypertrophied heart: are they a methodological artifact? Am J Physiol Endocrinol Metab 282 5 2002 E1039 E1045