Molecular Control of Cardiac Fetal/Neonatal Remodeling
Abstract
:1. Introduction
2. Molecular Control of Myocardial Metabolism
2.1. HIF Signaling
2.2. AMPK Signaling
2.3. PPAR Signaling
3. Control of Postnatal Mitochondrial Biogenesis
4. Neonatal Cardiac Mitosis and Regeneration
5. Future Challenges
Conflicts of Interest
References
- Makinde, A.O.; Kantor, P.F.; Lopaschuk, G.D. Maturation of fatty acid and carbohydrate metabolism in the newborn heart. Mol. Cell. Biochem. 1998, 188, 49–56. [Google Scholar] [CrossRef]
- Oparil, S.; Bishop, S.P.; Clubb, F.J., Jr. Myocardial cell hypertrophy or hyperplasia. Hypertension 1984, 6, III38–III43. [Google Scholar]
- Porrello, E.R.; Mahmoud, A.I.; Simpson, E.; Hill, J.A.; Richardson, J.A.; Olson, E.N.; Sadek, H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331, 1078–1080. [Google Scholar] [CrossRef]
- Lopaschuk, G.D.; Jaswal, J.S. Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J. Cardiovasc. Pharmacol. 2010, 56, 130–140. [Google Scholar] [CrossRef]
- Lopaschuk, G.D.; Ussher, J.R.; Folmes, C.D.; Jaswal, J.S.; Stanley, W.C. Myocardial fatty acid metabolism in health and disease. Physiol. Rev. 2010, 90, 207–258. [Google Scholar] [CrossRef]
- Agata, Y.; Hiraishi, S.; Oguchi, K.; Misawa, H.; Horiguchi, Y.; Fujino, N.; Yashiro, K.; Shimada, N. Changes in left ventricular output from fetal to early neonatal life. J. Pediatr. 1991, 119, 441–445. [Google Scholar] [CrossRef]
- Itoi, T.; Lopaschuk, G.D. The contribution of glycolysis, glucose oxidation, lactate oxidation, and fatty acid oxidation to atp production in isolated biventricular working hearts from 2-week-old rabbits. Pediatr. Res. 1993, 34, 735–741. [Google Scholar] [CrossRef]
- Chung, S.; Arrell, D.K.; Faustino, R.S.; Terzic, A.; Dzeja, P.P. Glycolytic network restructuring integral to the energetics of embryonic stem cell cardiac differentiation. J. Mol. Cell. Cardiol. 2010, 48, 725–734. [Google Scholar] [CrossRef]
- Lopaschuk, G.D.; Spafford, M.A.; Marsh, D.R. Glycolysis is predominant source of myocardial atp production immediately after birth. Am. J. Physiol. 1991, 261, H1698–H1705. [Google Scholar]
- Jones, C.T.; Rolph, T.P. Metabolic events associated with the preparation of the fetus for independent life. Ciba Found. Symp. 1981, 86, 214–233. [Google Scholar]
- Cotter, D.G.; d'Avignon, D.A.; Wentz, A.E.; Weber, M.L.; Crawford, P.A. Obligate role for ketone body oxidation in neonatal metabolic homeostasis. J. Biol. Chem. 2011, 286, 6902–6910. [Google Scholar]
- Bougneres, P.F.; Karl, I.E.; Hillman, L.S.; Bier, D.M. Lipid transport in the human newborn. Palmitate and glycerol turnover and the contribution of glycerol to neonatal hepatic glucose output. J. Clin. Invest. 1982, 70, 262–270. [Google Scholar] [CrossRef]
- Nau, P.N.; Van Natta, T.; Ralphe, J.C.; Teneyck, C.J.; Bedell, K.A.; Caldarone, C.A.; Segar, J.L.; Scholz, T.D. Metabolic adaptation of the fetal and postnatal ovine heart: Regulatory role of hypoxia-inducible factors and nuclear respiratory factor-1. Pediatr. Res. 2002, 52, 269–278. [Google Scholar] [CrossRef]
- Mitchell, J.A.; Van Kainen, B.R. Effects of alcohol on intrauterine oxygen tension in the rat. Alcoh. Clin. Exp. Res. 1992, 16, 308–310. [Google Scholar] [CrossRef]
- Reynolds, J.D.; Penning, D.H.; Dexter, F.; Atkins, B.; Hrdy, J.; Poduska, D.; Brien, J.F. Ethanol increases uterine blood flow and fetal arterial blood oxygen tension in the near-term pregnant ewe. Alcohol 1996, 13, 251–256. [Google Scholar] [CrossRef]
- Soothill, P.W.; Nicolaides, K.H.; Rodeck, C.H.; Campbell, S. Effect of gestational age on fetal and intervillous blood gas and acid-base values in human pregnancy. Fetal Therapy 1986, 1, 168–175. [Google Scholar] [CrossRef]
- Huang, Y.; Hickey, R.P.; Yeh, J.L.; Liu, D.; Dadak, A.; Young, L.H.; Johnson, R.S.; Giordano, F.J. Cardiac myocyte-specific hif-1alpha deletion alters vascularization, energy availability, calcium flux, and contractility in the normoxic heart. FASEB J. 2004, 18, 1138–1140. [Google Scholar]
- Krishnan, J.; Ahuja, P.; Bodenmann, S.; Knapik, D.; Perriard, E.; Krek, W.; Perriard, J.C. Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ. Res. 2008, 103, 1139–1146. [Google Scholar] [CrossRef]
- Maxwell, P.H.; Wiesener, M.S.; Chang, G.W.; Clifford, S.C.; Vaux, E.C.; Cockman, M.E.; Wykoff, C.C.; Pugh, C.W.; Maher, E.R.; Ratcliffe, P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399, 271–275. [Google Scholar] [CrossRef]
- Lei, L.; Mason, S.; Liu, D.; Huang, Y.; Marks, C.; Hickey, R.; Jovin, I.S.; Pypaert, M.; Johnson, R.S.; Giordano, F.J. Hypoxia-inducible factor-dependent degeneration, failure, and malignant transformation of the heart in the absence of the von hippel-lindau protein. Mol. Cell. Biol. 2008, 28, 3790–3803. [Google Scholar] [CrossRef]
- Neary, M.T.; Mohun, T.J.; Breckenridge, R.A. A mouse model to study the link between hypoxia, long QT interval and sudden infant death syndrome. Dis. Mod. Mech. 2013, 6, 503–507. [Google Scholar] [CrossRef]
- Breckenridge, R.A.; Piotrowska, I.; Ng, K.E.; Ragan, T.J.; West, J.A.; Kotecha, S.; Towers, N.; Bennett, M.; Kienesberger, P.C.; Smolenski, R.T.; et al. Hypoxic regulation of hand1 controls the fetal-neonatal switch in cardiac metabolism. PLoS Biol. 2013, 11, e1001666. [Google Scholar] [CrossRef]
- Formenti, F.; Constantin-Teodosiu, D.; Emmanuel, Y.; Cheeseman, J.; Dorrington, K.L.; Edwards, L.M.; Humphreys, S.M.; Lappin, T.R.; McMullin, M.F.; McNamara, C.J.; et al. Regulation of human metabolism by hypoxia-inducible factor. Proc. Nat. Acad. Sci. USA 2010, 107, 12722–12727. [Google Scholar] [CrossRef]
- Minchenko, O.; Opentanova, I.; Caro, J. Hypoxic regulation of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene family (pfkfb-1–4) expression in vivo. FEBS Lett. 2003, 554, 264–270. [Google Scholar] [CrossRef]
- Yatscoff, M.A.; Jaswal, J.S.; Grant, M.R.; Greenwood, R.; Lukat, T.; Beker, D.L.; Rebeyka, I.M.; Lopaschuk, G.D. Myocardial hypertrophy and the maturation of fatty acid oxidation in the newborn human heart. Pediatr. Res. 2008, 64, 643–647. [Google Scholar] [CrossRef]
- Makinde, A.O.; Gamble, J.; Lopaschuk, G.D. Upregulation of 5'-amp-activated protein kinase is responsible for the increase in myocardial fatty acid oxidation rates following birth in the newborn rabbit. Circ. Res. 1997, 80, 482–489. [Google Scholar] [CrossRef]
- Evans, R.M.; Barish, G.D.; Wang, Y.X. Ppars and the complex journey to obesity. Nat. Med. 2004, 10, 355–361. [Google Scholar] [CrossRef]
- Krishnan, J.; Suter, M.; Windak, R.; Krebs, T.; Felley, A.; Montessuit, C.; Tokarska-Schlattner, M.; Aasum, E.; Bogdanova, A.; Perriard, E.; et al. Activation of a hif1alpha-ppargamma axis underlies the integration of glycolytic and lipid anabolic pathways in pathologic cardiac hypertrophy. Cell Metab. 2009, 9, 512–524. [Google Scholar] [CrossRef]
- Belanger, A.J.; Luo, Z.; Vincent, K.A.; Akita, G.Y.; Cheng, S.H.; Gregory, R.J.; Jiang, C. Hypoxia-inducible factor 1 mediates hypoxia-induced cardiomyocyte lipid accumulation by reducing the DNA binding activity of peroxisome proliferator-activated receptor alpha/retinoid x receptor. Biochem. Biophys. Res. Commun. 2007, 364, 567–572. [Google Scholar] [CrossRef]
- Narravula, S.; Colgan, S.P. Hypoxia-inducible factor 1-mediated inhibition of peroxisome proliferator-activated receptor alpha expression during hypoxia. J. Immunol. 2001, 166, 7543–7548. [Google Scholar]
- Planavila, A.; Rodriguez-Calvo, R.; Jove, M.; Michalik, L.; Wahli, W.; Laguna, J.C.; Vazquez-Carrera, M. Peroxisome proliferator-activated receptor beta/delta activation inhibits hypertrophy in neonatal rat cardiomyocytes. Cardiovasc. Res. 2005, 65, 832–841. [Google Scholar] [CrossRef]
- Cheng, L.; Ding, G.; Qin, Q.; Xiao, Y.; Woods, D.; Chen, Y.E.; Yang, Q. Peroxisome proliferator-activated receptor delta activates fatty acid oxidation in cultured neonatal and adult cardiomyocytes. Biochem. Biophys. Res. Commun. 2004, 313, 277–286. [Google Scholar] [CrossRef]
- Steinmetz, M.; Quentin, T.; Poppe, A.; Paul, T.; Jux, C. Changes in expression levels of genes involved in fatty acid metabolism: Upregulation of all three members of the ppar family (alpha, gamma, delta) and the newly described adiponectin receptor 2, but not adiponectin receptor 1 during neonatal cardiac development of the rat. Basic Res. Cardiol. 2005, 100, 263–269. [Google Scholar] [CrossRef]
- Chung, S.; Dzeja, P.P.; Faustino, R.S.; Perez-Terzic, C.; Behfar, A.; Terzic, A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat. Clin. Practi. Cardiovasc. Med. 2007, 4 (Suppl. 1), S60–S67. [Google Scholar] [CrossRef]
- Lai, L.; Leone, T.C.; Zechner, C.; Schaeffer, P.J.; Kelly, S.M.; Flanagan, D.P.; Medeiros, D.M.; Kovacs, A.; Kelly, D.P. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008, 22, 1948–1961. [Google Scholar] [CrossRef]
- Papanicolaou, K.N.; Kikuchi, R.; Ngoh, G.A.; Coughlan, K.A.; Dominguez, I.; Stanley, W.C.; Walsh, K. Mitofusins 1 and 2 are essential for postnatal metabolic remodeling in heart. Circ. Res. 2012, 111, 1012–1026. [Google Scholar] [CrossRef]
- Lehman, J.J.; Barger, P.M.; Kovacs, A.; Saffitz, J.E.; Medeiros, D.M.; Kelly, D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 2000, 106, 847–856. [Google Scholar] [CrossRef]
- Lehman, J.J.; Kelly, D.P. Transcriptional activation of energy metabolic switches in the developing and hypertrophied heart. Clin. Exp. Pharmacol. Physiol. 2002, 29, 339–345. [Google Scholar] [CrossRef]
- Leone, T.C.; Lehman, J.J.; Finck, B.N.; Schaeffer, P.J.; Wende, A.R.; Boudina, S.; Courtois, M.; Wozniak, D.F.; Sambandam, N.; Bernal-Mizrachi, C.; et al. Pgc-1alpha deficiency causes multi-system energy metabolic derangements: Muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005, 3, e101. [Google Scholar] [CrossRef] [Green Version]
- Lin, J.; Wu, P.H.; Tarr, P.T.; Lindenberg, K.S.; St-Pierre, J.; Zhang, C.Y.; Mootha, V.K.; Jager, S.; Vianna, C.R.; Reznick, R.M.; et al. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 2004, 119, 121–135. [Google Scholar] [CrossRef]
- Sonoda, J.; Mehl, I.R.; Chong, L.W.; Nofsinger, R.R.; Evans, R.M. PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc. Nat. Acad. Sci. USA 2007, 104, 5223–5228. [Google Scholar] [CrossRef]
- Vianna, C.R.; Huntgeburth, M.; Coppari, R.; Choi, C.S.; Lin, J.; Krauss, S.; Barbatelli, G.; Tzameli, I.; Kim, Y.B.; Cinti, S.; et al. Hypomorphic mutation of PGC-1beta causes mitochondrial dysfunction and liver insulin resistance. Cell Metab. 2006, 4, 453–464. [Google Scholar] [CrossRef]
- Mollova, M.; Bersell, K.; Walsh, S.; Savla, J.; Das, L.T.; Park, S.Y.; Silberstein, L.E.; Dos Remedios, C.G.; Graham, D.; Colan, S.; et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Nat. Acad. Sci. USA 2013, 110, 1446–1451. [Google Scholar] [CrossRef]
- Sengupta, A.; Kalinichenko, V.V.; Yutzey, K.E. FoxO1 and FoxM1 transcription factors have antagonistic functions in neonatal cardiomyocyte cell-cycle withdrawal and IGF1 gene regulation. Circ. Res. 2013, 112, 267–277. [Google Scholar] [CrossRef]
- Flink, I.L. Cell cycle reentry of ventricular and atrial cardiomyocytes and cells within the epicardium following amputation of the ventricular apex in the axolotl, amblystoma mexicanum: Confocal microscopic immunofluorescent image analysis of bromodeoxyuridine-labeled nuclei. Anat. Embryol. 2002, 205, 235–244. [Google Scholar] [CrossRef]
- Poss, K.D.; Wilson, L.G.; Keating, M.T. Heart regeneration in zebrafish. Science 2002, 298, 2188–2190. [Google Scholar] [CrossRef]
- Porrello, E.R.; Mahmoud, A.I.; Simpson, E.; Johnson, B.A.; Grinsfelder, D.; Canseco, D.; Mammen, P.P.; Rothermel, B.A.; Olson, E.N.; Sadek, H.A. Regulation of neonatal and adult mammalian heart regeneration by the MIR-15 family. Proc. Nat. Acad. Sci. USA 2013, 110, 187–192. [Google Scholar] [CrossRef]
- Porrello, E.R.; Johnson, B.A.; Aurora, A.B.; Simpson, E.; Nam, Y.J.; Matkovich, S.J.; Dorn, G.W., 2nd; van Rooij, E.; Olson, E.N. MIR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ. Res. 2011, 109, 670–679. [Google Scholar] [CrossRef]
- Eulalio, A.; Mano, M.; Dal Ferro, M.; Zentilin, L.; Sinagra, G.; Zacchigna, S.; Giacca, M. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012, 492, 376–381. [Google Scholar] [CrossRef]
- Mahmoud, A.I.; Kocabas, F.; Muralidhar, S.A.; Kimura, W.; Koura, A.S.; Thet, S.; Porrello, E.R.; Sadek, H.A. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 2013, 497, 249–253. [Google Scholar] [CrossRef]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Breckenridge, R.A. Molecular Control of Cardiac Fetal/Neonatal Remodeling. J. Cardiovasc. Dev. Dis. 2014, 1, 29-36. https://doi.org/10.3390/jcdd1010029
Breckenridge RA. Molecular Control of Cardiac Fetal/Neonatal Remodeling. Journal of Cardiovascular Development and Disease. 2014; 1(1):29-36. https://doi.org/10.3390/jcdd1010029
Chicago/Turabian StyleBreckenridge, Ross A. 2014. "Molecular Control of Cardiac Fetal/Neonatal Remodeling" Journal of Cardiovascular Development and Disease 1, no. 1: 29-36. https://doi.org/10.3390/jcdd1010029