Redox signaling in cardiac renewal

Antioxidants and Redox Signaling

Volumn 21, Issue 11, 2014, Pages 1660-1673

  Kimura, Wataru ^a   Muralidhar, Shalini ^a   Canseco, Diana C ^a   Puente, Bao ^a   Zhang, Cheng Cheng ^a   Xiao, Feng ^a   Abderrahman, Yezan H ^a   Sadek, Hesham A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; ANTIOXIDANT;

CARDIAC STEM CELL; CELL DIFFERENTIATION; CELL REGENERATION; CELL RENEWAL; HEART MUSCLE CELL; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; LUNG CANCER CELL LINE; METABOLIC REGULATION; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; REVIEW; ANIMAL; ANOXIA; CYTOLOGY; METABOLISM; OXIDATIVE STRESS; REGENERATION; SIGNAL TRANSDUCTION; STEM CELL; TUMOR MICROENVIRONMENT;

ANIMALS; ANOXIA; ANTIOXIDANTS; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; HUMANS; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REGENERATION; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84907476552     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.6029     Document Type: Review

References (180)

1. Abramson S, Miller RG, and Phillips RA. The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med 145: 1567-1579, 1977.
2. Abu-Issa R and Kirby ML. Heart field: from mesoderm to heart tube. Annu Rev Cell Dev Biol 23: 45-68, 2007.
3. Adler CP and Costabel U. Cell number in human heart in atrophy, hypertrophy, and under the influence of cytostatics. Recent Adv Stud Cardiac Struct Metab 6: 343-355, 1975.
4. Alfakir M, Dawe N, Eyre R, Tyson-Capper A, Britton K, Robson SC, and Meeson AP. The temporal and spatial expression patterns of ABCG2 in the developing human heart. Int J Cardiol 156: 133-138, 2012.
5. Ali SR, Hippenmeyer S, Saadat LV, Luo L, Weissman IL, and Ardehali R. Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice. Proc Natl Acad Sci USA 111: 8850-8855, 2014.
6. Bartrons R and Caro J. Hypoxia, glucose metabolism and the Warburg's effect. J Bioenerg Biomembr 39: 223-229, 2007.
7. Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De Angelis A, Yasuzawa-Amano S, Trofimova I, Siggins RW, Lecapitaine N, Cascapera S, Beltrami AP, D'Alessandro DA, Zias E, Quaini F, Urbanek K, Michler RE, Bolli R, Kajstura J, Leri A, and Anversa P. Human cardiac stem cells. Proc Natl Acad Sci USA 104: 14068-14073, 2007.
8. Becker LB, vanden Hoek TL, Shao ZH, Li CQ, and Schumacker PT. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol 277: H2240-H2246, 1999.
9. Beerman I, Maloney WJ, Weissmann IL, and Rossi DJ. Stem cells and the aging hematopoietic system. Curr Opin Immunol 22: 500-506, 2010.
10. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, and Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763-776, 2003.
11. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, and Frisen J. Evidence for cardiomyocyte renewal in humans. Science 324: 98-102, 2009.
12. Bock-Marquette I, Saxena A, White MD, Dimaio JM, and Srivastava D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432: 466-472, 2004.
13. Bollini S, Smart N, and Riley PR. Resident cardiac progenitor cells: at the heart of regeneration. J Mol Cell Cardiol 50: 296-303, 2011.
14. Brown MD, Gilmore PE, Hart CA, Samuel JD, Ramani VA, George NJ, and Clarke NW. Characterization of benign and malignant prostate epithelial Hoechst 33342 side populations. Prostate 67: 1384-1396, 2007.
15. Buggisch M, Ateghang B, Ruhe C, Strobel C, Lange S, Wartenberg M, and Sauer H. Stimulation of ES-cellderived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase. J Cell Sci 120: 885-894, 2007.
16. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, and Stallcup WB, Denton CP, McCulloch A, Chen J, Evans SM. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108, 2008.
17. Challen GA and Little MH. A side order of stem cells: the SP phenotype. Stem Cells 24: 3-12, 2006.
18. Chan SK and Mann RS. A structural model for a homeotic protein-extradenticle-DNA complex accounts for the choice of HOX protein in the heterodimer. Proc Natl Acad Sci USA 93: 5223-5228, 1996.
19. Chan SK, Popperl H, Krumlauf R, and Mann RS. An extradenticle-induced conformational change in a HOX protein overcomes an inhibitory function of the conserved hexapeptide motif. EMBO J 15: 2476-2487, 1996.
20. Chaudhari P, Ye Z, and Jang YY. Roles of reactive oxygen species in the fate of stem cells. Antioxid Redox Signal 20: 1881-1890, 2014.
21. Choi WY and Poss KD. Cardiac regeneration. Curr Top Dev Biol 100: 319-344, 2012.
22. Chong JJ, Chandrakanthan V, Xaymardan M, Asli NS, Li J, Ahmed I, Heffernan C, Menon MK, Scarlett CJ, Rashidianfar A, Biben C, Zoellner H, Colvin EK, Pimanda JE, Biankin AV, Zhou B, Pu WT, Prall OW, and Harvey RP. Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 9: 527-540, 2011.
23. Davis DR, Zhang Y, Smith RR, Cheng K, Terrovitis J, Malliaras K, Li TS, White A, Makkar R, and Marban E. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One 4: e7195, 2009.
24. Del Monte G and Harvey RP. An endothelial contribution to coronary vessels. Cell 151: 932-934, 2012.
25. Di Meo S and Venditti P. Mitochondria in exercise-induced oxidative stress. Biol Signals Recept 10: 125-140, 2001.
26. Di Nardo P, Forte G, Ahluwalia A, and Minieri M. Cardiac progenitor cells: potency and control. J Cell Physiol 224: 590-600, 2010.
27. Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, and Tyryshkin A. The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98: 2170-2175, 2001.
28. Dor FJ, Ramirez ML, Parmar K, Altman EL, Huang CA, Down JD, and Cooper DK. Primitive hematopoietic cell populations reside in the spleen: studies in the pig, baboon, and human. Exp Hematol 34: 1573-1582, 2006.
29. Drenckhahn JD, Schwarz QP, Gray S, Laskowski A, Kiriazis H, Ming Z, Harvey RP, Du XJ, Thorburn DR, and Cox TC. Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development. Dev Cell 15: 521-533, 2008.
30. Dyer LA and Kirby ML. The role of secondary heart field in cardiac development. Dev Biol 336: 137-144, 2009.
31. Dzierzak E and Speck NA. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 9: 129-136, 2008.
32. Eaton P, Li JM, Hearse DJ, and Shattock MJ. Formation of 4-hydroxy-2-nonenal-modified proteins in ischemic rat heart. Am J Physiol 276: H935-H943, 1999.
33. Ebner A, Cabernard C, Affolter M, and Merabet S. Recognition of distinct target sites by a unique Labial/Extradenticle/Homothorax complex. Development 132: 1591-1600, 2005.
34. Eliasson P and Jonsson JI. The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol 222: 17-22, 2010.
35. Else PL and Hulbert AJ. Mammals: an allometric study of metabolism at tissue and mitochondrial level. Am J Physiol 248: R415-R421, 1985.
36. Evseenko DA, Murthi P, Paxton JW, Reid G, Emerald BS, Mohankumar KM, Lobie PE, Brennecke SP, Kalionis B, and Keelan JA. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J 21: 3592-3605, 2007.
37. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, Ikeda Y, Perez-Terzic C, and Terzic A. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14: 264-271, 2011.
38. Frangogiannis NG, Smith CW, and Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res 53: 31-47, 2002.
39. Fuchs E, Tumbar T, and Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 116: 769-778, 2004.
40. Fujisaki J, Wu J, Carlson AL, Silberstein L, Putheti P, Larocca R, Gao W, Saito TI, Lo Celso C, Tsuyuzaki H, Sato T, Cote D, Sykes M, Strom TB, and Scadden DT, Lin CP. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474: 216-219, 2011.
41. Fukuda K, Saikawa Y, Ohashi M, Kumagai K, Kitajima M, Okano H, Matsuzaki Y, and Kitagawa Y. Tumor initiating potential of side population cells in human gastric cancer. Int J Oncol 34: 1201-1207, 2009.
42. Geiger H and Rudolph KL. Aging in the lymphohematopoietic stem cell compartment. Trends Immunol 30: 360-365, 2009.
43. Ghadge SK, Muhlstedt S, Ozcelik C, and Bader M. SDF-1alpha as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol Ther 129: 97-108, 2011.
44. Goodell MA, Brose K, Paradis G, Conner AS, and Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806, 1996.
45. Gorbunov N, Petrovski G, Gurusamy N, Ray D, Kim do H, and Das DK. Regeneration of infarcted myocardium with resveratrol-modified cardiac stem cells. J Cell Mol Med 16: 174-184, 2012.
46. Gurusamy N, Mukherjee S, Lekli I, Bearzi C, Bardelli S, and Das DK. Inhibition of ref-1 stimulates the production of reactive oxygen species and induces differentiation in adult cardiac stem cells. Antioxid Redox Signal 11: 589-600, 2009.
47. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, and Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9: 617-628, 2005.
48. Hadnagy A, Gaboury L, Beaulieu R, and Balicki D. SP analysis may be used to identify cancer stem cell populations. Exp Cell Res 312: 3701-3710, 2006.
49. Handy DE and Loscalzo J. Redox regulation of mitochondrial function. Antioxid Redox Signal 16: 1323-1367, 2012.
50. Harrison JS, Rameshwar P, Chang V, and Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood 99: 394, 2002.
51. Ho MM, Ng AV, Lam S, and Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67: 4827-4833, 2007.
52. Hosoda T, D'Amario D, Cabral-Da-Silva MC, Zheng H, Padin-Iruegas ME, Ogorek B, Ferreira-Martins J, Yasuzawa-Amano S, Amano K, Ide-Iwata N, Cheng W, Rota M, Urbanek K, Kajstura J, Anversa P, and Leri A. Clonality of mouse and human cardiomyogenesis in vivo. Proc Natl Acad Sci USA 106: 17169-17174, 2009.
53. Huang X, Cho S, and Spangrude GJ. Hematopoietic stem cells: generation and self-renewal. Cell Death Differ 14: 1851-1859, 2007.
54. Huss JM and Kelly DP. Nuclear receptor signaling and cardiac energetics. Circ Res 95: 568-578, 2004.
55. Ishii Y, Langberg J, Rosborough K, and Mikawa T. Endothelial cell lineages of the heart. Cell Tissue Res 335: 67-73, 2009.
56. Itou J, Oishi I, Kawakami H, Glass TJ, Richter J, Johnson A, Lund TC, and Kawakami Y. Migration of cardiomyocytes is essential for heart regeneration in zebrafish. Development 139: 4133-4142, 2012.
57. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, and Semenza GL. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12: 149-162, 1998.
58. Jang YY and Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110: 3056-3063, 2007.
59. Jennings RB and Reimer KA. Acute myocardial ischemia: effects of reperfusion with arterial blood. Artif Cells Blood Substit Immobil Biotechnol 22: 253-278, 1994.
60. Jo JO, Kim SR, Bae MK, Kang YJ, Ock MS, Kleinman HK, and Cha HJ. Thymosin beta4 induces the expression of vascular endothelial growth factor (VEGF) in a hypoxia-inducible factor (HIF)-1alpha-dependent manner. Biochim Biophys Acta 1803: 1244-1251, 2010.
61. Jopling C, Sleep E, Raya M, Marti M, Raya A, and Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464: 606-609, 2010.
62. Jopling C, Sune G, Faucherre A, Fabregat C, and Izpisua Belmonte JC. Hypoxia induces myocardial regeneration in zebrafish. Circulation 126: 3017-3027, 2012.
63. Jordan CT, McKearn JP, and Lemischka IR. Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61: 953-963, 1990.
64. Jurgensen JS, Rosenberger C, Wiesener MS, Warnecke C, Horstrup JH, Grafe M, Philipp S, Griethe W, Maxwell PH, Frei U, Bachmann S, Willenbrock R, and Eckardt KU. Persistent induction of HIF-1alpha and-2alpha in cardiomyocytes and stromal cells of ischemic myocardium. FASEB J 18: 1415-1417, 2004.
65. Kajstura J, Gurusamy N, Ogorek B, Goichberg P, Clavo-Rondon C, Hosoda T, D'Amario D, Bardelli S, Beltrami AP, Cesselli D, Bussani R, del Monte F, Quaini F, Rota M, Beltrami CA, Buchholz BA, Leri A, and Anversa P. Myocyte turnover in the aging human heart. Circ Res 107: 1374-1386, 2010.
66. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, and Conaway JW. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci USA 97: 10430-10435, 2000.
67. Katare R, Oikawa A, Cesselli D, Beltrami AP, Avolio E, Muthukrishnan D, Munasinghe PE, Angelini G, Emanueli C, and Madeddu P. Boosting the pentose phosphate pathway restores cardiac progenitor cell availability in diabetes. Cardiovasc Res 97: 55-65, 2012.
68. Kato K, Yoshimoto M, Kato K, Adachi S, Yamayoshi A, Arima T, Asanoma K, Kyo S, Nakahata T, and Wake N. Characterization of side-population cells in human normal endometrium. Hum Reprod 22: 1214-1223, 2007.
69. Khan M, Mohsin S, Avitabile D, Siddiqi S, Nguyen J, Wallach K, Quijada P, McGregor M, Gude N, Alvarez R, Tilley DG, Koch WJ, and Sussman MA. beta-Adrenergic regulation of cardiac progenitor cell death versus survival and proliferation. Circ Res 112: 476-486, 2013.
70. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DY, and Poss KD. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464: 601-605, 2010.
71. Kimura W and Sadek HA. The cardiac hypoxic niche: emerging role of hypoxic microenvironment in cardiac progenitors. Cardiovasc Diagn Ther 2: 278-289, 2012.
72. Klaunig JE and Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44: 239-267, 2004.
73. Kobayashi CI and Suda T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol 227: 421-430, 2011.
74. Kocabas F, Mahmoud AI, Sosic D, Porrello ER, Chen R, Garcia JA, Deberardinis RJ, and Sadek HA. The hypoxic epicardial and subepicardial microenvironment. J Cardiovasc Transl Res 5: 654-665, 2012.
75. Kocabas F, Zheng J, Thet S, Copeland NG, Jenkins NA, Deberardinis RJ, Zhang C, and Sadek HA. Meis1 regulates the metabolic phenotype and oxidant defense of hematopoietic stem cells. Blood 120: 4963-4972, 2012.
76. Koitabashi N, Arai M, Tomaru K, Takizawa T, Watanabe A, Niwano K, Yokoyama T, Wuytack F, Periasamy M, Nagai R, and Kurabayashi M. Carvedilol effectively blocks oxidative stress-mediated downregulation of sarcoplasmic reticulum Ca2 +-ATPase 2 gene transcription through modification of Sp1 binding. Biochem Biophys Res Commun 328: 116-124, 2005.
77. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, and Willems PH. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470, 2010.
78. Krishnamurthy P, Ross DD, Nakanishi T, Bailey-Dell K, Zhou S, Mercer KE, Sarkadi B, Sorrentino BP, and Schuetz JD. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 279: 24218-24225, 2004.
79. Laflamme MA and Murry CE. Regenerating the heart. Nat Biotechnol 23: 845-856, 2005.
80. Laflamme MA and Murry CE. Heart regeneration. Nature 473: 326-335, 2011.
81. Levy NS, Chung S, Furneaux H, and Levy AP. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273: 6417-6423, 1998.
82. Li F, Wang X, Capasso JM, and Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 28: 1737-1746, 1996.
83. Li TS, Cheng K, Lee ST, Matsushita S, Davis D, Malliaras K, Zhang Y, Matsushita N, Smith RR, and Marban E. Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells 28: 2088-2098, 2010.
84. Li TS, Cheng K, Malliaras K, Matsushita N, Sun B, Marban L, Zhang Y, and Marban E. Expansion of human cardiac stem cells in physiological oxygen improves cell production efficiency and potency for myocardial repair. Cardiovasc Res 89: 157-165, 2011.
85. Li TS and Marban E. Physiological levels of reactive oxygen species are required to maintain genomic stability in stem cells. Stem Cells 28: 1178-1185, 2010.
86. Lie-Venema H, van den Akker NM, Bax NA, Winter EM, Maas S, Kekarainen T, Hoeben RC, deRuiter MC, Poelmann RE, and Gittenberger-de Groot AC. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. ScientificWorldJournal 7: 1777-1798, 2007.
87. Loffredo FS, Steinhauser ML, Gannon J, and Lee RT. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 8: 389-398, 2011.
88. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S, Bruce C, Shields BJ, Skiba B, Ooms LM, Stepto N, Wu B, Mitchell CA, Tonks NK, Watt MJ, Febbraio MA, Crack PJ, Andrikopoulos S, and Tiganis T. Reactive oxygen species enhance insulin sensitivity. Cell Metab 10: 260-272, 2009.
89. Lopaschuk GD and Jaswal JS. Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J Cardiovasc Pharmacol 56: 130-140, 2010.
90. Mahmoud AI, Kocabas F, Muralidhar SA, Kimura W, Koura AS, Thet S, Porrello ER, and Sadek HA. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 497: 249-253, 2013.
91. Majmundar AJ, Wong WJ, and Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40: 294-309, 2010.
92. Malinda KM, Goldstein AL, and Kleinman HK. Thymosin beta 4 stimulates directional migration of human umbilical vein endothelial cells. FASEB J 11: 474-481, 1997.
93. Marnett LJ, Riggins JN, and West JD. Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest 111: 583-593, 2003.
94. Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, Wada H, Sano M, Toko H, Akazawa H, Sato T, Nakaya H, Kasanuki H, and Komuro I. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279: 11384-11391, 2004.
95. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, and Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
96. Maynard MA, Evans AJ, Hosomi T, Hara S, Jewett MA, and Ohh M. Human HIF-3alpha4 is a dominant-negative regulator of HIF-1 and is down-regulated in renal cell carcinoma. FASEB J 19: 1396-1406, 2005.
97. McClung JP, Roneker CA, Mu W, Lisk DJ, Langlais P, Liu F, and Lei XG. Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci USA 101: 8852-8857, 2004.
98. Medvinsky A, Rybtsov S, and Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development 138: 1017-1031, 2011.
99. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M, Vivarelli E, Frati L, Cossu G, and Giacomello A. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95: 911-921, 2004.
100. Mirotsou M, Jayawardena TM, Schmeckpeper J, Gnecchi M, and Dzau VJ. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol 50: 280-289, 2011.
101. Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, Yamazaki S, Matsuoka S, Miyamoto T, Ito K, Ohmura M, Chen C, Hosokawa K, Nakauchi H, Nakayama K, Nakayama KI, Harada M, Motoyama N, Suda T, and Hirao A. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1: 101-112, 2007.
102. Mollova M, Bersell K, Walsh S, Savla J, Das LT, Park SY, Silberstein LE, Dos Remedios CG, Graham D, Colan S, and Kuhn B. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA 110: 1446-1451, 2012.
103. Moos PJ, Edes K, and Fitzpatrick FA. Inactivation of wild-type p53 tumor suppressor by electrophilic prostaglandins. Proc Natl Acad Sci USA 97: 9215-9220, 2000.
104. Nassar R, Reedy MC, and Anderson PA. Developmental changes in the ultrastructure and sarcomere shortening of the isolated rabbit ventricular myocyte. Circ Res 61: 465-483, 1987.
105. Ogasawara MA and Zhang H. Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid Redox Signal 11: 1107-1122, 2009.
106. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, and Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100: 12313-12318, 2003.
107. Olivetti G, Cigola E, Maestri R, Corradi D, Lagrasta C, Gambert SR, and Anversa P. Aging, cardiac hypertrophy and ischemic cardiomyopathy do not affect the proportion of mononucleated and multinucleated myocytes in the human heart. J Mol Cell Cardiol 28: 1463-1477, 1996.
108. Owusu-Ansah E and Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461: 537-541, 2009.
109. Oyama T, Nagai T, Wada H, Naito AT, Matsuura K, Iwanaga K, Takahashi T, Goto M, Mikami Y, Yasuda N, Akazawa H, Uezumi A, Takeda S, and Komuro I. Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes in vitro and in vivo. J Cell Biol 176: 329-341, 2007.
110. Parmar K, Mauch P, Vergilio JA, Sackstein R, and Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 104: 5431-5436, 2007.
111. Passier R, van Laake LW, and Mummery CL. Stem-cellbased therapy and lessons from the heart. Nature 453: 322-329, 2008.
112. Perrelli MG, Pagliaro P, and Penna C. Ischemia/reperfusion injury and cardioprotective mechanisms: role of mitochondria and reactive oxygen species. World J Cardiol 3: 186-200, 2011.
113. Pfister O, Mouquet F, Jain M, Summer R, Helmes M, Fine A, Colucci WS, and Liao R. CD31-but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97: 52-61, 2005.
114. Pfister O, Oikonomopoulos A, Sereti KI, Sohn RL, Cullen D, Fine GC, Mouquet F, Westerman K, and Liao R. Role of the ATP-binding cassette transporter Abcg2 in the phenotype and function of cardiac side population cells. Circ Res 103: 825-835, 2008.
115. Porrello ER, Johnson BA, Aurora AB, Simpson E, Nam YJ, Matkovich SJ, Dorn GW, 2nd, van Rooij E, and Olson EN. MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ Res 109: 670-679, 2013.
116. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, and Sadek HA. Transient regenerative potential of the neonatal mouse heart. Science 331: 1078-1080, 2011.
117. Puceat M, Travo P, Quinn MT, and Fort P. A dual role of the GTPase Rac in cardiac differentiation of stem cells. Mol Biol Cell 14: 2781-2792, 2003.
118. Puente BN, Kimura W, Muralidhar SA, Moon J, Amatruda JF, Phelps KL, Grinsfelder D, Rothermel BA, Chen R, Garcia JA, Santos CX, Thet S, Mori E, Kinter MT, Rindler PM, Zacchigna S, Mukherjee S, Chen DJ, Mahmoud AI, Giacca M, Rabinovitch PS, Aroumougame A, Shah AM, Szweda LI, and Sadek HA. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157: 565-579, 2014.
119. Qiu FY, Song XX, Zheng H, Zhao YB, and Fu GS. Thymosin beta4 induces endothelial progenitor cell migration via PI3K/Akt/eNOS signal transduction pathway. J Cardiovasc Pharmacol 53: 209-214, 2009.
120. Rota M, LeCapitaine N, Hosoda T, Boni A, De Angelis A, Padin-Iruegas ME, Esposito G, Vitale S, Urbanek K, Casarsa C, Giorgio M, Luscher TF, Pelicci PG, Anversa P, Leri A, and Kajstura J. Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene. Circ Res 99: 42-52, 2006.
121. Rudolph AM and Heyman MA. Fetal and neonatal circulation and respiration. Annu Rev Physiol 36: 187-207, 1974.
122. Ruzankina Y, Asare A, and Brown EJ. Replicative stress, stemcells and aging. Mech Ageing Dev 129: 460-466, 2008.
123. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, and Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 105: 6392-6397, 2008.
124. Salceda S and Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitinproteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 272: 22642-22647, 1997.
125. Salih DA and Brunet A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr Opin Cell Biol 20: 126-136, 2008.
126. Sanada F, Kim J, Czarna A, Chan NY, Signore S, Ogorek B, Isobe K, Wybieralska E, Borghetti G, Pesapane A, Sorrentino A, Mangano E, Cappetta D, Mangiaracina C, Ricciardi M, Cimini M, Ifedigbo E, Perrella MA, Goichberg P, Choi AM, Kajstura J, Hosoda T, Rota M, Anversa P, and Leri A. c-Kit-positive cardiac stem cells nested in hypoxic niches are activated by stem cell factor reversing the aging myopathy. Circ Res 114: 41-55, 2013.
127. Sandstedt J, Jonsson M, Kajic K, Sandstedt M, Lindahl A, Dellgren G, Jeppsson A, and Asp J. Left atrium of the human adult heart contains a population of side population cells. Basic Res Cardiol 107: 255, 2012.
128. Santos CX, Anilkumar N, Zhang M, Brewer AC, and Shah AM. Redox signaling in cardiac myocytes. Free Radic Biol Med 50: 777-793, 2011.
129. Sauer H, Rahimi G, Hescheler J, and Wartenberg M. Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells. FEBS Lett 476: 218-223, 2000.
130. Schmelter M, Ateghang B, Helmig S, Wartenberg M, and Sauer H. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 20: 1182-1184, 2006.
131. Schofield R. The relationship between the spleen colonyforming cell and the haemopoietic stem cell. Blood Cells 4: 7-25, 1978.
132. Schulz C, von Andrian UH, and Massberg S. Hematopoietic stem and progenitor cells: their mobilization and homing to bone marrow and peripheral tissue. Immunol Res 44: 160-168, 2009.
133. Scortegagna M, Ding K, Oktay Y, Gaur A, Thurmond F, Yan LJ, Marck BT, Matsumoto AM, Shelton JM, Richardson JA, Bennett MJ, and Garcia JA. Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/-mice. Nat Genet 35: 331-340, 2003.
134. Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33: 207-214, 2012.
135. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, Wu TD, Guerquin-Kern JL, Lechene CP, and Lee RT. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493: 433-436, 2013.
136. Seshadri G, Che PL, Boopathy AV, and Davis ME. Characterization of superoxide dismutases in cardiac progenitor cells demonstrates a critical role for manganese superoxide dismutase. Stem Cells Dev 21: 3136-3146, 2012.
137. Shao L, Li H, Pazhanisamy SK, Meng A, Wang Y, and Zhou D. Reactive oxygen species and hematopoietic stem cell senescence. Int J Hematol 94: 24-32, 2011.
138. Shiozawa Y, Havens AM, Pienta KJ, and Taichman RS. The bone marrow niche: habitat to hematopoietic and mesenchymal stem cells, and unwitting host to molecular parasites. Leukemia 22: 941-950, 2008.
139. Signer RA and Morrison SJ. Mechanisms that regulate stem cell aging and life span. Cell Stem Cell 12: 152-165, 2013.
140. Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zhang CC, and Sadek HA. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7: 380-390, 2010.
141. Smart N, Bollini S, Dube KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, and Riley PR. De novo cardiomyocytes from within the activated adult heart after injury. Nature 474: 640-644, 2011.
142. Smart N, Dube KN, and Riley PR. Epicardial progenitor cells in cardiac regeneration and neovascularisation. Vascul Pharmacol 58: 164-73, 2013.
143. Smart N, Risebro CA, Clark JE, Ehler E, Miquerol L, Rossdeutsch A, Marber MS, and Riley PR. Thymosin beta4 facilitates epicardial neovascularization of the injured adult heart. Ann N Y Acad Sci 1194: 97-104, 2010.
144. Soonpaa MH and Field LJ. Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. Am J Physiol 272: H220-H226, 1997.
145. Soonpaa MH, Kim KK, Pajak L, Franklin M, and Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271: H2183-H2189, 1996.
146. Spradling A, Drummond-Barbosa D, and Kai T. Stem cells find their niche. Nature 414: 98-104, 2001.
147. Stanley WC, Recchia FA, and Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85: 1093-1129, 2005.
148. Su H, Arakawa-Hoyt J, and Kan YW. Adeno-associated viral vector-mediated hypoxia response element-regulated gene expression in mouse ischemic heart model. Proc Natl Acad Sci USA 99: 9480-9485, 2002.
149. Suarez-Alvarez B, Lopez-Vazquez A, and Lopez-Larrea C. Mobilization and homing of hematopoietic stem cells. Adv Exp Med Biol 741: 152-170, 2012.
150. Suda T, Takubo K, and Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9: 298-310, 2011.
151. Summer R, Kotton DN, Sun X, Ma B, Fitzsimmons K, and Fine A. Side population cells and Bcrp1 expression in lung. Am J Physiol Lung Cell Mol Physiol 285: L97-L104, 2003.
152. Takamiya M, Haider KH, and Ashraf M. Identification and characterization of a novel multipotent sub-population of Sca-1(+) cardiac progenitor cells for myocardial regeneration. PLoS One 6: e25265, 2011.
153. Takimoto E and Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 49: 241-248, 2007.
154. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, and Suda T. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7: 391-402, 2010.
155. Takubo K, Nagamatsu G, Kobayashi CI, Nakamura-Ishizu A, Kobayashi H, Ikeda E, Goda N, Rahimi Y, Johnson RS, Soga T, Hirao A, Suematsu M, and Suda T. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12: 49-61, 2013.
156. Takubo K and Suda T. Roles of the hypoxia response system in hematopoietic and leukemic stem cells. Int J Hematol 95: 478-483, 2012.
157. Tothova Z and Gilliland DG. FoxO transcription factors and stem cell homeostasis: insights from the hematopoietic system. Cell Stem Cell 1: 140-152, 2007.
158. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, McDowell EP, Lazo-Kallanian S, Williams IR, Sears C, Armstrong SA, Passegue E, DePinho RA, and Gilliland DG. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339, 2007.
159. Uchida S, De Gaspari P, Kostin S, Jenniches K, Kilic A, Izumiya Y, Shiojima I, Grosse Kreymborg K, Renz H, Walsh K, and Braun T. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Reports 1: 397-410, 2013.
160. Ueno H and Weissman IL. The origin and fate of yolk sac hematopoiesis: application of chimera analyses to developmental studies. Int J Dev Biol 54: 1019-1031, 2010.
161. Unnisa Z, Clark JP, Roychoudhury J, Thomas E, Tessarollo L, Copeland NG, Jenkins NA, Grimes HL, and Kumar AR. Meis1 preserves hematopoietic stem cells in mice by limiting oxidative stress. Blood 120: 4973-4981, 2012.
162. Unno K, Jain M, and Liao R. Cardiac side population cells: moving toward the center stage in cardiac regeneration. Circ Res 110: 1355-1363, 2012.
163. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SC, Middleton RC, Marban E, and Molkentin JD. c-kit + cells minimally contribute cardiomyocytes to the heart. Nature 509: 337-341, 2014.
164. Wagner KD, Wagner N, Wellmann S, Schley G, Bondke A, Theres H, and Scholz H. Oxygen-regulated expression of the Wilms' tumor suppressor Wt1 involves hypoxiainducible factor-1 (HIF-1). FASEB J 17: 1364-1366, 2003.
165. Walsh S, Ponten A, Fleischmann BK, and Jovinge S. Cardiomyocyte cell cycle control and growth estimation in vivo-an analysis based on cardiomyocyte nuclei. Cardiovasc Res 86: 365-373, 2010.
166. Warren LA and Rossi DJ. Stem cells and aging in the hematopoietic system. Mech Ageing Dev 130: 46-53, 2009.
167. Wei C, Kumar S, Kim IK, and Gupta S. Thymosin beta 4 protects cardiomyocytes from oxidative stress by targeting anti-oxidative enzymes and anti-apoptotic genes. PLoS One 7: e42586, 2012.
168. Weksberg DC, Chambers SM, Boles NC, and Goodell MA. CD150-side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood 111: 2444-2451, 2008.
169. Wheaton WW and Chandel NS. Hypoxia. 2. Hypoxia regulates cellular metabolism. Am J Physiol Cell Physiol 300: C385-C393, 2011.
170. Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549-561, 2008.
171. Wu Y and Wu EX. MR study of postnatal development of myocardial structure and left ventricular function. J Magn Reson Imaging 30: 47-53, 2009.
172. Yalcin S, Zhang X, Luciano JP, Mungamuri SK, Marinkovic D, Vercherat C, Sarkar A, Grisotto M, Taneja R, and Ghaffari S. Foxo3 is essential for the regulation of ataxia telangiectasia mutated and oxidative stress-mediated homeostasis of hematopoietic stem cells. J Biol Chem 283: 25692-25705, 2008.
173. Yan F, Yao Y, Chen L, Li Y, Sheng Z, and Ma G. Hypoxic preconditioning improves survival of cardiac progenitor cells: role of stromal cell derived factor-1alpha-CXCR4 axis. PLoS One 7: e37948, 2012.
174. Yang Y and Loscalzo J. S-nitrosoprotein formation and localization in endothelial cells. Proc Natl Acad Sci USA 102: 117-122, 2005.
175. Yellon DM and Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med 357: 1121-1135, 2007.
176. Yu WM, Liu X, Shen J, Jovanovic O, Pohl EE, Gerson SL, Finkel T, Broxmeyer HE, and Qu CK. Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell 12: 62-74, 2013.
177. Yusuf S, Dagenais G, Pogue J, Bosch J, and Sleight P. Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 342: 154-160, 2000.
178. Zhang J and Ju Z. Telomere, DNA damage, and oxidative stress in stem cell aging. Birth Defects Res C Embryo Today 90: 297-307, 2010.
179. Zhou B, Honor LB, He H, Ma Q, Oh JH, Butterfield C, Lin RZ, Melero-Martin JM, Dolmatova E, Duffy HS, Gise A, Zhou P, Hu YW, Wang G, Zhang B, Wang L, Hall JL, Moses MA, McGowan FX, and Pu WT. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J Clin Invest 121: 1894-1904, 2011.
180. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, and Pu WT. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109-113, 2008.