Building and re-building the heart by cardiomyocyte proliferation

Development (Cambridge)

Volumn 143, Issue 5, 2016, Pages 729-740

  Foglia, Matthew J ^a   Poss, Kenneth D ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiomyocyte; Heart regeneration; Proliferation

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ADULT; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL CYCLE; CELL PROLIFERATION; CYTOLOGY; EMBRYOLOGY; HEART; HOMEOSTASIS; HUMAN; METABOLISM; MOUSE; ORGANOGENESIS; PHYSIOLOGY; REGENERATION; ZEBRA FISH;

ADULT; ANIMALS; CELL CYCLE; CELL PROLIFERATION; HEART; HOMEOSTASIS; HUMANS; MICE; MYOCARDIUM; MYOCYTES, CARDIAC; ORGANOGENESIS; REACTIVE OXYGEN SPECIES; REGENERATION; ZEBRAFISH;

EID: 84959309444     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.132910     Document Type: Review

References (155)

1. Ali, S. R., Hippenmeyer, S., Saadat, L. V., Luo, L, Weissman, I. L. and Ardehali, R. (2014). Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice. Proc. Natl. Acad. Sci. USA 111, 8850-8855.
2. Alkass, K., Panula, J., Westman, M., Wu, T.-D., Guerquin-Kern, J.-L. and Bergmann, O. (2015). No evidence for cardiomyocyte number expansion in preadolescent mice. Cell 163, 1026-1036.
3. Aurora, A. B., Porrello, E. R., Tan, W., Mahmoud, A. I., Hill, J. A., Bassel-Duby, R., Sadek, H. A. and Olson, E. N. (2014). Macrophages are required for neonatal heart regeneration. J. Clin. Invest. 124, 1382-1392.
4. Bader, D. and Oberpriller, J. O. (1978). Repair and reorganization of minced cardiac muscle in the adult newt (Notophthalmus viridescens). J. Morphol. 155, 349-357.
5. Bader, D (2014). Telomerase expression confers cardioprotection in the adult mouse heart after acute myocardial infarction. Nat. Commun. 5, 5863
6. Berpriller, J. O 1978 Telomerase is essential for zebrafish heart regeneration. Cell Rep. 12, 1691-1703
7. Behfar, A., Crespo-Diaz, R., Terzic, A. and Gersh, B. J. (2014). Cell therapy for cardiac repair—lessons from clinical trials. Nat. Rev. Cardiol. 11, 232-246
8. Beltrami, A. P., Barlucchi, L., Torella, D., Baker, M., Limana, F., Chimenti, S., Kasahara, H., Rota, M., Musso, E., and Urbanek, K. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776.
9. Bergmann, O., Bhardwaj, R. D., Bernard, S., Zdunek, S. (2009). Evidence for cardiomyocyte renewal in humans. Science 324, 98-102
10. Bergmann, O., Zdunek, S., Felker, A., Salehpour, M., Alkass, K., Bernard, S., Sjostrom, S. L., Szewczykowska, M., Jackowska, T., dos Remedios, C. et al. (2015). Dynamics of cell generation and turnover in the human heart. Cell 161, 1566-1575.
11. Bersell, K., Arab, S., Haring, B (2009). Neuregulin1/ErbB4 signaling Induces cardiomyocyte proliferation and repair of heart Injury. Cell 138, 257-270
12. Bettencourt-Dias, M., Mittnacht, S. and Brockes, J. P. (2003). Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J. Cell Sci. 116, 4001-4009.
13. Bosch, T. C. G. (2007). Why polyps regenerate and we don’t: Towards a cellular and molecular framework for Hydra regeneration. Dev. Biol. 303, 421-433.
14. Brade, T., Kumar, S., Cunningham, T. J., Chatzi, C., Zhao, X., Cavallero, S., Li, P., Sucov, H. M., Ruiz-Lozano, P. and Duester, G. (2011). Retinoic acid stimulates myocardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2. Development 138, 139-148.
15. Brockes, J. P. and Kumar, A. (2008). Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol. 24, 525-549.
16. Brodsky, V., Arefyeva, A. M., Gvasava, I. G., Sarkisov, D. S. and Panova, N. W. (1994). Polyploidy in cardiac myocytes of normal and hypertrophic human hearts; range of values. Virchows Arch. 424, 429-435.
17. Buckingham, M., Meilhac, S. and Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6, 826-837.
18. Buggisch, M., Ateghang, B., Ruhe, C., Strobel, C., Lange, S., Wartenberg, M. and Sauer, H. (2007). Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase. J. Cell Sci. 120, 885-894.
19. Chablais, F., Veit, J., Rainer, G.(2011). The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol. 11, 21
20. Challice, C. E (1974). The architectural development of the early mammalian heart. Tissue Cell 6, 447-462.
21. Chaudhry, H. W., Dashoush, N. H., Tang, H., Zhang, L, Wang, X., Wu, E. X. and Wolgemuth, D. J. (2004). Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J. Biol. Chem. 279, 35858-35866.
22. Chen, T. H.-P., Chang, T.-C., Kang, J.-O., Choudhary, B., Makita, T., Tran, C. M., Burch, J. B. E., Eid, H. and Sucov, H. M. (2002). Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev. Biol. 250, 198-207.
23. Chen, H., Shi, S., Acosta, L., Li, W., Lu, J., Bao, S., Chen, Z., Yang, Z., Schneider, M. D., Chien, K. R. et al. (2004). BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131, 2219-2231.
24. Chen, J. X., Krane, M., Deutsch, M.-A., Wang, L., Rav-Acha, M., Gregoire, S., Engels, M. C., Rajarajan, K., Karra, R., Abel, E. D. et al. (2012). Inefficient reprogramming of fibroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ. Res. 111, 50-55.
25. Chen, H., Zhang, W., Sun, X., Yoshimoto, M., Chen, Z., Zhu, W., Liu, J., Shen, Y., Yong, W., Li, D. et al. (2013). Fkbp1a controls ventricular myocardium trabeculation and compaction by regulating endocardial Notch1 activity. Development 140, 1946-1957.
26. Christoffels, V. M., Habets, P. E. M. H., Franco, D., Campione, M., de Jong, F., Lamers, W. H., Bao, Z.-Z., Palmer, S., Biben, C., Harvey, R. P. et al. (2000). Chamber formation and morphogenesis in the developing mammalian heart. Dev. Biol. 223, 266-278.
27. Clark, E. B., Hu, N., Frommelt, P., Vandekieft, G. K., Dummett, J. L. and Tomanek, R. J. (1989). Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am. J. Physiol. 257, H55-H61.
28. de Pater, E., Clijsters, L., Marques, S. R., Lin, Y.-F., Garavito-Aguilar, Z. V., Yelon, D. and Bakkers, J. (2009). Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136, 1633-1641.
29. Drenckhahn, J.-D., Schwarz, Q. P., Gray, S., Laskowski, A., Kiriazis, H., Ming, Z., Harvey, R. P., Du, X.-J., Thorburn, D. R. and Cox, T. C. (2008). Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development. Dev. Cell 15, 521-533.
30. D’Uva, G., Aharonov, A., Lauriola, M., Kain, D., Yahalom-Ronen, Y., Carvalho, S., Weisinger, K., Bassat, E., Rajchman, D., Yifa, O. et al. (2015). ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation. Nat. Cell Biol. 17, 627-638.
31. Ellison, G. M., Vicinanza, C., Smith, A. J., Aquila, I., Leone, A., Waring, C. D., Henning, B. J., Stirparo, G. G., Papait, R., Scarfo, M. et al. (2013). Adult c-kit (pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 154, 827-842.
32. Engel, F. B., Schebesta, M., Duong, M. T., Lu, G., Ren, S., Madwed, J. B., Jiang, H., Wang, Y. and Keating, M. T. (2005). p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev. 19, 1175-1187.
33. Eulalio, A., Mano, M., Dal Ferro, M., Zentilin, L., Sinagra, G., Zacchigna, S. and Giacca, M. (2012). Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492, 376-381.
34. Fang, Y., Gupta, V., Karra, R., Holdway, J. E., Kikuchi, K. and Poss, K. D. (2013). Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA 110, 13416-13421.
35. Flink, I. (2002). Cell cycle reentry of ventricular and atrial cardiomyocytes and cells within the epicardium following amputation of the ventricular apex in the axolotl, Amblystoma mexicanum: confocal microscopic immunofluorescent image analysis of bromodeoxyuridine-labeled nuclei. Anat. Embryol. 205, 235-244.
36. Flink, I. L., Oana, S., Maitra, N., Bahl, J. J. and Morkin, E. (1998). Changes in E2F complexes containing retinoblastoma protein family members and increased cyclin-dependent kinase inhibitor activities during terminal differentiation of cardiomyocytes. J. Mol. Cell Cardiol. 30, 563-578.
37. Forsyth, N. R., Wright, W. E. and Shay, J. W. (2002). Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 69, 188-197.
38. Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R. and Lemke, G. (1995). Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390-394.
39. Gemberling, M., Karra, R., Dickson, A. L. and Poss, K. D. (2015). Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. eLife 4, e05871.
40. Gerczuk, P. Z. and Kloner, R. A. (2012). An update on cardioprotection: a review of the latest adjunctive therapies to limit myocardial infarction size in clinical trials. J. Am. Coll. Cardiol. 59, 969-978.
41. Gerety, S. S., Wang, H. U., Chen, Z.-F. and Anderson, D. J. (1999). Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell 4, 403-414.
42. Giacca, M. and Zacchigna, S. (2015). Harnessing the microRNA pathway for cardiac regeneration. J. Mol. Cell Cardiol. 89A, 68-74.
43. Gnecchi, M., Zhang, Z., Ni, A. and Dzau, V. J. (2008). Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 103, 1204-1219.
44. Gnecchi, M. (2011). Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 138, 1663-1674
45. Gnecchi, M. (2012). Pan-epicardial lineage tracing reveals that epicardium derived cells give rise to myofibroblasts and perivascular cells during zebrafish heart regeneration. Dev. Biol. 370, 173-186.
46. Grego-Bessa, J., Luna-Zurita, L., del Monte, G. (2007). Notch signaling is essential for ventricular chamber development. Dev. Cell 12, 415-429
47. Grego-Bessa, J., Luna-Zurita, L. (2015). HIF1α represses cell stress pathways to allow proliferation of hypoxic fetal cardiomyocytes. Dev. Cell 33, 507-521
48. Gupta, V. and Poss, K. D. (2012). Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 484, 479-484.
49. Gupta, V., Gemberling, M., Karra, R., Rosenfeld, G. E., Evans, T. and Poss, K. D. (2013). An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr. Biol. 23, 1221-1227.
50. Han, P., Zhou, X.-H., Chang, N., Xiao, C.-L., Yan, S., Ren, H., Yang, X.-Z., Zhang, M.-L., Wu, Q., Tang, B. et al. (2014). Hydrogen peroxide primes heart regeneration with a derepression mechanism. Cell Res. 24, 1091-1107.
51. Haubner, B. J., Adamowicz-Brice, M., Khadayate, S., Tiefenthaler, V., Metzler, B., Aitman, T. and Penninger, J. M. (2012). Complete cardiac regeneration in a mouse model of myocardial infarction. Aging 4, 966-977.
52. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R. L. and Martin, J. F. (2011). Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461.
53. Heallen, T., Morikawa, Y., Leach, J., Tao, G, Willerson, J. T., Johnson, R. L. and Martin, J. F. (2013). Hippo signaling impedes adult heart regeneration. Development 140, 4683-4690.
54. Hirai, M., Chen, J. and Evans, S. M. (2015). Tissue-specific cell cycle indicator reveals unexpected findings for cardiac myocyte proliferation. Circ. Res. 118, 20-28.
55. Hong, K. U., Guo, Y., Li, Q.-H., Cao, P., Al-Maqtari, T., Vajravelu, B. N., Du, J., Book, M. J., Zhu, X., Nong, Y. et al. (2014). c-kit+ cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PLoS ONE 9, e96725.
56. Huang, Y., Harrison, M. R., Osorio, A., Kim, J., Baugh, A., Duan, C., Sucov, H. M. and Lien, C.-L. (2013). Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS ONE 8, e67266.
57. Ieda, M., Fu, J.-D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G. and Srivastava, D. (2010). Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142, 375-386.
58. Ito, K., Morioka, M., Kimura, S., Tasaki, M., Inohaya, K. and Kudo, A. (2014). Differential reparative phenotypes between zebrafish and medaka after cardiac injury. Dev. Dyn. 243, 1106-1115.
59. Jessup, M. and Brozena, S. (2003). Heart failure. N. Engl. J. Med. 348, 2007-2018.
60. Jopling, C., Sleep, E., Raya, M., (2010). Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609
61. Jopling, C. (2012). Hypoxia induces myocardial regeneration in zebrafish. Circulation 126, 3017-3027
62. Karra, R., Knecht, A. K., Kikuchi, K. and Poss, K. D. (2015). Myocardial NF-κB activation is essential for zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA 112, 13255-13260.
63. Kelly, R. G., Brown, N. A. and Buckingham, M. E. (2001). The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1, 435-440.
64. Kelly, R. G., Buckingham, M. E. and Moorman, A. F. (2014). Heart fields and cardiac morphogenesis. Cold Spring Harb. Perspect. Med. 4, a015750.
65. Kikuchi, K., Holdway, J. E., Werdich, A. A., Anderson, R. M., Fang, Y., Egnaczyk, G. F., Evans, T., Macrae, C. A., Stainier, D. Y. and Poss, K. D. (2010). Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes. Nature 464, 601-605.
66. Kikuchi, K., Gupta, V., Wang, J., Holdway, J. E., Wills, A. A., Fang, Y. and Poss, K. D. (2011a). tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 138, 2895-2902.
67. Kikuchi, K., Holdway, J. E., Major, R. J., Blum, N., Dahn, R. D., Begemann, G. and Poss, K. D. (2011b). Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 20, 397-404.
68. Kim, J., Wu, Q., Zhang, Y., Wiens, K. M., Huang, Y., Rubin, N., Shimada, H., Handin, R. I., Chao, M. Y., Tuan, T.-L. et al. (2010). PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. USA 107, 17206-17210.
69. Kimura, W., Xiao, F., Canseco, D. C., Muralidhar, S., Thet, S., Zhang, H. M., Abderrahman, Y., Chen, R., Garcia, J. A., Shelton, J. M. et al. (2015). Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart. Nature 523, 226-230.
70. Kreidberg, J. A., Sariola, H., Loring, J. M., Maeda, M., Pelletier, J., Housman, D. and Jaenisch, R. (1993). WT-1 is required for early kidney development. Cell 74, 679-691.
71. Kuo, C. T., Morrisey, E. E., Anandappa, R., Sigrist, K., Lu, M. M., Parmacek, M. S., Soudais, C. and Leiden, J. M. (1997). GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11, 1048-1060.
72. Laflamme, M. A. and Murry, C. E. (2011). Heart regeneration. Nature 473, 326-335.
73. Lafontant, P. J., Burns, A. R., Grivas, J. A., Lesch, M. A., Lala, T. D., Reuter, S. P., Field, L. J. and Frounfelter, T. D. (2012). The Giant Danio (D. aequipinnatus) as a model of cardiac remodeling and regeneration. Anat. Rec. 295, 234-248.
74. Lavine, K. J., Epelman, S., Uchida, K., Weber, K. J., Nichols, C. G., Schilling, J. D., Ornitz, D. M., Randolph, G. J. and Mann, D. L. (2014). Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc. Nat. Acad. Sci. USA 111, 16029-16034.
75. Lee, K.-F., Simon, H., Chen, H., Bates, B., Hung, M.-C. and Hauser, C. (1995). Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394-398.
76. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G. and Poss, K. D. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619.
77. Li, F., Wang, X., Capasso, J. M. and Gerdes, A. M. (1996). Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J. Mol. Cell. Cardiol. 28, 1737-1746.
78. Li, F, Wang, X., Bunger, P. C. and Gerdes, A. M. (1997). Formation of binucleated cardiac myocytes in rat heart: I. Role of actin–myosin contractile ring. J. Mol. Cell. Cardiol. 29, 1541-1551.
79. Li, P., Cavallero, S., Gu, Y., Chen, T. H. P., Hughes, J., Hassan, A. B. (2011). IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138, 1795-1805
80. Lien, C.-L., Schebesta, M., Makino, S., Weber, G. J. and Keating, M. T. (2006). Gene expression analysis of zebrafish heart regeneration. PLoS Biol. 4, e260.
81. Lin, Z., von Gise, A., Zhou, P., Gu, F., Ma, Q., Jiang, J., Yau, A. L., Buck, J. N., Gouin, K. A., van Gorp, P. R. R. et al. (2014). Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ. Res. 115, 354-363.
82. Liu, J., Bressan, M., Hassel, D., Huisken, J., Staudt, D., Kikuchi, K., Poss, K. D., Mikawa, T. and Stainier, D. Y. R. (2010). A dual role for ErbB2 signaling in cardiac trabeculation. Development 137, 3867-3875.
83. Livet, J., Weissman, T. A., Kang, H., Draft, R. W., Lu, J., Bennis, R. A., Sanes, J. R. and Lichtman, J. W. (2007). Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56-62.
84. Mahmoud, A. I., Kocabas, F., Muralidhar, S. A., Kimura, W., Koura, A. S., Thet, S., Porrello, E. R. and Sadek, H. A. (2013). Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 497, 249-253.
85. Mahmoud, A. I., O’Meara, C. C., Gemberling, M., Zhao, L., Bryant, D. M., Zheng, R., Gannon, J. B., Cai, L., Choi, W.-Y., Egnaczyk, G. F. et al. (2015). Nerves regulate cardiomyocyte proliferation and heart regeneration. Dev. Cell 34, 387-399.
86. Masters, M. and Riley, P. R. (2014). The epicardium signals the way towards heart regeneration. Stem Cell Res. 13, 683-692.
87. Matz, D. G., Oberpriller, J. O. and Oberpriller, J. C. (1998). Comparison of mitosis in binucleated and mononucleated newt cardiac myocytes. Anat. Rec. 251, 245-255.
88. McMurray, J. J. V. C., Adamopoulos, S., Anker, S. D., Auricchio, A. (2012). ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2012. Eur. J. Heart Fail. 14, 803-869
89. Meilhac, S. M., Kelly, R. G., Rocancourt, D., Eloy-Trinquet, S., Nicolas, J.-F. and Buckingham, M. E. (2003). A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 130, 3877-3889.
90. Merki, E., Zamora, M., Raya, A., Kawakami, Y., Wang, J., Zhang, X., Burch, J., Kubalak, S.W., Kaliman, P., Belmonte, J. C. I. et al. (2005). Epicardial retinoid X receptor α is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. USA 102, 18455-18460.
91. Meyer, D. and Birchmeier, C. (1995). Multiple essential functions of neuregulin in development. Nature 378, 386-390.
92. Mikawa, T., Borisov, A., Brown, A. M. C. and Fischman, D. A. (1992a). Clonal analysis of cardiac morphogenesis in the chicken embryo using a replicationdefective retrovirus: I. Formation of the ventricular myocardium. Dev. Dyn. 193, 11-23.
93. Mikawa, T., Cohen-Gould, L. and Fischman, D. A. (1992b). Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus. III: Polyclonal origin of adjacent ventricular myocytes. Dev. Dyn. 195, 133-141.
94. Mjaatvedt, C. H., Nakaoka, T., Moreno-Rodriguez, R., Norris, R. A., Kern, M. J., Eisenberg, C. A., Turner, D. and Markwald, R. R. (2001). The outflow tract of the heart Is recruited from a novel heart-forming field. Dev. Biol. 238, 97-109.
95. Molkentin, J. D., Lin, Q., Duncan, S. A. and Olson, E. N. (1997). Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11, 1061-1072.
96. Mollova, M., Bersell, K., Walsh, S., Savla, J., Das, L. T., Park, S.-Y., Silberstein, L. E., dos Remedios, C. G., Graham, D., Colan, S. et al. (2013). Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl. Acad. Sci. USA 110, 1446-1451.
97. Murray, T. V. A., Smyrnias, I., Schnelle, M., Mistry, R. K., Zhang, M., Beretta, M., Martin, D., Anilkumar, N., de Silva, S. M., Shah, A. M. et al. (2015). Redox regulation of cardiomyocyte cell cycling via an ERK1/2 and c-Myc-dependent activation of cyclin D2 transcription. J. Mol. Cell Cardiol. 79, 54-68.
98. Naqvi, N., Li, M., Calvert, J.W., Tejada, T., Lambert, J. P., Wu, J., Kesteven, S. H., Holman, S. R., Matsuda, T., Lovelock, J. D. et al. (2014). A proliferative burst during preadolescence establishes the final cardiomyocyte number. Cell 157, 795-807.
99. Naqvi, N., Singh, R., Iismaa, S. E., Li, M., Calvert, J. W., Martin, D. I. K., Harvey, R. P., Graham, R. M. and Husain, A. (2015). Cardiomyocytes replicate and their numbers increase in young hearts. Cell 163, 783-784.
100. Oberpriller, J. O. and Oberpriller, J. C. (1974). Response of the adult newt ventricle to injury. J. Exp. Zool. 187, 249-259.
101. Olivetti, G., Cigola, E., Maestri, R., Corradi, D., Lagrasta, C., Gambert, S. R. and Anversa, P. (1996). 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.
102. Paige, S. L., Plonowska, K., Xu, A. and Wu, S. M. (2015). Molecular regulation of cardiomyocyte differentiation. Circ. Res. 116, 341-353.
103. Pasumarthi, K. B. S., Nakajima, H., Nakajima, H. O., Soonpaa, M. H. and Field, L. J. (2005). Targeted expression of Cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ. Res. 96, 110-118.
104. Pennisi, D. J., Ballard, V. L. T. and Mikawa, T. (2003). Epicardium is required for the full rate of myocyte proliferation and levels of expression of myocyte mitogenic factors FGF2 and its receptor, FGFR-1, but not for transmural myocardial patterning in the embryonic chick heart. Dev. Dyn. 228, 161-172.
105. Pennisi, D. J., Ballard, V. L. T. (2002). Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev. Biol. 247, 307-326
106. Polizzotti, B. D., Ganapathy, B, Walsh, S., Choudhury, S., Ammanamanchi, N., Bennett, D. G., dos Remedios, C. G., Haubner, B. J., Penninger, J. M. and Kuhn, B. (2015). Neuregulin stimulation of cardiomyocyte regeneration in mice and human myocardium reveals a therapeutic window. Sci. Transl. Med. 7, 281ra45.
107. Poolman, R. A. and Brooks, G. (1998). Expressions and activities of cell cycle regulatory molecules during the transition from myocyte hyperplasia to hypertrophy. J. Mol. Cell. Cardiol. 30, 2121-2135.
108. Porrello, E. R., Mahmoud, A. I., Simpson, E., Hill, J. A., Richardson, J. A., Olson, E. N. and Sadek, H. A. (2011). Transient regenerative potential of the neonatal mouse heart. Science 331, 1078-1080.
109. Porrello, E. R., Mahmoud, A. I., Simpson, E., Johnson, B. A., Grinsfelder, D., Canseco, D., Mammen, P. P., Rothermel, B. A., Olson, E. N. and Sadek, H. A. (2013). Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. USA 110, 187-192.
110. Poss, K. D. (2010). Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat. Rev. Genet. 11, 710-722.
111. Poss, K. D., Wilson, L. G. and Keating, M. T. (2002). Heart regeneration in zebrafish. Science 298, 2188-2190.
112. Puente, B. N., Kimura, W., Muralidhar, S. A., Moon, J., Amatruda, J. F., Phelps, K. L., Grinsfelder, D., Rothermel, B. A., Chen, R., Garcia, J. A. et al. (2014). The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 157, 565-579.
113. Qian, L., Huang, Y., Spencer, C. I., Foley, A., Vedantham, V., Liu, L., Conway, S. J., Fu, J.-d. and Srivastava, D. (2012). In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598.
114. Qu, X., Jia, H., Garrity, D. M., Tompkins, K., Batts, L., Appel, B., Zhong, T. P. and Baldwin, H. S. (2008). ndrg4 is required for normal myocyte proliferation during early cardiac development in zebrafish. Dev. Biol. 317, 486-496.
115. Reddien, P. W. (2004). Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20, 725-757
116. Reuter, S., Soonpaa, M. H., Firulli, A. B., Chang, A. N. and Field, L. J. (2014). Recombinant neuregulin 1 does not activate cardiomyocyte DNA synthesis in normal or infarcted adult mice. PLoS ONE 9, e115871.
117. Sadahiro, T., Yamanaka, S. and Ieda, M. (2015). Direct cardiac reprogramming: progress and challenges in basic biology and clinical applications. Circ. Res. 116, 1378-1391.
118. Saiki, Y., Konig, A., Waddell, J. and Rebeyka, I. M. (1997). Hemodynamic alteration by fetal surgery accelerates myocyte proliferation in fetal guinea pig hearts. Surgery 122, 412-419.
119. Schnabel, K., Wu, C.-C., Kurth, T. and Weidinger, G. (2011). Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS ONE 6, e18503.
120. Sdek, P., Zhao, P, Wang, Y., Huang, C.-j., Ko, C. Y., Butler, P. C, Weiss, J. N. and MacLellan, W. R. (2011). Rb and p130 control cell cycle gene silencing to maintain the postmitotic phenotype in cardiac myocytes. J. Cell Biol. 194, 407-423.
121. Sedmera, D., Pexieder, T., Hu, N. and Clark, E. B. (1997). Developmental changes in the myocardial architecture of the chick. Anat. Rec. 248, 421-432.
122. Sedmera, D., Pexieder, T., Vuillemin, M., Thompson, R. P. and Anderson, R. H. (2000). Developmental patterning of the myocardium. Anat. Rec. 258, 319-337.
123. Senyo, S. E., Steinhauser, M. L., Pizzimenti, C. L., Yang, V. K., Cai, L, Wang, M., Wu, T.-D., Guerquin-Kern, J.-L., Lechene, C. P. and Lee, R. T. (2013). Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493, 433-436.
124. Sissman, N. J. (1966). Cell multiplication rates during development of the primitive cardiac tube in the chick embryo. Nature 210, 504-507.
125. Sizarov, A., Ya, J., de Boer, B. A., Lamers, W. H., Christoffels, V. M. and Moorman, A. F. M. (2011). Formation of the building plan of the human heart: morphogenesis, growth, and differentiation. Circulation 123, 1125-1135.
126. Smart, N., Bollini, S., (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature 474, 640-644
127. Song, K., Nam, Y.-J., Luo, X., Qi, X., Tan, W., Huang, G. N., Acharya, A., Smith, C. L., Tallquist, M. D., Neilson, E. G. et al. (2012). Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485, 599-604.
128. Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. and Field, L. J. (1996). Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 271, H2183-H2189.
129. Soonpaa, M. H., Koh, G. Y., Pajak, L., Jing, S., Wang, H., Franklin, M. T., Kim, K. K. and Field, L. J. (1997). Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. J. Clin. Invest. 99,2644-2654.
130. Soonpaa, M. H., Zebrowski, D. C., Platt, C., Rosenzweig, A., Engel, F. B. and Field, L. J. (2015). Cardiomyocyte cell-cycle activity during preadolescence. Cell 163, 781-782.
131. Soufan, A. T., van den Berg, G., Ruijter, J. M., de Boer, P. A. J., van den Hoff, M. J. B. and Moorman, A. F. M. (2006). Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ. Res. 99, 545-552.
132. Staudt, D. W., Liu, J., Thorn, K. S., Stuurman, N., Liebling, M. and Stainier, D. Y. R. (2014). High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation. Development 141, 585-593.
133. Stuckmann, I., Evans, S. and Lassar, A. B. (2003). Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol. 255, 334-349.
134. Sturzu, A. C., Rajarajan, K., Passer, D., Plonowska, K., Riley, A., Tan, T. C., Sharma, A., Xu, A. F., Engels, M. C., Feistritzer, R. et al. (2015). The fetal mammalian heart generates a robust compensatory response to cell loss. Circulation 132, 109-121.
135. Sutton, M. G. S. J. and Sharpe, N. (2000). Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101, 2981-2988.
136. Tian, Y., Liu, Y, Wang, T., Zhou, N., Kong, J., Chen, L., Snitow, M., Morley, M., Li, D., Petrenko, N. et al. (2015). A microRNA-Hippo pathway that promotes cardiomyocyte proliferation and cardiac regeneration in mice. Sci. Transl. Med. 7, 279ra38.
137. van Berlo, J. H. and Molkentin, J. D. (2014). An emerging consensus on cardiac regeneration. Nat. Med. 20, 1386-1393.
138. van Berlo, J. H., Kanisicak, O., Maillet, M., Vagnozzi, R. J., Karch, J., Lin, S.-C. J., Middleton, R. C.. (2014). c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509, 337-341
139. van den Berg, G., Abu-Issa, R., de Boer, B. A., Hutson, M. R., de Boer, P. A. J., Soufan, A. T., Ruijter, J. M., Kirby, M. L., van den Hoff, M. J. B. and Moorman, A. F. M. (2009). A caudal proliferating growth center contributes to both poles of the forming heart tube. Circ. Res. 104, 179-188.
140. von Gise, A., Lin, Z., Schlegelmilch, K., Honor, L. B., Pan, G. M., Buck, J. N., Ma, Q., Ishiwata, T., Zhou, B., Camargo, F. D. et al. (2012). YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl. Acad. Sci. USA 109, 2394-2399.
141. Waldo, K. L., Kumiski, D. H, Wallis, K. T., Stadt, H. A., Hutson, M. R., Platt, D. H. and Kirby, M. L. (2001). Conotruncal myocardium arises from a secondary heart field. Development 128, 3179-3188.
142. Wang, H. U., Chen, Z.-F. and Anderson, D. J. (1998). Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin- B2 and its receptor Eph-B4. Cell 93, 741-753.
143. Wang, J., (2011). The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138, 3421-3430
144. Wang, J., Cao, J., Dickson, A. L. and Poss, K. D. (2015). Epicardial regeneration is guided by cardiac outflow tract and Hedgehog signalling. Nature 522, 226-230.
145. Wei, K., Serpooshan, V., Hurtado, C., (2015). Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature 525, 479-485
146. Wills, A. A., Holdway, J. E., Major, R. J. and Poss, K. D. (2008). Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 135, 183-192.
147. Witman, N., Murtuza, B., Davis, B., Arner, A. and Morrison, J. I. (2011). Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. Dev. Biol. 354, 67-76.
148. Wu, H., Lee, S. H., Gao, J., Liu, X. and Iruela-Arispe, M. L. (1999). Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 126, 3597-3605.
149. Xin, M., Kim, Y., Sutherland, L. B., Qi, X., McAnally, J., Schwartz, R. J., Richardson, J. A., Bassel-Duby, R. and Olson, E. N. (2011). Regulation of Insulin-like growth factor signaling by Yap governrs cardiomyocyte proliferation and embryonic heart size. Sci. Signal. 25, ra70.
150. Xin, M., Kim, Y., Sutherland, L. B., Murakami, M., Qi, X., McAnally, J., Porrello, E. R., Mahmoud, A. I., Tan, W., Shelton, J. M. et al. (2013). Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA 110, 13839-13844.
151. Zak, R. (1973). Cell proliferation during cardiac growth. Am. J. Cardiol. 31, 211-219.
152. Zhang, R., Han, P., Yang, H., Ouyang, K., Lee, D., Lin, Y.-F., Ocorr, K., Kang, G., Chen, J., Stainier, D. Y. et al. (2013). In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 498, 497-501.
153. Zhao, Y.-y., Sawyer, D. R., Baliga, R. R., Opel, D. J., Han, X., Marchionni, M. A. and Kelly, R. A. (1998). Neuregulins promote survival and growth of cardiac myocytes: persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 273, 10261-10269.
154. Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Yu, J., Lin, J. D., Wang, C. Y., Chinnaiyan, A. M. et al. (2008). TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971.
155. Zhou, Q., Li, L., Zhao, B. and Guan, K.-L. (2015). The Hippo pathway in heart development, regeneration, and diseases. Circ. Res. 116, 1431-1447.