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Review Article

The effect of reactive oxygen species on cardiomyocyte differentiation of pluripotent stem cells

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Pages 150-158 | Received 30 Sep 2017, Accepted 18 Dec 2017, Published online: 11 Jan 2018

References

  • Al-Khami AA, Rodriguez PC, Ochoa AC. Energy metabolic pathways control the fate and function of myeloid immune cells. J Leukoc Biol 2017;102:369–380.
  • Hu C, Fan L, Cen P, Chen E., Jiang Z, Li L. Energy metabolism plays a critical role in stem cell maintenance and differentiation. Int J Mol Sci 2016;17:253.
  • Siska PJ, Rathmell JC. Metabolic signaling drives IFN-γ. Cell Metab 2016;24:651–652.
  • Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 2007;4:S60–S67.
  • Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 2011;29:486–495.
  • Hom JR, Quintanilla RA, Hoffman DL., de Mesy Bentley KL., Molkentin JD., Sheu SS, et al. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell 2011;21:469–478.
  • Folmes CD, Dzeja PP, Nelson TJ, Terzic A. Mitochondria in control of cell fate. Circ Res 2012;110:526–529.
  • Sumandea MP, Steinberg SF. Redox signaling and cardiac sarcomeres. J Biol Chem 2011;286:9921–9927.
  • Buggisch M, Ateghang B, Ruhe C, Strobel C., Lange S., Wartenberg M, Sauer H. Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase. J Cell Sci 2007;120:885–894.
  • Pucéat M, Travo P, Quinn MT, Fort P. A dual role of the GTPase Rac in cardiac differentiation of stem cells. Mol Biol Cell 2003;14:2781–2792.
  • Na L, Wartenberg M, Nau H, Hescheler J, Sauer H. Anticonvulsant valproic acid inhibits cardiomyocyte differentiation of embryonic stem cells by increasing intracellular levels of reactive oxygen species. Birth Defects Res A Clin Mol Teratol 2003;67:174–180.
  • Qu J, Chen W, Hu R, Feng H. The injury and therapy of reactive oxygen species in intracerebral hemorrhage looking at mitochondria. Oxid Med Cell Longev 2016;2016:2592935.
  • Murray TV, Smyrnias I, Shah AM, Brewer AC. NADPH oxidase 4 regulates cardiomyocyte differentiation via redox activation of c-Jun protein and the cis-regulation of GATA-4 gene transcription. J Biol Chem 2013;288:15745–15759.
  • Ostman A, Frijhoff J, Sandin A, Bohmer FD. Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 2011;150:345–356.
  • Sauvanet C, Duvezin-Caubet S, di Rago JP, Rojo M. Energetic requirements and bioenergetic modulation of mitochondrial morphology and dynamics. Semin Cell Dev Biol 2010;21:558–565.
  • Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology. Circ Res 2011;108:378–396.
  • Lei I, Liu L, Sham MH, Wang Z. SWI/SNF in cardiac progenitor cell differentiation. J Cell Biochem 2013;114:2437–2445.
  • Rahman I, Marwick J, Kirkham P. Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-kappaB and pro-inflammatory gene expression. Biochem Pharmacol 2004;68:1255–1267.
  • Kreuz S, Fischle W. Oxidative stress signaling to chromatin in health and disease. Epigenomics 2016;8:843–862.
  • Dickinson BC, Chang CJ. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 2011;7:504–511.
  • Wang K, Zhang T, Dong Q, Nice EC, Huang C, Wei Y. Redox homeostasis: the linchpin in stem cell selfrenewal and differentiation. Cell Death Dis 2013;4:e537.
  • Katsuyama M. NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. J Pharmacol Sci 2010;114:134–146.
  • Sart S, Song L, Li Y. Controlling redox status for stem cell survival, expansion, and differentiation. Oxid Med Cell Longev 2015;2015:105135.
  • Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest 2004;114:147–152.
  • Hernández-García D, Wood CD, Castro-Obregón S, Covarrubias L. Reactive oxygen species: a radical role in development? Free Radic Biol Med 2010;49:130–143.
  • Armstrong L, Tilgner K, Saretzki G, Atkinson SP., Stojkovic M, Moreno R, et al. Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells 2010;28:661–673.
  • Prigione A, Fauler B, Lurz R, Lehrach H, Adjaye J. The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 2010;28:721–733.
  • Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008;88:581–609.
  • Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012;48:158–167.
  • Ding L, Liang XG, Hu Y, Zhu DY, Lou YJ. Involvement of p38MAPK and reactive oxygen species in icariin-induced cardiomyocyte differentiation of murine embryonic stem cells in vitro. Stem Cells Dev 2008;17:751–760.
  • Li J, Stouffs M, Serrander L, Banfi B, Bettiol E, Charnay Y, et al. The NADPH oxidase NOX4 drives cardiac differentiation: role in regulating cardiac transcription factors and MAP kinase activation. Mol Biol Cell 2006;17:3978–3988.
  • Abreu IA, Cabelli DE. Superoxide dismutases-a review of the metal-associated mechanistic variations. Biochim Biophys Acta 2010;1804:263–274.
  • Ribas V, García-Ruiz C, Fernández-Checa JC. Glutathione and mitochondria. Front Pharmacol 2014;5:151.
  • Lee S, Kim SM, Lee RT. Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Antioxid Redox Signal 2013;18:1165–1207.
  • Vlasits J, Jakopitsch C, Bernroitner M, Zamocky M, Furtmuller PG, Obinger C. Mechanisms of catalase activity of heme peroxidases. Arch Biochem Biophys 2010;500:74–81.
  • Ishii T, Mann GE. Redox status in mammalian cells and stem cells during culture in vitro: critical roles of Nrf2 and cystine transporter activity in the maintenance of redox balance. Redox Biol 2014;2:786–794.
  • Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002;295:2450–2452.
  • Takahashi M. Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 2012;58:1–9.
  • Shi X, Zhang Y, Zheng J, Pan J. Reactive oxygen species in cancer stem cells. Antioxid Redox Signal 2012;16:1215–1228.
  • Naka K, Muraguchi T, Hoshii T, Hirao A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal 2008;10:1883–1894.
  • Wang QY, Liu ZS, Wang J, Wang HX, Li A, Yang Y, et al. Glutathione peroxidase-1 is required for selfrenewal of murine embryonic stem cells. Biochem Biophys Res Commun 2014;448:454–460.
  • Cho YM, Kwon S, Pak YK., Seol HW, Choi YM, Park DJ, et al. Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 2006;348:1472–1478.
  • Varum S, Rodrigues AS, Moura MB., Momcilovic O, Easley CA 4th., Ramalho-Santos J, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011;6:e20914.
  • Yao Y, Lu Y, Chen WC, Jiang Y, Cheng T, Ma Y, et al. Cobalt and nickel stabilize stem cell transcription factor OCT4 through modulating its SUMOylation and ubiquitination. PLoS One 2014;9:e86620.
  • Pervaiz S, Taneja R, Ghaffari S. Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal 2009;11:2777–2789.
  • Sauer H, Rahimi G, Hescheler J, Wartenberg M. Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett 2000;476:218–223.
  • Schmelter M, Ateghang B, Helmig S, Wartenberg M, Sauer H. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 2006;20:1182–1184.
  • Serena E, Figallo E, Tandon N, Cannizzaro C, Gerecht S, Elvassore N, et al. Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Exp Cell Res 2009;315:3611–3619.
  • Crespo FL, Sobrado VR, Gomez L, Cervera AM, McCreath KJ. Mitochondrial reactive oxygen species mediate cardiomyocyte formation from embryonic stem cells in high glucose. Stem Cells 2010;28:1132–1142.
  • Lingan JV, Alanzalon RE, Porter GA, Jr. Preventing permeability transition pore opening increases mitochondrial maturation, myocyte differentiation and cardiac function in the neonatal mouse heart. Pediatr Res 2017;81:932–941.
  • Dennery PA. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 2007;81:155–162.
  • Hossein MS, Hashem MA, Jeong YW, Lee MS, Kim S, Kim JH, et al. Temporal effects of alpha-tocopherol and L-ascorbic acid on in vitro fertilized porcine embryo development. Anim Reprod Sci 2007;100:107–117.
  • Tian XZ, Wen Q, Shi JM, Liang W, Zeng SM, Tian JH, et al. Effects of melatonin on in vitro development of mouse two-cell embryos cultured in HTF medium. Endocr Res 2010;35:17–23.
  • Timme-Laragy AR, Goldstone JV, Imhoff BR, Stegeman JJ, Hahn ME, Hansen JM. Glutathione redox dynamics and expression of glutathione-related genes in the developing embryo. Free Radic Biol Med 2013;65:89–101.
  • Drenckhahn JD. Heart development: mitochondria in command of cardiomyocyte differentiation. Dev Cell 2011;21:392–393.
  • Tsou PS, Talia NN, Pinney AJ, Kendzicky A, Piera-Velazquez S, Jimenez S, et al. Effect of oxidative stress on protein tyrosine phosphatase 1B in scleroderma dermal fibroblasts. Arthritis Rheum 2012;64:1978–1989.
  • Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 2005;17:183–189.
  • Salmeen A, Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid Redox Signal 2005;7:560–577.
  • Templeton DJ, Aye MS, Rady J, Xu F, Cross JV. Purification of reversibly oxidized proteins (PROP) reveals a redox switch controlling p38 MAP kinase activity. PLOS one 2010;5:e15012.
  • Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005;120:649–661.
  • Nagai H, Noguchi T, Takeda K, Ichijo H. Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 2007;40:1–6.
  • Görlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: a mutual interplay. Redox Biol 2015;6:260–271.
  • Li J, Pucéat M, Perez-Terzic C, Mery A, Nakamura K, Michalak M, et al. Calreticulin reveals a critical Ca(2+) checkpoint in cardiac myofibrillogenesis. J Cell Biol 2002;158:103–113.
  • Puceat M. Role of Rac-GTPase and reactive oxygen species in cardiac differentiation of stem cells. Antioxid Redox Signal 2005;7:1435–1439.
  • Yanes O, Clark J, Wong DM, Patti GJ, Sanchez-Ruiz A, Benton, HP, et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat Chem Biol 2010;6:411–417.
  • Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 2011;14:264–271.
  • Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, Bernard D, et al. A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 2007;9:293–299.
  • Prigione A, Lichtner B, Kuhl H, Struys EA, Wamelink M, Lehrach H, et al. Human induced pluripotent stem cells harbor homoplasmic and heteroplasmic mitochondrial DNA mutations while maintaining human embryonic stem cell-like metabolic reprogramming. Stem Cells 2011;29:1338–1348.
  • Facucho-Oliveira JM, St John JC. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 2009;5:140–158.
  • Folmes CD, Nelson TJ, Dzeja PP, Terzic A. Energy metabolism plasticity enables stemness programs. Ann N Y Acad Sci 2012;1254:82–89.
  • Jheng HF, Tsai PJ, Guo SM, Kuo LH., Chang CS, Su IJ, et al. Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 2012;32:309–319.
  • Mitra K, Rikhy R, Lilly M, Lippincott-Schwartz J. DRP1-dependent mitochondrial fission initiates follicle cell differentiation during Drosophila oogenesis. J Cell Biol 2012;197:487–497.
  • Kasahara A, Cipolat S, Chen Y, Dorn GW 2nd, Scorrano L. Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling. Science 2013;342:734–737.
  • Bolisetty S, Jaimes EA. Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 2013;14:6306–6344.
  • Giedt RJ, Yang C, Zweier JL, Matzavinos A, Alevriadou BR. Mitochondrial fission in endothelial cells after simulated ischemia/reperfusion: role of nitric oxide and reactive oxygen species. Free Radic Biol Med 2012;52:348–356.
  • Pletjushkina OY, Lyamzaev KG, Popova EN., Nepryakhina OK, Ivanova OY, Domnina LV, et al. Effect of oxidative stress on dynamics of mitochondrial reticulum. Biochim Biophys Acta 2006;1757:518–524.
  • Zhang X, Yalcin S, Lee DF., Yeh TY, Lee SM, Su J, et al. FoxO1 is an essential regulator of pluripotency in human embryonic stem cells. Nat Cell Biol 2011;13:1092–1099.
  • Brunet A, Sweeney LB, Sturgill JF., Chua KF, Greer PL, Lin Y, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004;303:2011–2015.
  • Boopathy AV, Pendergrass KD, Che PL, Yoon YS, Davis ME. Oxidative stress-induced Notch1 signaling promotes cardiogenic gene expression in mesenchymal stem cells. Stem Cell Res Ther 2013;4:43.
  • Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004;432:107–112.
  • Rasmussen TP. Embryonic stem cell differentiation: a chromatin perspective. Reprod Biol Endocrinol 2003;1:100.

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