Mechanisms of Cardiac Regeneration

Developmental Cell

Volumn 36, Issue 4, 2016, Pages 362-374

  Uygur, Aysu ^a,b   Lee, Richard T ^a,b  

^a Harvard University   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC MYOSIN; CRE RECOMBINASE; EPIDERMAL GROWTH FACTOR; NEUREGULIN1; UNCLASSIFIED DRUG;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANURA; APOPTOSIS; CARDIAC REGENERATION; CARDIOVASCULAR MORTALITY; CELL ADHESION; CELL FATE; CELL PROLIFERATION; COLD INJURY; DOWN REGULATION; DROSOPHILA; EPICARDIUM; EXTRACELLULAR MATRIX; FETUS HEART; GENE EXPRESSION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; IMMUNE RESPONSE; INFLAMMATORY CELL; MOUSE; MUSCLE REGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; REGENERATION; REVIEW; SALAMANDRIDAE; SIGNAL TRANSDUCTION; TELEOST; X CHROMOSOME INACTIVATION; ZEBRA FISH; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HEART; MAMMAL; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; HEART; HUMANS; MAMMALS; MYOCARDIUM; MYOCYTES, CARDIAC; REGENERATION;

EID: 84958687916     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.01.018     Document Type: Review

References (152)

1. Andersen D.C., Ganesalingam S., Jensen C.H., Sheikh S.P. Do neonatal mouse hearts regenerate following heart apex resection?. Stem Cell Rep. 2014, 2:406-413.
2. Angert D., Berretta R.M., Kubo H., Zhang H., Chen X., Wang W., Ogorek B., Barbe M., Houser S.R. Repair of the injured adult heart involves new myocytes potentially derived from resident cardiac stem cells. Circ. Res. 2011, 108:1226-1237.
3. Aurora A.B., Porrello E.R., Tan W., Mahmoud A.I., Hill J.A., Bassel-Duby R., Sadek H.A., Olson E.N. Macrophages are required for neonatal heart regeneration. J. Clin. Invest. 2014, 124:1382-1392.
4. Azcoitia V., Aracil M., Martínez-A C., Torres M. The homeodomain protein Meis1 is essential for definitive hematopoiesis and vascular patterning in the mouse embryo. Dev. Biol. 2005, 280:307-320.
5. Baliga R.R., Pimental D.R., Zhao Y.Y., Simmons W.W., Marchionni M.A., Sawyer D.B., Kelly R.A. NRG-1-induced cardiomyocyte hypertrophy. Role of PI-3-kinase, p70(S6K), and MEK-MAPK-RSK. Am. J. Physiol. 1999, 277:H2026-H2037.
6. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
7. Becker R.O., Chapin S., Sherry R. Regeneration of the ventricular myocardium in amphibians. Nature 1974, 248:145-147.
8. Becker T., Wullimann M.F., Becker C.G., Bernhardt R.R., Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 1997, 377:577-595.
9. Beltrami A.P., Barlucchi L., Torella D., Baker M., Limana F., Chimenti S., Kasahara H., Rota M., Musso E., Urbanek K., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114:763-776.
10. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabé-Heider F., Walsh S., Zupicich J., Alkass K., Buchholz B.A., Druid H., et al. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
11. Bergmann O., Zdunek S., Felker A., Salehpour M., Alkass K., Bernard S., Sjostrom S.L., Szewczykowska M., Jackowska T., Dos Remedios C., et al. Dynamics of cell generation and turnover in the human heart. Cell 2015, 161:1566-1575.
12. Bersell K., Arab S., Haring B., Kühn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009, 138:257-270.
13. Bondue A., Lapouge G., Paulissen C., Semeraro C., Iacovino M., Kyba M., Blanpain C. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 2008, 3:69-84.
14. Bryant D.M., O'Meara C.C., Ho N.N., Gannon J., Cai L., Lee R.T. A systematic analysis of neonatal mouse heart regeneration after apical resection. J. Mol. Cell. Cardiol. 2014, 79:315-318.
15. Butcher J.T., Norris R.A., Hoffman S., Mjaatvedt C.H., Markwald R.R. Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev. Biol. 2007, 302:256-266.
16. Cai C.-L., Liang X., Shi Y., Chu P.-H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 2003, 5:877-889.
17. Chablais F., Jazwinska A. The regenerative capacity of the zebrafish heart is dependent on TGFβ signaling. Development 2012, 139:1921-1930.
18. Chablais F., Veit J., Rainer G., Jaźwińska A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol. 2011, 11:21.
19. Chen J., Huang Z.-P., Seok H.Y., Ding J., Kataoka M., Zhang Z., Hu X., Wang G., Lin Z., Wang S., et al. mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ. Res. 2013, 112:1557-1566.
20. Chong J.J.H., Yang X., Don C.W., Minami E., Liu Y.-W., Weyers J.J., Mahoney W.M., Van Biber B., Cook S.M., Palpant N.J., et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510:273-277.
21. da Costa Martins P.A., Bourajjaj M., Gladka M., Kortland M., van Oort R.J., Pinto Y.M., Molkentin J.D., De Windt L.J. Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 2008, 118:1567-1576.
22. Darehzereshki A., Rubin N., Gamba L., Kim J., Fraser J., Huang Y., Billings J., Mohammadzadeh R., Wood J., Warburton D., et al. Differential regenerative capacity of neonatal mouse hearts after cryoinjury. Dev. Biol. 2015, 399:91-99.
23. Drenckhahn J.-D., Schwarz Q.P., Gray S., Laskowski A., Kiriazis H., Ming Z., Harvey R.P., Du X.-J., Thorburn D.R., Cox T.C. Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development. Dev. Cell 2008, 15:521-533.
24. D'Uva G., Aharonov A., Lauriola M., Kain D., Yahalom-Ronen Y., Carvalho S., Weisinger K., Bassat E., Rajchman D., Yifa O., et al. ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation. Nat. Cell Biol. 2015, 17:627-638.
25. Ehrman L.A., Yutzey K.E. Lack of regulation in the heart forming region of avian embryos. Dev. Biol. 1999, 207:163-175.
26. Epelman S., Liu P.P., Mann D.L. Role of innate and adaptive immune mechanisms in cardiac injury and repair. Nat. Rev. Immunol. 2015, 15:117-129.
27. Eulalio A., Mano M., Dal Ferro M., Zentilin L., Sinagra G., Zacchigna S., Giacca M. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012, 492:376-381.
28. Faber J. An experimental analysis of regional organization in the regenerating fore limb of the axolotl (Ambystoma mexicanum). Arch. Biol. 1960, 71:1-72.
29. Flink I.L. 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-label. Anat. Embryol. 2002, 205:235-244.
30. Fratz S., Hager A., Schreiber C., Schwaiger M., Hess J., Stern H.C. Long-term myocardial scarring after operation for anomalous left coronary artery from the pulmonary artery. Ann. Thorac. Surg. 2011, 92:1761-1765.
31. Gamba L., Harrison M., Lien C.-L. Cardiac regeneration in model organisms. Curr. Treat. Options Cardiovasc. Med. 2014, 16:288.
32. Gemberling M., Karra R., Dickson A.L., Poss K.D. Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. Elife 2015, 4:e05871.
33. Godwin J.W., Rosenthal N. Scar-free wound healing and regeneration in amphibians: immunological influences on regenerative success. Differentiation 2014, 87:66-75.
34. Godwin J.W., Pinto A.R., Rosenthal N.A. Macrophages are required for adult salamander limb regeneration. Proc. Natl. Acad. Sci. USA 2013, 110:9415-9420.
35. González-Rosa J.M., Martín V., Peralta M., Torres M., Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138:1663-1674.
36. Gospodarowicz D., Mescher A.L. Fibroblast growth factor and the control of vertebrate regeneration and repair. Ann. N. Y. Acad. Sci. 1980, 339:151-174.
37. Gottlieb P.D., Pierce S.A., Sims R.J., Yamagishi H., Weihe E.K., Harriss J.V., Maika S.D., Kuziel W.A., King H.L., Olson E.N., et al. Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet. 2002, 31:25-32.
38. Grego-Bessa J., Luna-Zurita L., del Monte G., Bolós V., Melgar P., Arandilla A., Garratt A.N., Zang H., Mukouyama Y.-S., Chen H., et al. Notch signaling is essential for ventricular chamber development. Dev. Cell 2007, 12:415-429.
39. Grow M., Neff A.W., Mescher A.L., King M.W. Global analysis of gene expression in Xenopus hindlimbs during stage-dependent complete and incomplete regeneration. Dev. Dyn. 2006, 235:2667-2685.
40. Gupta V., Poss K.D. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 2012, 484:479-484.
41. Gupta V., Gemberling M., Karra R., Rosenfeld G.E., Evans T., Poss K.D. An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr. Biol. 2013, 23:1221-1227.
42. Han C., Nie Y., Lian H., Liu R., He F., Huang H., Hu S. Acute inflammation stimulates a regenerative response in the neonatal mouse heart. Cell Res. 2015, 25:1137-1151.
43. Hang C.T., Yang J., Han P., Cheng H.-L., Shang C., Ashley E., Zhou B., Chang C.-P. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 2010, 466:62-67.
44. Harrison M.R.M., Bussmann J., Huang Y., Zhao L., Osorio A., Burns C.G., Burns C.E., Sucov H.M., Siekmann A.F., Lien C.-L. Chemokine-guided angiogenesis directs coronary vasculature formation in zebrafish. Dev. Cell 2015, 33:442-454.
45. Hatzistergos K.E., Quevedo H., Oskouei B.N., Hu Q., Feigenbaum G.S., Margitich I.S., Mazhari R., Boyle A.J., Zambrano J.P., Rodriguez J.E., et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ. Res. 2010, 107:913-922.
46. Hatzistergos K.E., Takeuchi L.M., Saur D., Seidler B., Dymecki S.M., Mai J.J., White I.A., Balkan W., Kanashiro-Takeuchi R.M., Schally A.V., et al. cKit+ cardiac progenitors of neural crest origin. Proc. Natl. Acad. Sci. USA 2015, 112:13051-13056.
47. Haubner B.J., Adamowicz-Brice M., Khadayate S., Tiefenthaler V., Metzler B., Aitman T., Penninger J.M. Complete cardiac regeneration in a mouse model of myocardial infarction. Aging (Albany NY) 2012, 4:966-977.
48. Haubner B.J., Schneider J., Schweigmann U.U., Schuetz T., Dichtl W., Velik-Salchner C., Stein J.-I., Penninger J.M. Functional recovery of a human neonatal heart after severe myocardial infarction. Circ. Res. 2015, 10.1161/CIRCRESAHA.115.307017.
49. Heallen T., Zhang M., Wang J., Bonilla-Claudio M., Klysik E., Johnson R.L., Martin J.F. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011, 332:458-461.
50. Heallen T., Morikawa Y., Leach J., Tao G., Willerson J.T., Johnson R.L., Martin J.F. Hippo signaling impedes adult heart regeneration. Development 2013, 140:4683-4690.
51. Hertig C.M., Kubalak S.W., Wang Y., Chien K.R. Synergistic roles of neuregulin-1 and insulin-like growth factor-I in activation of the phosphatidylinositol 3-kinase pathway and cardiac chamber morphogenesis. J. Biol. Chem. 1999, 274:37362-37369.
52. Huang Y., Harrison M.R., Osorio A., Kim J., Baugh A., Duan C., Sucov H.M., Lien C.-L. Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS One 2013, 8:e67266.
53. Ieda M., Tsuchihashi T., Ivey K.N., Ross R.S., Hong T.-T., Shaw R.M., Srivastava D. Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev. Cell 2009, 16:233-244.
54. Ito K., Morioka M., Kimura S., Tasaki M., Inohaya K., Kudo A. Differential reparative phenotypes between zebrafish and medaka after cardiac injury. Dev. Dyn. 2014, 243:1106-1115.
55. Izutsu Y., Yoshizato K. Metamorphosis-dependent recognition of larval skin as non-self by inbred adult frogs (Xenopus laevis). J. Exp. Zool. 1993, 266:163-167.
56. Jain R., Li D., Gupta M., Manderfield L.J., Ifkovits J.L., Wang Q., Liu F., Liu Y., Poleshko A., Padmanabhan A., et al. HEART DEVELOPMENT. Integration of Bmp and Wnt signaling by Hopx specifies commitment of cardiomyoblasts. Science 2015, 348:aaa6071.
57. Jesty S.A., Steffey M.A., Lee F.K., Breitbach M., Hesse M., Reining S., Lee J.C., Doran R.M., Nikitin A.Y., Fleischmann B.K., et al. C-Kit+ precursors support postinfarction myogenesis in the neonatal, but not adult. Heart Proc. Natl. Acad. Sci. 2012, 109:13380-13385.
58. Johnson S.L., Weston J.A. Temperature-sensitive mutations that cause stage-specific defects in Zebrafish fin regeneration. Genetics 1995, 141:1583-1595.
59. Jonker S.S., Zhang L., Louey S., Giraud G.D., Thornburg K.L., Faber J.J. Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart. J. Appl. Physiol. 2007, 102:1130-1142.
60. Jopling C., Sleep E., Raya M., Martí M., Raya A., Izpisúa Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464:606-609.
61. Kikuchi K., Poss K.D. Cardiac regenerative capacity and mechanisms. Annu. Rev. Cell Dev. Biol. 2012, 28:719-741.
62. Kikuchi K., Holdway J.E., Werdich A.A., Anderson R.M., Fang Y., Egnaczyk G.F., Evans T., MacRae C.A., Stainier D.Y.R., Poss K.D. Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes. Nature 2010, 464:601-605.
63. 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. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. USA 2010, 107:17206-17210.
64. Kimura W., Xiao F., Canseco D.C., Muralidhar S., Thet S., Zhang H.M., Abdulrahman Y., Chen R., Garcia J.A., Shelton J.M., et al. Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart. Nature 2015, 523:226-230.
65. King M.W., Neff A.W., Mescher A.L. The developing Xenopus limb as a model for studies on the balance between inflammation and regeneration. Anat. Rec. 2012, 295:1552-1561.
66. Kleinheinz S.J. Regenerative Medicine and Tissue Engineering 2013, InTech.
67. Kroehne V., Freudenreich D., Hans S., Kaslin J., Brand M. Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development 2011, 138:4831-4841.
68. Kühn B., del Monte F., Hajjar R.J., Chang Y.-S., Lebeche D., Arab S., Keating M.T. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat. Med. 2007, 13:962-969.
69. Kumar A., Brockes J.P. Nerve dependence in tissue, organ, and appendage regeneration. Trends Neurosci. 2012, 35:691-699.
70. Kumar A., Godwin J.W., Gates P.B., Garza-Garcia A.A., Brockes J.P. Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 2007, 318:772-777.
71. Kyritsis N., Kizil C., Zocher S., Kroehne V., Kaslin J., Freudenreich D., Iltzsche A., Brand M. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 2012, 338:1353-1356.
72. Laube F., Heister M., Scholz C., Borchardt T., Braun T. Re-programming of newt cardiomyocytes is induced by tissue regeneration. J. Cell Sci. 2006, 119:4719-4729.
73. Lavine K.J., Yu K., White A.C., Zhang X., Smith C., Partanen J., Ornitz D.M. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 2005, 8:85-95.
74. Lavine K.J., Epelman S., Uchida K., Weber K.J., Nichols C.G., Schilling J.D., Ornitz D.M., Randolph G.J., Mann D.L. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc. Natl. Acad. Sci. USA 2014, 111:16029-16034.
75. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., Poss K.D. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006, 127:607-619.
76. Li P., Cavallero S., Gu Y., Chen T.H.P., Hughes J., Hassan A.B., Brüning J.C., Pashmforoush M., Sucov H.M. IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 2011, 138:1795-1805.
77. Lickert H., Takeuchi J.K., Von Both I., Walls J.R., McAuliffe F., Adamson S.L., Henkelman R.M., Wrana J.L., Rossant J., Bruneau B.G. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004, 432:107-112.
78. Lien C.-L., Schebesta M., Makino S., Weber G.J., Keating M.T. Gene expression analysis of zebrafish heart regeneration. PLoS Biol. 2006, 4:e260.
79. 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. Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ. Res. 2014, 115:354-363.
80. Litvin J., Zhu S., Norris R., Markwald R. Periostin family of proteins: therapeutic targets for heart disease. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2005, 287:1205-1212.
81. Litwiller R. Quantitative studies on nerve regeneration in Amphibia II. Factors controlling nerve regeneration in regenerating limbs. J. Exp. Zool. 1938, 79:377-397.
82. Livet J., Weissman T.A., Kang H., Draft R.W., Lu J., Bennis R.A., Sanes J.R., Lichtman J.W. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 2007, 450:56-62.
83. Lorts A., Schwanekamp J.A., Elrod J.W., Sargent M.A., Molkentin J.D. Genetic manipulation of periostin expression in the heart does not affect myocyte content, cell cycle activity, or cardiac repair. Circ. Res. 2009, 104:e1-e7.
84. Lucas D., Scheiermann C., Chow A., Kunisaki Y., Bruns I., Barrick C., Tessarollo L., Frenette P.S. Chemotherapy-induced bone marrow nerve injury impairs hematopoietic regeneration. Nat. Med. 2013, 19:695-703.
85. Macmahon H.E. Hyperplasia and regeneration of the myocardium in infants and in children. Am. J. Pathol. 1937, 13:845-854.
86. Mahmoud A.I., Kocabas F., Muralidhar S.A., Kimura W., Koura A.S., Thet S., Porrello E.R., Sadek H.A. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 2013, 497:249-253.
87. 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. Nerves regulate cardiomyocyte proliferation and heart regeneration. Dev. Cell 2015, 34:387-399.
88. Mercer S.E., Odelberg S.J., Simon H.-G. A dynamic spatiotemporal extracellular matrix facilitates epicardial-mediated vertebrate heart regeneration. Dev. Biol. 2013, 382:457-469.
89. Miesfeld J.B., Link B.A. Establishment of transgenic lines to monitor and manipulate Yap/Taz-Tead activity in zebrafish reveals both evolutionarily conserved and divergent functions of the Hippo pathway. Mech. Dev. 2014, 133:177-188.
90. Molkentin J.D., Lin Q., Duncan S.A., Olson E.N. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 1997, 11:1061-1072.
91. 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. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl. Acad. Sci. USA 2013, 110:1446-1451.
92. Mysliwiec M.R., Carlson C.D., Tietjen J., Hung H., Ansari A.Z., Lee Y. Jarid2 (Jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J. Biol. Chem. 2012, 287:1235-1241.
93. Nabrit S.M. The role of the fin rays in the regeneration in the tail fins of fishes (fundulus and goldfish). Biol. Bull. 1929, 56:235-266.
94. Oberpriller J.O., Oberpriller J.C. Response of the adult newt ventricle to injury. J. Exp. Zool. 1974, 187:249-253.
95. Ogura Y., Ouchi N., Ohashi K., Shibata R., Kataoka Y., Kambara T., Kito T., Maruyama S., Yuasa D., Matsuo K., et al. Therapeutic impact of follistatin-like 1 on myocardial ischemic injury in preclinical models. Circulation 2012, 126:1728-1738.
96. Oka T., Xu J., Kaiser R.A., Melendez J., Hambleton M., Sargent M.A., Lorts A., Brunskill E.W., Dorn G.W., Conway S.J., et al. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ. Res. 2007, 101:313-321.
97. Orlic D., Kajstura J., Chimenti S., Jakoniuk I., Anderson S.M., Li B., Pickel J., McKay R., Nadal-Ginard B., Bodine D.M., et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001, 410:701-705.
98. Oshima Y., Ouchi N., Sato K., Izumiya Y., Pimentel D.R., Walsh K. Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation 2008, 117:3099-3108.
99. O'Meara C.C., Wamstad J.A., Gladstone R.A., Fomovsky G.M., Butty V.L., Shrikumar A., Gannon J.B., Boyer L.A., Lee R.T. Transcriptional reversion of cardiac myocyte fate during mammalian cardiac regeneration. Circ. Res. 2015, 116:804-815.
100. Pesce M., Burba I., Gambini E., Prandi F., Pompilio G., Capogrossi M.C. Endothelial and cardiac progenitors: boosting, conditioning and (re)programming for cardiovascular repair. Pharmacol. Ther. 2011, 129:50-61.
101. Piatkowski T., Mühlfeld 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. 2013, 22:1921-1931.
102. Porrello E.R., Olson E.N. A neonatal blueprint for cardiac regeneration. Stem Cell Res. 2014, 13:556-570.
103. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
104. Porrello E.R., Johnson B.A., Aurora A.B., Simpson E., Nam Y.-J., Matkovich S.J., Dorn G.W., van Rooij E., Olson E.N. MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ. Res. 2011, 109:670-679.
105. Porrello E.R., Mahmoud A.I., Simpson E., Johnson B.A., Grinsfelder D., Canseco D., Mammen P.P., Rothermel B.A., Olson E.N., Sadek H.A. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. USA 2013, 110:187-192.
106. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science 2002, 298:2188-2190.
107. Qian L., Huang Y., Spencer C.I., Foley A., Vedantham V., Liu L., Conway S.J., Fu J., Srivastava D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
108. Reischauer S., Arnaout R., Ramadass R., Stainier D.Y.R. Actin binding GFP allows 4D in vivo imaging of myofilament dynamics in the zebrafish heart and the identification of Erbb2 signaling as a remodeling factor of myofibril architecture. Circ. Res. 2014, 115:845-856.
109. Reuter S., Soonpaa M.H., Firulli A.B., Chang A.N., Field L.J. Recombinant neuregulin 1 does not activate cardiomyocyte DNA synthesis in normal or infarcted adult mice. PLoS One 2014, 9:e115871.
110. Robledo M. Myocardial regeneration in young rats. Am. J. Pathol. 1956, 32:1215-1239.
111. Rojas-Muñoz A., Rajadhyksha S., Gilmour D., van Bebber F., Antos C., Rodríguez Esteban C., Nüsslein-Volhard C., Izpisúa Belmonte J.C. ErbB2 and ErbB3 regulate amputation-induced proliferation and migration during vertebrate regeneration. Dev. Biol. 2009, 327:177-190.
112. Rollins-Smith L.A. Metamorphosis and the amphibian immune system. Immunol. Rev. 1998, 166:221-230.
113. Rumjancev P.P., Carlson B.M. Growth and Hyperplasia of Cardiac Muscle Cells 1991, Taylor & Francis.
114. Rumyantsev P.P. Post-injury DNA synthesis, mitosis and ultrastructural reorganization of adult frog cardiac myocytes. An electron microscopic-autoradiographic study. Z. Zellforsch. Mikrosk. Anat. 1973, 139:431-450.
115. Rumyantsev P.P. Interrelations of the proliferation and differentiation processes during cardiac myogenesis and regeneration. Int. Rev. Cytol. 1977, 51:186-273.
116. Schindler Y.L., Garske K.M., Wang J., Firulli B.A., Firulli A.B., Poss K.D., Yelon D. Hand2 elevates cardiomyocyte production during zebrafish heart development and regeneration. Development 2014, 141:3112-3122.
117. Schnabel K., Wu C.-C., Kurth T., Weidinger G. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 2011, 6:e18503.
118. 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., Lee R.T. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493:433-436.
119. Soonpaa M.H., Kim K.K., Pajak L., Franklin M., Field L.J. Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 1996, 271:H2183-H2189.
120. Spallanzani A. Reproductions of the legs in the aquatic salamander. An Essay on Animal Reproductions 1769, 68-82. Becket and de Hondt).
121. Stankunas K., Shang C., Twu K.Y., Kao S.-C., Jenkins N.A., Copeland N.G., Sanyal M., Selleri L., Cleary M.L., Chang C.-P. Pbx/Meis deficiencies demonstrate multigenetic origins of congenital heart disease. Circ. Res. 2008, 103:702-709.
122. Stanton L.W., Garrard L.J., Damm D., Garrick B.L., Lam A., Kapoun A.M., Zheng Q., Protter A.A., Schreiner G.F., White R.T. Altered patterns of gene expression in response to myocardial infarction. Circ. Res. 2000, 86:939-945.
123. Strungs E.G., Ongstad E.L., O'Quinn M.P., Palatinus J.A., Jourdan L.J., Gourdie R.G. Cryoinjury models of the adult and neonatal mouse heart for studies of scarring and regeneration. Methods Mol. Biol. 2013, 1037:343-353.
124. Suetsugu-Maki R., Maki N., Nakamura K., Sumanas S., Zhu J., Del Rio-Tsonis K., Tsonis P.A. Lens regeneration in axolotl: new evidence of developmental plasticity. BMC Biol. 2012, 10:103.
125. Sultana N., Zhang L., Yan J., Chen J., Cai W., Razzaque S., Jeong D., Sheng W., Bu L., Xu M., et al. Resident c-kit(+) cells in the heart are not cardiac stem cells. Nat. Commun. 2015, 6:8701.
126. Szibor M., Pöling J., Warnecke H., Kubin T., Braun T. Remodeling and dedifferentiation of adult cardiomyocytes during disease and regeneration. Cell. Mol. Life Sci. 2014, 71:1907-1916.
127. Takaya T., Kawamura T., Morimoto T., Ono K., Kita T., Shimatsu A., Hasegawa K. Identification of p300-targeted acetylated residues in GATA4 during hypertrophic responses in cardiac myocytes. J. Biol. Chem. 2008, 283:9828-9835.
128. Temsah R., Nemer M. GATA factors and transcriptional regulation of cardiac natriuretic peptide genes. Regul. Pept. 2005, 128:177-185.
129. Todd J.T. On the process of reproduction of the members of the aquatic salamander. Q. J. Sci. Lit. Arts 1823, 16:84-96.
130. Tournefier A., Laurens V., Chapusot C., Ducoroy P., Padros M.R., Salvadori F., Sammut B. Structure of MHC class I and class II cDNAs and possible immunodeficiency linked to class II expression in the Mexican axolotl. Immunol. Rev. 1998, 166:259-277.
131. Trinh L.A., Stainier D.Y.R. Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev. Cell 2004, 6:371-382.
132. Trivedi C.M., Zhu W., Wang Q., Jia C., Kee H.J., Li L., Hannenhalli S., Epstein J.A. Hopx and Hdac2 interact to modulate Gata4 acetylation and embryonic cardiac myocyte proliferation. Dev. Cell 2010, 19:450-459.
133. van Berlo J.H., Kanisicak O., Maillet M., Vagnozzi R.J., Karch J., Lin S.-C.J., Middleton R.C., Marbán E., Molkentin J.D. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 2014, 509:337-341.
134. Vihtelic T.S., Hyde D.R. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J. Neurobiol. 2000, 44:289-307.
135. 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. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl. Acad. Sci. USA 2012, 109:2394-2399.
136. Wang L., Marchionni M.A., Tassava R.A. Cloning and neuronal expression of a type III newt neuregulin and rescue of denervated, nerve-dependent newt limb blastemas by rhGGF2. J. Neurobiol. 2000, 43:150-158.
137. Wang J., Greene S.B., Bonilla-Claudio M., Tao Y., Zhang J., Bai Y., Huang Z., Black B.L., Wang F., Martin J.F. Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism. Dev. Cell 2010, 19:903-912.
138. Wang J., Panáková D., Kikuchi K., Holdway J.E., Gemberling M., Burris J.S., Singh S.P., Dickson A.L., Lin Y.-F., Sabeh M.K., et al. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 2011, 138:3421-3430.
139. Wang J., Karra R., Dickson A.L., Poss K.D. Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev. Biol. 2013, 382:427-435.
140. Wang J., Cao J., Dickson A.L., Poss K.D. Epicardial regeneration is guided by cardiac outflow tract and Hedgehog signalling. Nature 2015, 522:226-230.
141. Warthin A.S. The myocardial lesions of diphtheria. J. Infect. Dis. 1924, 35:32-66.
142. Wei K., Serpooshan V., Hurtado C., Diez-Cuñado M., Zhao M., Maruyama S., Zhu W., Fajardo G., Noseda M., Nakamura K., et al. Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature 2015, 525:479-485.
143. Weiss P., Walker R. Nerve pattern in regenerated urodele limbs. Exp. Biol. Med. 1934, 31:810-812.
144. White I.A., Gordon J., Balkan W., Hare J.M. Sympathetic reinnervation is required for mammalian cardiac regeneration. Circ. Res. 2015, 117:990-994.
145. Witman N., Murtuza B., Davis B., Arner A., Morrison J.I. Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. Dev. Biol. 2011, 354:67-76.
146. Xie M., Hill J.A. HDAC-dependent ventricular remodeling. Trends Cardiovasc. Med. 2013, 23:229-235.
147. Xin M., Olson E.N., Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat. Rev. Mol. Cell Biol. 2013, 14:529-541.
148. 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. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA 2013, 110:13839-13844.
149. Yin V.P., Lepilina A., Smith A., Poss K.D. Regulation of zebrafish heart regeneration by miR-133. Dev. Biol. 2012, 365:319-327.
150. Zangi L., Lui K.O., von Gise A., Ma Q., Ebina W., Ptaszek L.M., Später D., Xu H., Tabebordbar M., Gorbatov R., et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol. 2013, 31:898-907.
151. Zhao B., Tumaneng K., Guan K.-L. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 2011, 13:877-883.
152. Zhou Q., Li L., Zhao B., Guan K.-L. The hippo pathway in heart development, regeneration, and diseases. Circ. Res. 2015, 116:1431-1447.