Cardiomyocyte proliferation in cardiac development and regeneration: A guide to methodologies and interpretations

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 8, 2015, Pages H1237-H1250

  Leone, Marina ^a   Magadum, Ajit ^b   Engel, Felix B ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac regeneration; Cardiomyocyte proliferation; Newt; Zebrafish

Indexed keywords

AURORA A KINASE; HISTONE H3; KI 67 ANTIGEN; NUCLEOTIDE DERIVATIVE;

ANAPHASE; ANIMAL CELL; CELL CLONING; CELL COUNT; CELL CYCLE ARREST; CELL CYCLE ASSAY; CELL DEDIFFERENTIATION; CELL PROLIFERATION; COLORIMETRY; CYTOKINESIS; DNA REPLICATION; DNA SYNTHESIS; ENDURANCE TRAINING; FETUS DEVELOPMENT; FLUORESCENCE ACTIVATED CELL SORTING; HEART DEVELOPMENT; HEART FUNCTION; HEART HYPERTROPHY; HEART INJURY; HEART MUSCLE CELL; HISTONE PHOSPHORYLATION; HUMAN; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; REVIEW; SARCOMERE; ZEBRA FISH; ANIMAL; ANIMAL MODEL; BIOASSAY; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; HEART; HEART DISEASE; MEDICAL RESEARCH; METABOLISM; ORGANOGENESIS; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; REGENERATION; SALAMANDRIDAE; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL ASSAY; BIOMEDICAL RESEARCH; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; HEART; HEART DISEASES; HUMANS; MODELS, ANIMAL; MYOCYTES, CARDIAC; ORGANOGENESIS; REGENERATION; SALAMANDRIDAE; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84944411659     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00559.2015     Document Type: Review

References (132)

1. Adler CP, Friedburg H, Herget GW, Neuburger M, Schwalb H. Variability of cardiomyocyte DNA content, ploidy level and nuclear number in mammalian hearts. Virchows Arch 429: 159–164, 1996.
2. Aguirre A, Montserrat N, Zacchigna S, Nivet E, Hishida T, Krause MN, Kurian L, Ocampo A, Vazquez-Ferrer E, Rodriguez-Esteban C, Kumar S, Moresco JJ, Yates JR, Campistol JM, Sancho-Martinez I, Giacca M, Izpisua Belmonte JC. In vivo activation of a conserved microRNA program induces mammalian heart regeneration. Cell Stem Cell 15: 589–604, 2014.
3. Ahuja P, Perriard E, Perriard JC, Ehler E. Sequential myofibrillar breakdown accompanies mitotic division of mammalian cardiomyocytes. J Cell Sci 117: 3295–3306, 2004.
4. Ali SR, Hippenmeyer S, Saadat LV, Luo L, Weissman IL, Ardehali R. Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice. Proc Natl Acad Sci USA 111: 8850–8855, 2014.
5. Andersen DC, Ganesalingam S, Jensen CH, Sheikh SP. Do neonatal mouse hearts regenerate following heart apex resection? Stem Cell Reports 2: 406–413, 2014.
6. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel- Duby R, Sadek HA, Olson EN. Macrophages are required for neonatal heart regeneration. J Clin Invest 124: 1382–1392, 2014.
7. Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 91: 279–288, 2011.
8. Banerjee I, Fuseler JW, Price RL, Borg TK, Baudino TA. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293: H1883–H1891, 2007.
9. Becker RO, Chapin S, Sherry R. Regeneration of the ventricular myocardium in amphibians. Nature 248: 145–147, 1974.
10. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science 324: 98–102, 2009.
11. Bergmann O, Zdunek S, Felker A, Salehpour M, Alkass K, Bernard S, Sjostrom SL, Szewczykowska M, Jackowska T, Dos Remedios C, Malm T, Andra M, Jashari R, Nyengaard JR, Possnert G, Jovinge S, Druid H, Frisen J. Dynamics of cell generation and turnover in the human heart. Cell 161: 1566–1575, 2015.
12. Bettencourt-Dias M, Mittnacht S, Brockes JP. Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J Cell Sci 116: 4001–4009, 2003.
13. Bishop SP, Hine P. Carciac muscle cytoplasmic and nuclear development during canine neonatal growth. Recent Adv Stud Card Struct Metab 8: 77–98, 1975.
14. Borchardt T, Braun T. Cardiovascular regeneration in non-mammalian model systems: what are the differences between newts and man? Thromb Haemost 98: 311–318, 2007.
15. Borchardt T, Looso M, Bruckskotten M, Weis P, Kruse J, Braun T. Analysis of newly established EST databases reveals similarities between heart regeneration in newt and fish. BMC Genomics 11: 4, 2010.
16. Brockes JP, Kumar A. Appendage regeneration in adult vertebrates and implications for regenerative medicine. Science 310: 1919–1923, 2005.
17. Brodsky V, Sarkisov DS, Arefyeva AM, Panova NW, Gvasava IG. Polyploidy in cardiac myocytes of normal and hypertrophic human hearts; range of values. Virchows Arch 424: 429–435, 1994.
18. Brown DC, Gatter KC. Ki67 protein: the immaculate deception? Histopathology 40: 2–11, 2002.
19. Bryant DM, O’Meara CC, Ho NN, Gannon J, Cai L, Lee RT. A systematic analysis of neonatal mouse heart regeneration after apical resection. J Mol Cell Cardiol 79: 315–318, 2015.
20. Burton PB, Raff MC, Kerr P, Yacoub MH, Barton PJ. An intrinsic timer that controls cell-cycle withdrawal in cultured cardiac myocytes. Dev Biol 216: 659–670, 1999.
21. Chablais F, Veit J, Rainer G, Jazwinska A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev Biol 11: 21, 2011.
22. Chen CH, Durand E, Wang J, Zon LI, Poss KD. Zebraflash transgenic lines for in vivo bioluminescence imaging of stem cells and regeneration in adult zebrafish. Development 140: 4988–4997, 2013.
23. Chottova Dvorakova M, Wiegand S, Pesta M, Slavikova J, Grau V, Reischig J, Kuncova J, Kummer W. Expression of neuropeptide Y and its receptors Y1 and Y2 in the rat heart and its supplying autonomic and spinal sensory ganglia in experimentally induced diabetes. Neuroscience 151: 1016–1028, 2008.
24. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, Sen S, Allis CD, Sassone-Corsi P. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22: 874–885, 2002.
25. Curado S, Anderson RM, Jungblut B, Mumm J, Schroeter E, Stainier DY. Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn 236: 1025–1035, 2007.
26. Darehzereshki A, Rubin N, Gamba L, Kim J, Fraser J, Huang Y, Billings J, Mohammadzadeh R, Wood J, Warburton D, Kaartinen V, Lien CL. Differential regenerative capacity of neonatal mouse hearts after cryoinjury. Dev Biol 399: 91–99, 2014.
27. Drenckhahn JD, Schwarz QP, Gray S, Laskowski A, Kiriazis H, Ming Z, Harvey RP, Du XJ, Thorburn DR, 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.
28. Drenckhahn JD, Strasen J, Heinecke K, Langner P, Yin KV, Skole F, Hennig M, Spallek B, Fischer R, Blaschke F, Heuser A, Cox TC, Black MJ, Thierfelder L. Impaired myocardial development resulting in neonatal cardiac hypoplasia alters postnatal growth and stress response in the heart. Cardiovasc Res 106: 43–54, 2015.
29. Ebelt H, Hufnagel N, Neuhaus P, Neuhaus H, Gajawada P, Simm A, Muller-Werdan U, Werdan K, Braun T. Divergent siblings: E2F2 and E2F4 but not E2F1 and E2F3 induce DNA synthesis in cardiomyocytes without activation of apoptosis. Circ Res 96: 509–517, 2005.
30. Endl E, Gerdes J. The Ki-67 protein: fascinating forms and an unknown function. Exp Cell Res 257: 231–237, 2000.
31. Engel FB. Cardiomyocyte proliferation: a platform for mammalian cardiac repair. Cell Cycle 4: 1360–1363, 2005.
32. Engel FB, Hsieh PC, Lee RT, Keating MT. FGF1/p38 MAP kinase inhibitor therapy induces cardiomyocyte mitosis, reduces scarring, and rescues function after myocardial infarction. Proc Natl Acad Sci USA 103: 15546–15551, 2006.
33. Engel FB, Schebesta M, Duong MT, Lu G, Ren S, Madwed JB, Jiang H, Wang Y, Keating MT. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 19: 1175–1187, 2005.
34. Engel FB, Schebesta M, Keating MT. Anillin localization defect in cardiomyocyte binucleation. J Mol Cell Cardiol 41: 601–612, 2006.
35. Fang Y, Gupta V, Karra R, Holdway JE, Kikuchi K, Poss KD. Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proc Natl Acad Sci USA 110: 13416–13421, 2013.
36. Field CM, Alberts BM. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131: 165–178, 1995.
37. Fraticelli A, Josephson R, Danziger R, Lakatta E, Spurgeon H. Morphological and contractile characteristics of rat cardiac myocytes from maturation to senescence. Am J Physiol Heart Circ Physiol 257: H259–H265, 1989.
38. Gamba L, Harrison M, Lien CL. Cardiac regeneration in model organisms. Curr Treat Options Cardiovasc Med 16: 288, 2014.
39. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, 3rd Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB. Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation 129: e28–e292, 2014.
40. Gonzalez-Rosa JM, Guzman-Martinez G, Marques IJ, Sanchez-Iranzo H, Jimenez-Borreguero LJ, Mercader N. Use of echocardiography reveals reestablishment of ventricular pumping efficiency and partial ventricular wall motion recovery upon ventricular cryoinjury in the zebrafish. PLoS One 9: e115604, 2014.
41. Goss RJ. The natural history (and mystery) of regeneration. In: A History of Regeneration Research: Milestones in the Evolution of a Science. Cambridge, UK: Cambridge University Press, 1991.
42. Grabner W, Pfitzer P. Number of nuclei in isolated myocardial cells of pigs. Virchows Arch B Cell Pathol Incl Mol Pathol 15: 279–294, 1974.
43. Gupta V, Gemberling M, Karra R, Rosenfeld GE, Evans T, Poss KD. An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr Biol 23: 1221–1227, 2013.
44. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348–360, 1997.
45. Herget GW, Neuburger M, Plagwitz R, Adler CP. DNA content, ploidy level and number of nuclei in the human heart after myocardial infarction. Cardiovasc Res 36: 45–51, 1997.
46. Higuchi K, Hashizume H, Aizawa Y, Ushiki T. Scanning electron microscopic studies of the vascular smooth muscle cells and pericytes in the rat heart. Arch Histol Cytol 63: 115–126, 2000.
47. Hou J, Kang YJ. Regression of pathological cardiac hypertrophy: signaling pathways and therapeutic targets. Pharmacol Ther 135: 337–354, 2012.
48. Hu N, Yost HJ, Clark EB. Cardiac morphology and blood pressure in the adult zebrafish. Anat Rec 264: 1–12, 2001.
49. Huang Y, Harrison MR, Osorio A, Kim J, Baugh A, Duan C, Sucov HM, Lien CL. Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS One 8: e67266, 2013.
50. Itou J, Oishi I, Kawakami H, Glass TJ, Richter J, Johnson A, Lund TC, Kawakami Y. Migration of cardiomyocytes is essential for heart regeneration in zebrafish. Development 139: 4133–4142, 2012.
51. Jesty SA, Steffey MA, Lee FK, Breitbach M, Hesse M, Reining S, Lee JC, Doran RM, Nikitin AY, Fleischmann BK, Kotlikoff MI. c-kit_precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc Natl Acad Sci USA 109: 13380–13385, 2012.
52. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464: 606–609, 2010.
53. Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell 20: 397–404, 2011.
54. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DY, Poss KD. Primary contribution to zebrafish heart regeneration by gata4(_) cardiomyocytes. Nature 464: 601–605, 2010.
55. Kimura W, Xiao F, Canseco DC, Muralidhar S, Thet S, Zhang HM, Abderrahman Y, Chen R, Garcia JA, Shelton JM, Richardson JA, Ashour AM, Asaithamby A, Liang H, Xing C, Lu Z, Zhang CC, Sadek HA. Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart. Nature 523: 226–230, 2015.
56. Konfino T, Landa N, Ben-Mordechai T, Leor J. The type of injury dictates the mode of repair in neonatal and adult heart. J Am Heart Assoc 4: e001320, 2015.
57. Kostin S, Hein S, Arnon E, Scholz D, Schaper J. The cytoskeleton and related proteins in the human failing heart. Heart Fail Rev 5: 271–280, 2000.
58. Kuhn B, del Monte F, Hajjar RJ, Chang YS, Lebeche D, Arab S, Keating MT. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 13: 962–969, 2007.
59. Lavine KJ, Epelman S, Uchida K, Weber KJ, Nichols CG, Schilling JD, Ornitz DM, Randolph GJ, Mann DL. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc Natl Acad Sci USA 111: 16029–16034, 2014.
60. Lenhoff SG, Lenhoff HM. Hydra and the Birth of Experimental Biology, 1744: Abraham Trembley’s Memoires Concerning the Polyps. Pacific Grove, CA: Boxwood, 1986.
61. Li F, Wang X, Capasso JM, Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 28: 1737–1746, 1996.
62. Li P, Cavallero S, Gu Y, Chen TH, Hughes J, Hassan AB, Bruning JC, Pashmforoush M, Sucov HM. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138: 1795–1805, 2011.
63. Lien CL, Harrison MR, Tuan TL, Starnes VA. Heart repair and regeneration: recent insights from zebrafish studies. Wound Repair Regen 20: 638–646, 2012.
64. Lien CL, Schebesta M, Makino S, Weber GJ, Keating MT. Gene expression analysis of zebrafish heart regeneration. PLoS Biol 4: e260, 2006.
65. Lin Z, von Gise A, Zhou P, Gu F, Ma Q, Jiang J, Yau AL, Buck JN, Gouin KA, van Gorp PR, Zhou B, Chen J, Seidman JG, Wang DZ, Pu WT. Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ Res 115: 354–363, 2014.
66. Linke WA, Hamdani N. Gigantic business: titin properties and function through thick and thin. Circ Res 114: 1052–1068, 2014.
67. Liu N, Bezprozvannaya S, Williams AH, Qi X, Richardson JA, Bassel-Duby R, Olson EN. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev 22: 3242–3254, 2008.
68. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450: 56–62, 2007.
69. Looso M, Michel CS, Konzer A, Bruckskotten M, Borchardt T, Kruger M, Braun T. Spiked-in pulsed in vivo labeling identifies a new member of the CCN family in regenerating newt hearts. J Proteome Res 11: 4693–4704, 2012.
70. Looso M, Preussner J, Sousounis K, Bruckskotten M, Michel CS, Lignelli E, Reinhardt R, Hoffner S, Kruger M, Tsonis PA, Borchardt T, Braun T. A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration. Genome Biol 14: R16, 2013.
71. Lyons AB. Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Meth 243: 147–154, 2000.
72. Maes A, Flameng W, Nuyts J, Borgers M, Shivalkar B, Ausma J, Bormans G, Schiepers C, De Roo M, Mortelmans L. Histological alterations in chronically hypoperfused myocardium. Correlation with PET findings. Circulation 90: 735–745, 1994.
73. Mahmoud AI, Kocabas F, Muralidhar SA, Kimura W, Koura AS, Thet S, Porrello ER, Sadek HA. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 497: 249–253, 2013.
74. Malyshev II. [Mitotic activity of the myocardium in early ontogenesis of rabbits after minor mechanical injury to the heart]. Biull Eksp Biol Med 97: 734–736, 1984.
75. Malyshev II. [The recovery process in the fetal rabbit myocardium following mechanical trauma]. Biull Eksp Biol Med 80: 111–113, 1975.
76. Mann N, Rosenzweig A. Can exercise teach us how to treat heart disease? Circulation 126: 2625–2635, 2012.
77. Matz DG, Oberpriller JO, Oberpriller JC. Comparison of mitosis in binucleated and mononucleated newt cardiac myocytes. Anat Rec 251: 245–255, 1998.
78. Meckert PC, Rivello HG, Vigliano C, Gonzalez P, Favaloro R, Laguens R. Endomitosis and polyploidization of myocardial cells in the periphery of human acute myocardial infarction. Cardiovasc Res 67: 116–123, 2005.
79. Milani-Nejad N, Janssen PM. Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol Ther 141: 235–249, 2014.
80. Mollova M, Bersell K, Walsh S, Savla J, Das LT, Park SY, Silberstein LE, Dos Remedios CG, Graham D, Colan S, Kuhn B. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA 110: 1446–1451, 2013.
81. Moorman AF, Christoffels VM. Cardiac chamber formation: development, genes, and evolution. Physiol Rev 83: 1223–1267, 2003.
82. Naqvi N, Li M, Calvert JW, Tejada T, Lambert JP, Wu J, Kesteven SH, Holman SR, Matsuda T, Lovelock JD, Howard WW, Iismaa SE, Chan AY, Crawford BH, Wagner MB, Martin DI, Lefer DJ, Graham RM, Husain A. A proliferative burst during preadolescence establishes the final cardiomyocyte number. Cell 157: 795–807, 2014.
83. Nef HM, Mollmann H, Kostin S, Troidl C, Voss S, Weber M, Dill T, Rolf A, Brandt R, Hamm CW, Elsasser A. Tako-Tsubo cardiomyopathy: intraindividual structural analysis in the acute phase and after functional recovery. Eur Heart J 28: 2456–2464, 2007.
84. Neff AW, Dent AE, Armstrong JB. Heart development and regeneration in urodeles. Int J Dev Biol 40: 719–725, 1996.
85. Nemtsas P, Wettwer E, Christ T, Weidinger G, Ravens U. Adult zebrafish heart as a model for human heart? An electrophysiological study. J Mol Cell Cardiol 48: 161–171, 2010.
86. Noujaim SF, Lucca E, Munoz V, Persaud D, Berenfeld O, Meijler FL, Jalife J. From mouse to whale: a universal scaling relation for the PR Interval of the electrocardiogram of mammals. Circulation 110: 2802–2808, 2004.
87. Oberpriller J, Oberpriller JC. Mitosis in adult newt ventricle. J Cell Biol 49: 560–563, 1971.
88. Oberpriller JO, Oberpriller JC. Response of the adult newt ventricle to injury. J Exp Zool 187: 249–253, 1974.
89. Oberpriller JO, Oberpriller JC, Arefyeva AM, Mitashov VI, Carlson BM. Nuclear characteristics of cardiac myocytes following the proliferative response to mincing of the myocardium in the adult newt, Notophthalmus viridescens. Cell Tissue Res 253: 619–624, 1988.
90. Pauziene N, Pauza DH, Stropus R. Morphology of human intracardiac nerves: an electron microscope study. J Anat 197: 437–459, 2000.
91. Piatkowski T, Muhlfeld C, Borchardt T, Braun T. Reconstitution of the myocardium in regenerating newt hearts is preceded by transient deposition of extracellular matrix components. Stem Cells Dev 22: 1921–1931, 2013.
92. Piper HM, Jacobson SL, Schwartz P. Determinants of cardiomyocyte development in long-term primary culture. J Mol Cell Cardiol 20: 825–835, 1988.
93. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA. Transient regenerative potential of the neonatal mouse heart. Science 331: 1078–1080, 2011.
94. Porrello ER, Mahmoud AI, Simpson E, Johnson BA, Grinsfelder D, Canseco D, Mammen PP, Rothermel BA, Olson EN, Sadek HA. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci USA 110: 187–192, 2013.
95. Porrello ER, Olson EN. A neonatal blueprint for cardiac regeneration. Stem Cell Res 13: 556–570, 2014.
96. Poss KD. Getting to the heart of regeneration in zebrafish. Semin Cell Dev Biol 18: 36–45, 2007.
97. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science 298: 2188–2190, 2002.
98. 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, Sadek HA. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157: 565–579, 2014.
99. Réaumur RAF. Sur les diverses reproductions qui se font dans les Ecrevisse, les Omars, les Crabes, etc. et entr’autres sur celles de leurs Jambes et de leurs Ecailles. Memoirs Academic Royal Sciences 223–245, 1712.
100. Rosca MG, Tandler B, Hoppel CL. Mitochondria in cardiac hypertrophy and heart failure. J Mol Cell Cardiol 55: 31–41, 2013.
101. Sanchez Alvarado A. Regeneration in the metazoans: why does it happen? Bioessays 22: 578–590, 2000.
102. Sander V, Sune G, Jopling C, Morera C, Izpisua Belmonte JC. Isolation and in vitro culture of primary cardiomyocytes from adult zebrafish hearts. Nat Protoc 8: 800–809, 2013.
103. Sdek P, Zhao P, Wang Y, Huang CJ, Ko CY, Butler PC, Weiss JN, Maclellan WR. Rb and p130 control cell cycle gene silencing to maintain the postmitotic phenotype in cardiac myocytes. J Cell Biol 194: 407–423, 2011.
104. Senyo SE, Lee RT, Kuhn B. Cardiac regeneration based on mechanisms of cardiomyocyte proliferation and differentiation. Stem Cell Res 13: 532–541, 2014.
105. Shen H, Cavallero S, Estrada KD, Sandovici I, Kumar SR, Makita T, Lien CL, Constancia M, Sucov HM. Extracardiac control of embryonic cardiomyocyte proliferation and ventricular wall expansion. Cardiovasc Res 105: 271–8, 2015.
106. Sherman AJ, Klocke FJ, Decker RS, Decker ML, Kozlowski KA, Harris KR, Hedjbeli S, Yaroshenko Y, Nakamura S, Parker MA, Checchia PA, Evans DB. Myofibrillar disruption in hypocontractile myocardium showing perfusion-contraction matches and mismatches. Am J Physiol Heart Circ Physiol 278: H1320–H1334, 2000.
107. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol Heart Circ Physiol 271: H2183–H2189, 1996.
108. Soonpaa MH, Rubart M, Field LJ. Challenges measuring cardiomyocyte renewal. Biochim Biophys Acta 1833: 799–803, 2013.
109. Soufan AT, van den Berg G, Ruijter JM, de Boer PA, van den Hoff MJ, Moorman AF. Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ Res 99: 545–552, 2006.
110. Spahr R, Piper HM, Schwartz P, Probst I, Spieckermann PG. Morphological dedifferentiation of adult cardiac myocytes in coculture with hepatocytes. Basic Res Cardiol 80: 83–86, 1985.
111. Straight AF, Field CM, Mitchison TJ. Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol Biol Cell 16: 193–201, 2005.
112. Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR, Evans RM. RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev 8: 1007–1018, 1994.
113. Takeuchi T. Regulation of cardiomyocyte proliferation during development and regeneration. Dev Growth Diff 56: 402–409, 2014.
114. Tanaka EM. Regeneration: if they can do it, why can’t we? Cell 113: 559–562, 2003.
115. van Amerongen MJ, Engel FB. Features of cardiomyocyte proliferation and its potential for cardiac regeneration. J Cell Mol Med 12: 2233–2244, 2008.
116. VanDusen NJ, Casanovas J, Vincentz JW, Firulli BA, Osterwalder M, Lopez-Rios J, Zeller R, Zhou B, Grego-Bessa J, De La Pompa JL, Shou W, Firulli AB. Hand2 is an essential regulator for two notchdependent functions within the embryonic endocardium. Cell Rep 9: 2071–2083, 2014.
117. Vliegen HW, van der Laarse A, Cornelisse CJ, Eulderink F. Myocardial changes in pressure overload-induced left ventricular hypertrophy. A study on tissue composition, polyploidization and multinucleation. Eur Heart J 12: 488–494, 1991.
118. Wang F, Higgins JM. Histone modifications and mitosis: countermarks, landmarks, and bookmarks. Trends Cell Biol 23: 175–184, 2013.
119. Wang J, Panakova D, Kikuchi K, Holdway JE, Gemberling M, Burris JS, Singh SP, Dickson AL, Lin YF, Sabeh MK, Werdich AA, Yelon D, Macrae CA, Poss KD. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138: 3421–3430, 2011.
120. Wessels A, Sedmera D. Developmental anatomy of the heart: a tale of mice and man. Physiol Genomics 15: 165–176, 2003.
121. Wheatley SP, Carvalho A, Vagnarelli P, Earnshaw WC. INCENP is required for proper targeting of Survivin to the centromeres and the anaphase spindle during mitosis. Curr Biol 11: 886–890, 2001.
122. Wills AA, Holdway JE, Major RJ, Poss KD. Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 135: 183–192, 2008.
123. Witman N, Heigwer J, Thaler B, Lui WO, Morrison JI. miR-128 regulates non-myocyte hyperplasia, deposition of extracellular matrix and Islet1 expression during newt cardiac regeneration. Dev Biol 383: 253–263, 2013.
124. Witman N, Murtuza B, Davis B, Arner A, Morrison JI. Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. Dev Biol 354: 67–76, 2011.
125. Witman NM, Behm M, Ohman M, Morrison JI. ADAR-related activation of adenosine-to-inosine RNA editing during regeneration. Stem Cells Dev 22: 2254–2267, 2013.
126. Yin VP, Lepilina A, Smith A, Poss KD. Regulation of zebrafish heart regeneration by miR-133. Dev Biol 365: 319–327, 2012.
127. Yu F, Li R, Parks E, Takabe W, Hsiai TK. Electrocardiogram signals to assess zebrafish heart regeneration: implication of long QT intervals. Ann Biomed Eng 38: 2346–2357, 2010.
128. Zacchigna S, Giacca M. Extra- and intracellular factors regulating cardiomyocyte proliferation in postnatal life. Cardiovasc Res 102: 312–320, 2014.
129. Zebrowski DC, Engel FB. The cardiomyocyte cell cycle in hypertrophy, tissue homeostasis, and regeneration. Rev Physiol Biochem Pharmacol 165: 67–96, 2013.
130. Zebrowski DC, Vergarajauregui S, Wu CC, Piatkowski T, Becker R, Leone M, Hirth S, Ricciardi F, Falk N, Giessl A, Just S, Braun T, Weidinger G, Engel FB. Developmental alterations in centrosome integrity contribute to the post-mitotic state of mammalian cardiomyocytes. eLife 4: 2015.
131. Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE. Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci USA 111: 1403–1408, 2014.
132. Zong H, Espinosa JS, Su HH, Muzumdar MD, Luo L. Mosaic analysis with double markers in mice. Cell 121: 479–492, 2005.