Metabolic Control of Cardiomyocyte Cell Cycle

Ivan Menendez-Montes; Daniel J. Garry; Jianyi (Jay) Zhang; Hesham A. Sadek

doi:10.14797/mdcvj.1309

Metabolic Control of Cardiomyocyte Cell Cycle

Methodist DeBakey Cardiovascular Journal

Volume 19 (2023): Issue 5

By: Ivan Menendez-Montes , Daniel J. Garry , Jianyi (Jay) Zhang and Hesham A. Sadek

Open Access

|Nov 2023

Porrello ER, Mahmoud AI, Simpson E, et al. Transient regenerative potential of the neonatal mouse heart. Science. 2011 Feb 25;331(6020):1078-80. doi: 10.1126/science.1200708
Open DOI Search in Google Scholar Back to article
Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol. 1996 Nov;271(5 Pt 2):H2183-9. doi: 10.1152/ajpheart.1996.271.5.H2183
Open DOI Search in Google Scholar Back to article
Lopaschuk GD, Jaswal JS. Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J Cardiovasc Pharmacol. 2010 Aug;56(2):130-40. doi: 10.1097/FJC.0b013e3181e74a14
Open DOI Search in Google Scholar Back to article
Makinde AO, Kantor PF, Lopaschuk GD. Maturation of fatty acid and carbohydrate metabolism in the newborn heart. Mol Cell Biochem. 1998 Nov;188(1-2):49-56.
Search in Google Scholar Back to article
Puente BN, Kimura W, Muralidhar SA, et al. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell. 2014 Apr 24;157(3):565-79. doi: 10.1016/j.cell.2014.03.032. Erratum in: Cell. 2014 May 22;157(5):1243
Open DOI Search in Google Scholar Back to article
Gibb AA, Hill BG. Metabolic Coordination of Physiological and Pathological Cardiac Remodeling. Circ Res. 2018 Jun 22;123(1):107-128. doi: 10.1161/CIRCRESAHA.118.312017
Open DOI Search in Google Scholar Back to article
Karwi QG, Uddin GM, Ho KL, Lopaschuk GD. Loss of Metabolic Flexibility in the Failing Heart. Front Cardiovasc Med. 2018 Jun 6;5:68. doi: 10.3389/fcvm.2018.00068
Open DOI Search in Google Scholar Back to article
Opie LH. Metabolism of the heart in health and disease. II. Am Heart J. 1969 Jan;77(1):100-22 contd. doi: 10.1016/0002-8703(69)90135-5
Open DOI Search in Google Scholar Back to article
Neubauer S. The failing heart--an engine out of fuel. N Engl J Med. 2007 Mar 15;356(11):1140-51. doi: 10.1056/NEJMra063052
Open DOI Search in Google Scholar Back to article
Lee YM, Jeong CH, Koo SY, et al. Determination of hypoxic region by hypoxia marker in developing mouse embryos in vivo: a possible signal for vessel development. Dev Dyn. 2001 Feb;220(2):175-86. doi: 10.1002/1097-0177(20010201)220:2<;175::AID-DVDY1101>3.0.CO;2-F
Open DOI Search in Google Scholar Back to article
Ostadal B, Ostadalova I, Dhalla NS. Development of cardiac sensitivity to oxygen deficiency: comparative and ontogenetic aspects. Physiol Rev. 1999 Jul;79(3):635-59. doi: 10.1152/physrev.1999.79.3.635
Open DOI Search in Google Scholar Back to article
Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009 May 22;324(5930):1029-33. doi: 10.1126/science.1160809
Open DOI Search in Google Scholar Back to article
Hom JR, Quintanilla RA, Hoffman DL, et al. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell. 2011 Sep 13;21(3):469-78. doi: 10.1016/j.devcel.2011.08.008
Open DOI Search in Google Scholar Back to article
Shepard TH, Muffley LA, Smith LT. Ultrastructural study of mitochondria and their cristae in embryonic rats and primate (N. nemistrina). Anat Rec. 1998 Nov;252(3):383-92. doi: 10.1002/(SICI)1097-0185(199811)252:3<;383::AID-AR6>3.0.CO;2-Z
Open DOI Search in Google Scholar Back to article
Menendez-Montes I, Escobar B, Palacios B, et al. Myocardial VHL-HIF Signaling Controls an Embryonic Metabolic Switch Essential for Cardiac Maturation. Dev Cell. 2016 Dec 19;39(6):724-739. doi: 10.1016/j.devcel.2016.11.012
Open DOI Search in Google Scholar Back to article
Kimura W, Xiao F, Canseco DC, et al. Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart. Nature. 2015 Jul 9;523(7559):226-30. doi: 10.1038/nature14582
Open DOI Search in Google Scholar Back to article
Nakada Y, Canseco DC, Thet S, et al. Hypoxia induces heart regeneration in adult mice. Nature. 2017 Jan 12;541(7636):222-227. doi: 10.1038/nature20173
Open DOI Search in Google Scholar Back to article
Hönemann JN, Gerlach D, Hoffmann F, et al. Hypoxia and Cardiac Function in Patients With Prior Myocardial Infarction. Circ Res. 2023 Apr 28;132(9):1165-1167. doi: 10.1161/CIRCRESAHA.122.322334
Open DOI Search in Google Scholar Back to article
Menendez-Montes I, Abdisalaam S, Xiao F, et al. Mitochondrial fatty acid utilization increases chromatin oxidative stress in cardiomyocytes. Proc Natl Acad Sci U S A. 2021 Aug 24;118(34):e2101674118. doi: 10.1073/pnas.2101674118
Open DOI Search in Google Scholar Back to article
Cardoso AC, Lam NT, Savla JJ, et al. Mitochondrial Substrate Utilization Regulates Cardiomyocyte Cell Cycle Progression. Nat Metab. 2020 Feb;2(2):167-178. PMID: 32617517
Search in Google Scholar Back to article
Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010 Jan;90(1):207-58. doi: 10.1152/physrev.00015.2009
Open DOI Search in Google Scholar Back to article
Schneider H, Staudacher S, Poppelreuther M, Stremmel W, Ehehalt R, Füllekrug J. Protein mediated fatty acid uptake: synergy between CD36/FAT-facilitated transport and acyl-CoA synthetase-driven metabolism. Arch Biochem Biophys. 2014 Mar 15;546:8-18. doi: 10.1016/j.abb.2014.01.025
Open DOI Search in Google Scholar Back to article
Li Y, Yang M, Tan J, et al. Targeting ACSL1 promotes cardiomyocyte proliferation and cardiac regeneration. Life Sci. 2022 Apr 1;294:120371. doi: 10.1016/j.lfs.2022.120371
Open DOI Search in Google Scholar Back to article
Brown NF, Weis BC, Husti JE, Foster DW, McGarry JD. Mitochondrial carnitine palmitoyltransferase I isoform switching in the developing rat heart. J Biol Chem. 1995 Apr 14;270(15):8952-7. doi: 10.1074/jbc.270.15.8952
Open DOI Search in Google Scholar Back to article
Li X, Wu F, Günther S, et al. Inhibition of fatty acid oxidation enables heart regeneration in adult mice. Nature. 2023 Oct;622(7983):619-626. doi: 10.1038/s41586-023-06585-5
Open DOI Search in Google Scholar Back to article
Cao T, Liccardo D, LaCanna R, et al. Fatty Acid Oxidation Promotes Cardiomyocyte Proliferation Rate but Does Not Change Cardiomyocyte Number in Infant Mice. Front Cell Dev Biol. 2019 Mar 22;7:42. doi: 10.3389/fcell.2019.00042
Open DOI Search in Google Scholar Back to article
Roy R, Leigh T, Gao E, Zhang X, Tian Y. Activation or inhibition of PPARα-mediated fatty acid β-oxidation does not active cardiomyocyte proliferation in normal or infarcted adult mice. bioRxiv. 2019 Jun (preprint). DOI: 10.1101/667964
Open DOI Search in Google Scholar Back to article
Dyck JR, Hopkins TA, et al. Absence of malonyl coenzyme A decarboxylase in mice increases cardiac glucose oxidation and protects the heart from ischemic injury. Circulation. 2006 Oct 17;114(16):1721-8. doi: 10.1161/CIRCULATIONAHA.106.642009
Open DOI Search in Google Scholar Back to article
Dyck JR, Cheng JF, Stanley WC, et al. Malonyl coenzyme a decarboxylase inhibition protects the ischemic heart by inhibiting fatty acid oxidation and stimulating glucose oxidation. Circ Res. 2004 May 14;94(9):e78-84. doi: 10.1161/01.RES.0000129255.19569.8f
Open DOI Search in Google Scholar Back to article
Gilde AJ, van der Lee KA, Willemsen PH, et al. Peroxisome proliferator-activated receptor (PPAR) alpha and PPARbeta/delta, but not PPARgamma, modulate the expression of genes involved in cardiac lipid metabolism. Circ Res. 2003 Mar 21;92(5):518-24. doi: 10.1161/01.RES.0000060700.55247.7C
Open DOI Search in Google Scholar Back to article
Djouadi F, Brandt JM, Weinheimer CJ, Leone TC, Gonzalez FJ, Kelly DP. The role of the peroxisome proliferator-activated receptor alpha (PPAR alpha) in the control of cardiac lipid metabolism. Prostaglandins Leukot Essent Fatty Acids. 1999 May-Jun;60(5-6):339-43. doi: 10.1016/s0952-3278(99)80009-x
Open DOI Search in Google Scholar Back to article
Ding L, Liang X, Zhu D, Lou Y. Peroxisome proliferator-activated receptor alpha is involved in cardiomyocyte differentiation of murine embryonic stem cells in vitro. Cell Biol Int. 2007 Sep;31(9):1002-9. doi: 10.1016/j.cellbi.2007.03.013
Open DOI Search in Google Scholar Back to article
Nakada Y, Nhi Nguyen NU, Xiao F, et al. DNA Damage Response Mediates Pressure Overload-Induced Cardiomyocyte Hypertrophy. Circulation. 2019 Feb 26;139(9):1237-1239. doi: 10.1161/CIRCULATIONAHA.118.034822
Open DOI Search in Google Scholar Back to article
Nguyen NUN, Canseco DC, Xiao F, et al. A calcineurin-Hoxb13 axis regulates growth mode of mammalian cardiomyocytes. Nature. 2020 Jun;582(7811):271-276. doi: 10.1038/s41586-020-2228-6
Open DOI Search in Google Scholar Back to article
Lopaschuk GD, Spafford MA, Marsh DR. Glycolysis is predominant source of myocardial ATP production immediately after birth. Am J Physiol. 1991 Dec;261(6 Pt 2):H1698-705. doi: 10.1152/ajpheart.1991.261.6.H1698
Open DOI Search in Google Scholar Back to article
Abel ED. Glucose transport in the heart. Front Biosci. 2004 Jan 1;9:201-15. doi: 10.2741/1216
Open DOI Search in Google Scholar Back to article
Fajardo VM, Feng I, Chen BY, et al. GLUT1 overexpression enhances glucose metabolism and promotes neonatal heart regeneration. Sci Rep. 2021 Apr 21;11(1):8669. doi: 10.1038/s41598-021-88159-x
Open DOI Search in Google Scholar Back to article
Magadum A, Singh N, Kurian AA, et al. Pkm2 Regulates Cardiomyocyte Cell Cycle and Promotes Cardiac Regeneration. Circulation. 2020 Apr 14;141(15):1249-1265. doi: 10.1161/CIRCULATIONAHA.119.043067
Open DOI Search in Google Scholar Back to article
Zimmer HG. Regulation of and intervention into the oxidative pentose phosphate pathway and adenine nucleotide metabolism in the heart. Mol Cell Biochem. 1996 Jul-Aug;160-161:101-9. doi: 10.1007/BF00240038
Open DOI Search in Google Scholar Back to article
Jain M, Cui L, Brenner DA, et al. Increased myocardial dysfunction after ischemia-reperfusion in mice lacking glucose-6-phosphate dehydrogenase. Circulation. 2004 Feb 24;109(7):898-903. doi: 10.1161/01.CIR.0000112605.43318.CA
Open DOI Search in Google Scholar Back to article
Hebert LF Jr., Daniels MC, Zhou J, et al. Overexpression of glutamine:fructose-6-phosphate amidotransferase in transgenic mice leads to insulin resistance. J Clin Invest. 1996 Aug 15;98(4):930-6. doi: 10.1172/JCI118876
Open DOI Search in Google Scholar Back to article
Wells L, Vosseller K, Hart GW. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc. Science. 2001 Mar 23;291(5512):2376-8. doi: 10.1126/science.1058714
Open DOI Search in Google Scholar Back to article
Abouleisa RRE, McNally L, Salama ABM, et al. Cell cycle induction in human cardiomyocytes is dependent on biosynthetic pathway activation. Redox Biol. 2021 Oct;46:102094. doi: 10.1016/j.redox.2021.102094
Open DOI Search in Google Scholar Back to article
Rindler PM, Crewe CL, Fernandes J, Kinter M, Szweda LI. Redox regulation of insulin sensitivity due to enhanced fatty acid utilization in the mitochondria. Am J Physiol Heart Circ Physiol. 2013 Sep 1;305(5):H634-43. doi: 10.1152/ajpheart.00799.2012
Open DOI Search in Google Scholar Back to article
Lewandowski ED, White LT. Pyruvate dehydrogenase influences postischemic heart function. Circulation. 1995 Apr 1;91(7):2071-9. doi: 10.1161/01.cir.91.7.2071
Open DOI Search in Google Scholar Back to article
Churchill EN, Murriel CL, Chen CH, Mochly-Rosen D, Szweda LI. Reperfusion-induced translocation of deltaPKC to cardiac mitochondria prevents pyruvate dehydrogenase reactivation. Circ Res. 2005 Jul 8;97(1):78-85. doi: 10.1161/01.RES.0000173896.32522.6e
Open DOI Search in Google Scholar Back to article
Bae J, Salamon RJ, Brandt EB, et al. Malonate Promotes Adult Cardiomyocyte Proliferation and Heart Regeneration. Circulation. 2021 May 18;143(20):1973-1986. doi: 10.1161/CIRCULATIONAHA.120.049952
Open DOI Search in Google Scholar Back to article
Bae J, Salamon RJ, Brandt EB, Paltzer WG, et al. Malonate Promotes Adult Cardiomyocyte Proliferation and Heart Regeneration. Circulation. 2021 May 18;143(20):1973-1986. doi: 10.1161/CIRCULATIONAHA.120.049952
Open DOI Search in Google Scholar Back to article
Drake KJ, Sidorov VY, McGuinness OP, Wasserman DH, Wikswo JP. Amino acids as metabolic substrates during cardiac ischemia. Exp Biol Med (Maywood). 2012 Dec;237(12):1369-78. doi: 10.1258/ebm.2012.012025
Open DOI Search in Google Scholar Back to article
Sun H, Wang Y. Branched chain amino acid metabolic reprogramming in heart failure. Biochim Biophys Acta. 2016 Dec;1862(12):2270-2275. doi: 10.1016/j.bbadis.2016.09.009
Open DOI Search in Google Scholar Back to article
Sun H, Olson KC, Gao C, et al. Catabolic Defect of Branched-Chain Amino Acids Promotes Heart Failure. Circulation. 2016 May 24;133(21):2038-49. doi: 10.1161/CIRCULATIONAHA.115.020226
Open DOI Search in Google Scholar Back to article
Uddin GM, Zhang L, Shah S, et al. Impaired branched chain amino acid oxidation contributes to cardiac insulin resistance in heart failure. Cardiovasc Diabetol. 2019 Jul 5;18(1):86. doi: 10.1186/s12933-019-0892-3
Open DOI Search in Google Scholar Back to article
Murashige D, Jang C, Neinast M, et al. Comprehensive quantification of fuel use by the failing and nonfailing human heart. Science. 2020 Oct 16;370(6514):364-368. doi: 10.1126/science.abc8861
Open DOI Search in Google Scholar Back to article
Lopaschuk GD, Karwi QG, Tian R, Wende AR, Abel ED. Cardiac Energy Metabolism in Heart Failure. Circ Res. 2021 May 14;128(10):1487-1513. doi: 10.1161/CIRCRESAHA.121.318241
Open DOI Search in Google Scholar Back to article
Talman V, Teppo J, Pöhö P, et al. Molecular Atlas of Postnatal Mouse Heart Development. J Am Heart Assoc. 2018 Oct 16;7(20):e010378. doi: 10.1161/JAHA.118.010378
Open DOI Search in Google Scholar Back to article
Lalowski MM, Björk S, Finckenberg P, et al. Characterizing the Key Metabolic Pathways of the Neonatal Mouse Heart Using a Quantitative Combinatorial Omics Approach. Front Physiol. 2018 Apr 11;9:365. doi: 10.3389/fphys.2018.00365
Open DOI Search in Google Scholar Back to article
Vellai, T.. How the amino acid leucine activates the key cell-growth regulator mTOR. Nature. 2021 Aug; 596(7871):192-194. doi: 10.1038/d41586-021-01943-7
Open DOI Search in Google Scholar Back to article
Sansbury BE, DeMartino AM, Xie Z, et al. Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circ Heart Fail. 2014 Jul;7(4):634-42. doi: 10.1161/CIRCHEARTFAILURE.114.001151
Open DOI Search in Google Scholar Back to article
Lu G, Sun H, She P, et al. Protein phosphatase 2Cm is a critical regulator of branched-chain amino acid catabolism in mice and cultured cells. J Clin Invest. 2009 Jun;119(6):1678-87. doi: 10.1172/JCI38151
Open DOI Search in Google Scholar Back to article
Li T, Zhang Z, Kolwicz SC Jr., et al. Defective Branched-Chain Amino Acid Catabolism Disrupts Glucose Metabolism and Sensitizes the Heart to Ischemia-Reperfusion Injury. Cell Metab. 2017 Feb 7;25(2):374-385. doi: 10.1016/j.cmet.2016.11.005
Open DOI Search in Google Scholar Back to article
Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. 2017 Mar 9;168(6):960-976. doi: 10.1016/j.cell.2017.02.004. Erratum in: Cell. 2017 Apr 6;169(2):361-371
Open DOI Search in Google Scholar Back to article
Watanabe K, Nagao M, Toh R, et al. Critical role of glutamine metabolism in cardiomyocytes under oxidative stress. Biochem Biophys Res Commun. 2021 Jan 1;534:687-693. doi: 10.1016/j.bbrc.2020.11.018
Open DOI Search in Google Scholar Back to article
Wang J, Xue Z, Lin J, et al. Proline improves cardiac remodeling following myocardial infarction and attenuates cardiomyocyte apoptosis via redox regulation. Biochem Pharmacol. 2020 Aug;178:114065. doi: 10.1016/j.bcp.2020.114065
Open DOI Search in Google Scholar Back to article
Moreira JBN, Wohlwend M, Fenk S, et al. Exercise Reveals Proline Dehydrogenase as a Potential Target in Heart Failure. Prog Cardiovasc Dis. 2019 Mar-Apr;62(2):193-202. doi: 10.1016/j.pcad.2019.03.002
Open DOI Search in Google Scholar Back to article
Smirnov VN, Asafov GB, Cherpachenko NM, et al. Ammonia neutralization and urea synthesis in cardiac muscle. Circ Res. 1974 Sep;35 Suppl 3:58-73. PMID: 4411934.
Search in Google Scholar Back to article
Duchesne R, Klein JD, Velotta JB, et al. UT-A urea transporter protein in heart: increased abundance during uremia, hypertension, and heart failure. Circ Res. 2001 Jul 20;89(2):139-45. doi: 10.1161/hh1401.093293
Open DOI Search in Google Scholar Back to article
Menendez-Montes I, Escobar B, Gomez MJ, et al. Activation of amino acid metabolic program in cardiac HIF1-alpha-deficient mice. iScience. 2021 Feb 3;24(2):102124. doi: 10.1016/j.isci.2021.102124
Open DOI Search in Google Scholar Back to article
Wentz AE, d’Avignon DA, Weber ML, et al. Adaptation of myocardial substrate metabolism to a ketogenic nutrient environment. J Biol Chem. 2010 Aug 6;285(32):24447-56. doi: 10.1074/jbc.M110.100651
Open DOI Search in Google Scholar Back to article
Puchalska P, Crawford PA. Multi-dimensional Roles of Ketone Bodies in Fuel Metabolism, Signaling, and Therapeutics. Cell Metab. 2017 Feb 7;25(2):262-284. doi: 10.1016/j.cmet.2016.12.022
Open DOI Search in Google Scholar Back to article
Yurista SR, Nguyen CT, Rosenzweig A, de Boer RA, Westenbrink BD. Ketone bodies for the failing heart: fuels that can fix the engine? Trends Endocrinol Metab. 2021 Oct;32(10):814-826. doi: 10.1016/j.tem.2021.07.006
Open DOI Search in Google Scholar Back to article
Chong D, Gu Y, Zhang T, et al. Neonatal ketone body elevation regulates postnatal heart development by promoting cardiomyocyte mitochondrial maturation and metabolic reprogramming. Cell Discov. 2022 Oct 11;8(1):106. doi: 10.1038/s41421-022-00447-6
Open DOI Search in Google Scholar Back to article
Cheng YY, Gregorich Z, Prajnamitra RP, et al. Metabolic Changes Associated With Cardiomyocyte Dedifferentiation Enable Adult Mammalian Cardiac Regeneration. Circulation. 2022 Dec 20;146(25):1950-1967. doi: 10.1161/CIRCULATIONAHA.122.061960
Open DOI Search in Google Scholar Back to article
Horton JL, Davidson MT, Kurishima C, et al. The failing heart utilizes 3-hydroxybutyrate as a metabolic stress defense. JCI Insight. 2019 Feb 21;4(4):e124079. doi: 10.1172/jci.insight.124079
Open DOI Search in Google Scholar Back to article
Matsuura TR, Puchalska P, Crawford PA, Kelly DP. Ketones and the Heart: Metabolic Principles and Therapeutic Implications. Circ Res. 2023 Mar 31;132(7):882-898. doi: 10.1161/CIRCRESAHA.123.321872
Open DOI Search in Google Scholar Back to article

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DOI: https://doi.org/10.14797/mdcvj.1309 | Journal eISSN: 1947-6108

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Language: English

Page range: 26 - 36

Submitted on: Oct 28, 2023

Accepted on: Oct 31, 2023

Published on: Nov 16, 2023

Published by: Houston Methodist DeBakey Heart & Vascular Center

In partnership with: Paradigm Publishing Services

Keywords:

glycolysis,

oxidative phosphorylation,

cardiomyocyte proliferation,

reactive oxygen species,

uridine diphosphate N-acetylglucosamine (UDP GlycNAC),

cardiac regeneration

© 2023 Ivan Menendez-Montes, Daniel J. Garry, Jianyi (Jay) Zhang, Hesham A. Sadek, published by Houston Methodist DeBakey Heart & Vascular Center
This work is licensed under the Creative Commons Attribution-NonCommercial 4.0 License.

Volume 19 (2023): Issue 5