Extra- and intracellular factors regulating cardiomyocyte proliferation in postnatal life

Cardiovascular Research

Volumn 102, Issue 2, 2014, Pages 312-320

  Zacchigna, Serena ^a   Giacca, Mauro ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Cardiomyocyte proliferation; Heart regeneration; MicroRNAs; Paracrine control; Secreted factors

Indexed keywords

BETA1 INTEGRIN; COLLAGEN TYPE 1; CYCLIN D1; CYCLIN G1; CYTOKINE; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; FOCAL ADHESION KINASE; GROWTH FACTOR; MESSENGER RNA; MICRORNA; NEU DIFFERENTIATION FACTOR; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE C; SCATTER FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR PAX7; VASCULOTROPIN;

ADIPOCYTE; APOPTOSIS; BONE MARROW CELL; CELL COUNT; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL SIZE; CONGESTIVE CARDIOMYOPATHY; CYTOKINESIS; DNA SYNTHESIS; EMBRYO DEVELOPMENT; ENDOTHELIAL PROGENITOR CELL; EXTRACELLULAR SPACE; FIBROBLAST; G2 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENETIC MANIPULATION; HEART DEVELOPMENT; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; HEMATOPOIETIC STEM CELL; HIGH THROUGHPUT SCREENING; HUMAN; INFLAMMATORY CELL; INTRACELLULAR SPACE; MESENCHYMAL STROMA CELL; MITOSIS; MONONUCLEAR CELL; NONHUMAN; OXYGEN TENSION; OXYGENATION; PERINATAL PERIOD; PRIORITY JOURNAL; REVIEW; STEM CELL NICHE; ANIMAL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL PROLIFERATION; HUMANS; MICRORNAS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84899055908     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu057     Document Type: Review

References (121)

1. Birks EJ. Molecular changes after left ventricular assist device support for heart failure. Circ Res 2013;113:777-791
2. Roger VL. Epidemiology of heart failure. Circ Res 2013;113:646-659
3. Kaye DMKrum H. Drug discovery for heart failure: Anewera or the end of the pipeline?. Nat Rev Drug Discov 2007;6:127-139
4. Sedmera D Reckova M DeAlmeida A Coppen SR Kubalak SW Gourdie RG Thompson RP. Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anat Rec A Discov Mol Cell Evol Biol 2003;274:773-777
5. Soonpaa MH Kim KK Pajak L Franklin M Field LJ. Cardiomyocyte DNA synthesis and binucleation During murine development. Am J Physiol 1996;271:H2183-H2189
6. Liang-Lam M Claycomb W. Regenerative potential of the mammalian heart. In: Engels FB ed. Heart Regeneratinon Stem Cells and Beyond. Singapore:World Scientific Publishing; 2012. p. 81-103
7. Bersell K Arab S Haring B Kuhn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009;138:257-270
8. Porrello ER Mahmoud AI Simpson E Hill JA Richardson JA Olson EN Sadek HA. Transient regenerative potential of the neonatal mouse heart. Science 2011;331: 1078-1080
9. Oberpriller JOOberpriller JC. Response of the adult newt ventricle to injury. J Exp Zool 1974;187:249-253
10. Poss KD Wilson LG Keating MT. Heart regeneration in zebrafish. Science 2002;298: 2188-2190
11. Jopling C Sleep E RayaM Marti M RayaA Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010;464: 606-609
12. Kikuchi K Holdway JE Werdich AA Anderson RM Fang Y Egnaczyk GF Evans T Macrae CA StainierDY PossKD. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010;464:601-605
13. GuptaV Gemberling M Karra R Rosenfeld GE Evans T Poss KD. An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr Biol 2013;23:1221-1227
14. Lepper C Conway SJ Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 2009;460:627-631
15. Collesi C Zentilin L Sinagra G Giacca M. Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol 2008;183:117-128
16. Campa VM Gutierrez-Lanza R Cerignoli F Diaz-Trelles R Nelson B Tsuji T Barcova M JiangW Mercola M. Notch activates cell cycle reentry and progression in quiescent cardiomyocytes. J Cell Biol 2008;183:129-141
17. Croquelois A Domenighetti AA Nemir M Lepore M Rosenblatt-Velin N Radtke F Pedrazzini T. Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J Exp Med 2008;205:3173-3185
18. Raya A Koth CM Buscher D Kawakami Y Itoh T Raya RM Sternik G Tsai HJ Rodriguez-Esteban C Izpisua-Belmonte JC. Activation of Notch signaling pathway precedes heart regeneration in zebrafish. Proc Natl Acad Sci USA 2003;100(Suppl 1): 11889-11895
19. Zhang R Han P Yang H Ouyang K Lee D Lin YF Ocorr K Kang G Chen J StainierDY Yelon D Chi NC. In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 2013;498:497-501
20. Li FWang X Bunger PC Gerdes AM. Formation of binucleated cardiac myocytes in rat heart: I. Role of actin-myosin contractile ring. J Mol Cell Cardiol 1997;29:1541-1551
21. Li FWang X Gerdes AM. Formation of binucleated cardiac myocytes in rat heart: II. Cytoskeletal organisation. J Mol Cell Cardiol 1997;29:1553-1565
22. Ahuja P Perriard E Perriard JC Ehler E. Sequential myofibrillar breakdown accompanies mitotic division of mammalian cardiomyocytes. J Cell Sci 2004;117:3295-3306
23. Claycomb WC. Control of cardiac muscle cell division. Trends Cardiovasc Med 1992;2: 231-236
24. Senyo SE Steinhauser ML Pizzimenti CL Yang VK Cai L Wang M Wu TD Guerquin-Kern JL Lechene CP Lee RT. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013;493:433-436
25. Burton PB Raff MC Kerr P Yacoub MH Barton PJ. An intrinsic timer that controls cellcycle withdrawal in cultured cardiac myocytes. Dev Biol 1999;216:659-670
26. Heymann MA Rudolph AM. Control of the ductus arteriosus. Physiol Rev 1975;55: 62-78
27. Yokoyama U Minamisawa S Ishikawa Y. Regulation of vascular tone and remodeling of the ductus arteriosus. J Smooth Muscle Res 2010;46:77-87
28. Kocabas F Mahmoud AI Sosic D Porrello ER Chen R Garcia JA DeBerardinis RJ Sadek HA. The hypoxic epicardial and subepicardial microenvironment. J Cardiovasc Transl Res 2012;5:654-665
29. Zhou B Ma Q Rajagopal S Wu SM Domian I Rivera-Feliciano J Jiang D von Gise A Ikeda S Chien KR Pu WT. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008;454:109-113
30. Cai CL Martin JC Sun Y Cui L Wang L Ouyang K Yang L Bu L Liang X Zhang X Stallcup WB Denton CP McCulloch A Chen J Evans SM. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008;454:104-108
31. Smart N Bollini S Dube KN Vieira JM Zhou B Davidson S Yellon D Riegler J Price AN LythgoeMF PuWT Riley PR. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011;474:640-644
32. Wei C Kumar S Kim IK Gupta S. Thymosin beta 4 protects cardiomyocytes from oxidative stress by targeting anti-oxidative enzymes and anti-Apoptotic genes. PLoS ONE 2012;7:e42586
33. van Oorschot AA Smits AM Pardali E Doevendans PA Goumans MJ. Low oxygen tension positively influences cardiomyocyte progenitor cell function. J Cell Mol Med 2011;15:2723-2734
34. Thompson RP Reckova M deAlmeida A Bigelow MR Stanley CP Spruill JB Trusk TT Sedmera D. The oldest toughest cells in the heart. Novartis Found Symp 2003;250: 157-174; discussion 174-156 276-159
35. Hoshijima M. Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk titin and associated structures. Am J Physiol Heart Circ Physiol 2006;290: H1313-H1325
36. Palmieri EA Benincasa G Di Rella F Casaburi C Monti MG De Simone G Chiariotti L Palombini L Bruni CB Sacca L Cittadini A. Differential expression of TNF-Alpha IL-6 and IGF-1 by graded mechanical stress in normal rat myocardium.Am J Physiol Heart Circ Physiol 2002;282:H926-H934
37. Schmelter M Ateghang B Helmig S Wartenberg M Sauer H. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 2006;20:1182-1184
38. Ieda M Tsuchihashi T Ivey KN Ross RS Hong TT Shaw RM Srivastava D. Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 2009;16:233-244
39. Hakim ZS DiMichele LA Doherty JT Homeister JW Beggs HE Reichardt LF Schwartz RJ Brackhan J Smithies O Mack CP Taylor JM. Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol Cell Biol 2007;27:5352-5364
40. Peng X Wu X Druso JE Wei H Park AY Kraus MS Alcaraz A Chen J Chien S Cerione RA Guan JL. Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc Natl Acad Sci USA 2008;105:6638-6643
41. ONeill TJ Mack CP Taylor JM. Germline deletion of FAK-related non-kinase delays post-natal cardiomyocyte mitotic arrest. J Mol Cell Cardiol 2012;53:156-164
42. DiMichele LA Hakim ZS Sayers RL Rojas M Schwartz RJ Mack CP Taylor JM. Transient expression of FRNK reveals stage-specific requirement for focal adhesion kinase activity in cardiac growth. Circ Res 2009;104:1201-1208
43. van Amerongen M Engel F. Induction of cardiomyocyte proliferation. In: Engels FB ed. Heart Regeneration Stem Cells and Beyond: Singapore:World Scientific Publishing; 2012. p. 105-134
44. Bicknell KA Coxon CH Brooks G. Can the cardiomyocyte cell cycle be reprogrammed?. J Mol Cell Cardiol 2007;42:706-721
45. Pasumarthi KB Field LJ. Cardiomyocyte cell cycle regulation. Circ Res 2002;90: 1044-1054
46. Chaudhry HW Dashoush NH Tang H Zhang L Wang X Wu EX Wolgemuth DJ. Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J Biol Chem 2004;279:35858-35866
47. Woo YJ Panlilio CM Cheng RK Liao GP Atluri P Hsu VM Cohen JE Chaudhry HW. Therapeutic delivery of cyclin A2 induces myocardial regeneration and enhances cardiac function in ischemic heart failure. Circulation 2006;114:I206-I213
48. Liao HS Kang PM Nagashima H Yamasaki N Usheva A Ding B Lorell BH Izumo S. Cardiac-specific overexpression of cyclin-dependent kinase 2 increases smaller mononuclear cardiomyocytes. Circ Res 2001;88:443-450
49. Soonpaa MH Koh GY Pajak L Jing SWang H Franklin MT Kim KK Field LJ. Cyclin D1 overexpression promotes cardiomyocyteDNAsynthesis andmultinucleation in transgenic mice. J Clin Invest 1997;99:2644-2654
50. Pasumarthi KB Nakajima H Nakajima HO Soonpaa MH Field LJ. Targeted expression of cyclinD2results in cardiomyocyteDNAsynthesis and infarct regression in transgenic mice. Circ Res 2005;96:110-118
51. Hassink RJ Pasumarthi KB Nakajima H Rubart M Soonpaa MH de la Riviere AB Doevendans PA Field LJ. Cardiomyocyte cell cycle activation improves cardiac function after myocardial infarction. Cardiovasc Res 2008;78:18-25
52. Mahmoud AI Kocabas F Muralidhar SA Kimura W Koura AS Thet S Porrello ER Sadek HA. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 2013; 497:249-253
53. Saucedo LJ Edgar BA. Filling out the Hippo pathway. Nat Rev Mol Cell Biol 2007;8: 613-621
54. Pan D. The Hippo signaling pathway in Development and cancer. Dev Cell 2010;19: 491-505
55. Heallen T Zhang MWang J Bonilla-Claudio M Klysik E Johnson RL Martin JF. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011;332:458-461
56. Yamamoto S Yang G Zablocki D Liu J Hong C Kim SJ Soler S Odashima M Thaisz J Yehia G Molina CA Yatani A Vatner DE Vatner SF Sadoshima J. Activation of Mst1 causes dilated cardiomyopathy by stimulating apoptosis without compensatory ventricular myocyte hypertrophy. J Clin Invest 2003;111:1463-1474
57. Matsui YY Nakano NN Shao DD Gao SS Luo WW Hong CC Zhai PP Holle EE Yu XX YabutaNNTaoWWWagnerTT Nojima HH Sadoshima JJ. Lats2 is a negative regulator of myocyte size in the heart. Circ Res 2008;103:1309-1318
58. Xin M Kim Y Sutherland LB Qi X McAnally J Schwartz RJ Richardson JA Bassel-Duby R Olson EN. Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci Signal 2011;4:ra70
59. von Gise A Lin Z Schlegelmilch K Honor LB Pan GM Buck JN Ma Q Ishiwata T Zhou B Camargo FD Pu WT. 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
60. Del Re DP Yang Y Nakano N Cho J Zhai P Yamamoto T Zhang N Yabuta N Nojima H PanD Sadoshima J. Yes-Associated protein isoform 1 (Yap1) promotes cardiomyocyte survival and growth to protect against myocardial ischemic injury. J Biol Chem 2013;288:3977-3988
61. Xin M Kim Y Sutherland LB Murakami M Qi X McAnally J Porrello ER Mahmoud AI Tan W Shelton JM Richardson JA Sadek HA Bassel-Duby R Olson EN. Hippo pathway effector Yap promotes cardiac regeneration. Proc Natl Acad Sci USA 2013; 110:13839-13844
62. Nishioka N Inoue K Adachi K Kiyonari H Ota M Ralston A Yabuta N Hirahara S Stephenson RO Ogonuki N Makita R Kurihara H Morin-Kensicki EM Nojima H Rossant J Nakao K Niwa H Sasaki H. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 2009;16:398-410
63. Heallen T Morikawa Y Leach J Tao G Willerson JT Johnson RL Martin JF. Hippo signaling impedes adult heart regeneration. Development 2013;140:4683-4690
64. Hamilton G Yee KS Scrace S ONeill E. ATM regulates a RASSF1A-dependent DNA damage response. Curr Biol 2009;19:2020-2025
65. Ota M Sasaki H. Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 2008;135: 4059-4069
66. Zhao BWei X LiW Udan RS Yang Q Kim J Xie J Ikenoue T Yu J Li L Zheng P Ye K Chinnaiyan A Halder G Lai ZC Guan KL. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007;21:2747-2761
67. Halder G Dupont S Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol 2012;13:591-600
68. van Rooij E. The art of microRNA research. Circ Res 2011;108:219-234
69. Small EM Frost RJ Olson EN. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2011;121:1022-1032
70. ZhaoY Samal E Srivastava D. Serum response factor regulates a muscle-specific micro-RNA that targets Hand2 during cardiogenesis. Nature 2005;436:214-220
71. Chen JF Murchison EP Tang R Callis TE Tatsuguchi M Deng Z Rojas M Hammond SM Schneider MD Selzman CH Meissner G Patterson C Hannon GJ Wang DZ. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA 2008;105:2111-2116
72. da Costa Martins PA Bourajjaj M Gladka M Kortland M van Oort RJ Pinto YM Molkentin JD De Windt LJ. Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 2008;118:1567-1576
73. Ali R HuangYMaher SE KimRW GiordanoFJTellides G Geirsson A. miR-1 mediated suppression of Sorcin regulates myocardial contractility through modulation of Ca2+ signaling. J Mol Cell Cardiol 2012;52:1027-1037
74. Porrello ER Johnson BA Aurora AB Simpson ENamYJ Matkovich SJ DornGWII van Rooij E Olson EN. MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ Res 2011;109:670-679
75. 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 2013; 110:187-192
76. Hullinger TG Montgomery RL Seto AG Dickinson BA Semus HM Lynch JM Dalby CM Robinson K Stack C Latimer PA Hare JM Olson EN van Rooij E. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res 2012;110:71-81
77. Yin VP Lepilina A Smith A Poss KD. Regulation of zebrafish heart regeneration by miR-133. Dev Biol 2012;365:319-327
78. CaoXWang JWang ZDuJ Yuan X HuangWMeng JGuH NieY Ji BHuS Zheng Z. MicroRNA profiling during rat ventricular maturation: A role for miR-29a in regulating cardiomyocyte cell cycle re-entry. FEBS Lett 2013;587:1548-1555
79. Eulalio A Mano M Dal FerroM Zentilin L Sinagra G Zacchigna S Giacca M. Functional screening identifiesmiRNAs inducing cardiac regeneration. Nature 2012;492:376-381
80. Li XWang J Jia Z Cui Q ZhangCWangW Chen P Ma K Zhou C. MiR-499 regulates cell proliferation and apoptosis during late-stage cardiac differentiation via Sox6 and cyclin D1. PLoS ONE 2013;8:e74504
81. He L Thomson JM Hemann MT Hernando-Monge E Mu D Goodson S Powers S Cordon-Cardo C Lowe SW Hannon GJ Hammond SM. A microRNA polycistron as a potential human oncogene. Nature 2005;435:828-833
82. ODonnell KA Wentzel EA Zeller KI Dang CV Mendell JT. c-Myc-regulated micro-RNAs modulate E2F1 expression. Nature 2005;435:839-843
83. Chen J Huang ZP Seok HY Ding J Kataoka M Zhang ZHuXWang G Lin ZWang S Pu WT Liao R Wang DZ. mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res 2013;112: 1557-1566.
84. Kardami E Banerji S DobleBW Dang X Fandrich RR JinY Cattini PA. PKC-dependent phosphorylation may regulate the ability of connexin43 to inhibit DNA synthesis. Cell Commun Adhes 2003;10:293-297
85. Lu SY Sontag DP Detillieux KA Cattini PA. FGF-16 is released from neonatal cardiac myocytes and alters growth-related signaling: A possible role in postnatal development. Am J Physiol Cell Physiol 2008;294:C1242-C1249
86. Hinrichsen R Haunso S Busk PK. Different regulation of p27 and Akt during cardiomyocyte proliferation and hypertrophy. Growth Factors 2007;25:132-140
87. Zhou B Honor LB He H Ma Q Oh JH Butterfield C Lin RZ Melero-Martin JM Dolmatova E Duffy HS Gise A Zhou P Hu YWWang G Zhang BWang L Hall JL Moses MA McGowan FX Pu WT. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J Clin Invest 2011;121:1894-1904
88. Przybyt E Krenning G Brinker MG Harmsen MC. Adipose stromal cells primed with hypoxia and inflammation enhance cardiomyocyte proliferation rate in vitro through STAT3 and Erk1/2. J Transl Med 2013;11:39
89. Novoyatleva T Diehl F van Amerongen MJ Patra C Ferrazzi F Bellazzi R Engel FB. TWEAK is a positive regulator of cardiomyocyte proliferation. Cardiovasc Res 2010; 85:681-690
90. Shi J Jiang B Qiu Y Guan J Jain M Cao X BauerM Su L Burkly LC Leone TC Kelly DP Liao R. PGC1alpha plays a critical role in TWEAK-induced cardiac dysfunction. PLoS ONE 2013;8:e54054
91. Novoyatleva T JanssenW Wietelmann A Schermuly RT Engel FB. TWEAK/Fn14 axis is a positive regulator of cardiac hypertrophy. Cytokine 2013;64:43-45
92. Lemmens K Doggen K De KeulenaerGW. Role of neuregulin-1/ErbB signaling in cardiovascular physiology and disease: Implications for therapy of heart failure. Circulation 2007;116:954-960
93. Engel FB Schebesta M Duong MT Lu G Ren S Madwed JB Jiang H Wang Y KeatingMT. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 2005;19:1175-1187
94. ZhaoYY Sawyer DR Baliga RR Opel DJHan X MarchionniMA Kelly RA. Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J Biol Chem 1998;273: 10261-10269
95. Odiete O Hill MF Sawyer DB. Neuregulin in cardiovascular development and disease. Circ Res 2012;111:1376-1385
96. Cote GM Sawyer DB Chabner BA. ERBB2 inhibition and heart failure. N Engl J Med 2012;367:2150-2153
97. 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 2007;13:962-969
98. Conway SJ Molkentin JD. Periostin as a heterofunctional regulator of cardiac development and disease. Curr Genomics 2008;9:548-555
99. Shimazaki M Nakamura K Kii I Kashima T Amizuka N Li M Saito M Fukuda K Nishiyama T Kitajima S Saga Y Fukayama M Sata M Kudo A. Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 2008;205:295-303
100. Lorts A Schwanekamp JA Elrod JW Sargent MA Molkentin JD. 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
101. Ladage D Yaniz-Galende E Rapti K Ishikawa K Tilemann L Shapiro S Takewa Y Muller-Ehmsen J Schwarz M Garcia MJ Sanz J Hajjar RJ Kawase Y. Stimulating myocardial regeneration with periostin peptide in large mammals improves function postmyocardial infarction but increases myocardial fibrosis. PLoS ONE 2013;8:e59656
102. Zhao SWuH XiaW Chen X Zhu S Zhang S ShaoYMaW Yang D Zhang J. Periostin expression is upregulated and associated with myocardial fibrosis in human failing hearts. J Cardiol 2013; [Epub ahead of print].
103. Segers VF Lee RT. Stem-cell therapy for cardiac disease. Nature 2008;451:937-942
104. Garbern JC Lee RT. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell 2013;12:689-698
105. Balsam LBWagers AJ Christensen JL Kofidis TWeissman IL Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 2004;428:668-673
106. Murry CE Soonpaa MH Reinecke H Nakajima H Nakajima HO Rubart M Pasumarthi KB Virag JI Bartelmez SH Poppa V Bradford G Dowell JD Williams DA Field LJ. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004;428:664-668
107. Malliaras K Zhang Y Seinfeld J Galang G Tseliou E Cheng K Sun B Aminzadeh M Marban E. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med 2013;5:191-209
108. Gnecchi M Zhang Z Ni A Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008;103:1204-1219
109. Mirotsou M Jayawardena TM Schmeckpeper J GnecchiM Dzau VJ. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J Mol Cell Cardiol 2011; 50:280-289
110. Koudstaal S Bastings MM Feyen DA Waring CD van Slochteren FJ Dankers PY Torella D Sluijter JP Nadal-Ginard B Doevendans PA EllisonGM Chamuleau SA. Sustained delivery of insulin-like growth factor-1/hepatocyte growth factor stimulates endogenous cardiac repair in the chronic infarcted pig heart. J Cardiovasc Transl Res 2014; [Epub ahead of print].
111. Ellison GM Torella D Dellegrottaglie S Perez-Martinez C Perez de Prado A Vicinanza C Purushothaman S Galuppo V Iaconetti C Waring CD Smith A Torella M Cuellas Ramon C Gonzalo-Orden JM Agosti V Indolfi C Galinanes M Fernandez-Vazquez F Nadal-Ginard B. Endogenous cardiac stem cell activation by insulin-like growth factor-1/hepatocyte growth factor intracoronary injection fosters survival and regeneration of the infarcted pig heart. J AmColl Cardiol 2011;58:977-986
112. Linke A Muller P Nurzynska D Casarsa C Torella D Nascimbene A Castaldo C Cascapera S Bohm M Quaini F Urbanek K Leri A Hintze TH Kajstura J Anversa P. Stem cells in the dog heart are self-renewing clonogenic and multipotent and regenerate infarcted myocardium improving cardiac function. Proc Natl Acad Sci USA 2005; 102:8966-8971
113. Beigi F Schmeckpeper J Pow-Anpongkul P Payne JA Zhang L Zhang Z Huang J Mirotsou M Dzau VJ. C3orf58 a novel paracrine protein stimulates cardiomyocyte cell-cycle progression through the PI3K-AKT-CDK7 pathway. Circ Res 2013;113: 372-380
114. Formiga FR Pelacho B Garbayo E Imbuluzqueta I Diaz-Herraez P Abizanda G Gavira JJ Simon-Yarza T Albiasu E Tamayo E Prosper F Blanco-Prieto MJ. Controlled delivery of fibroblast growth factor-1 and neuregulin-1 from biodegradable microparticles promotes cardiac repair in a rat myocardial infarction model through activation of endogenous regeneration. J Control Release 2014;173:132-139
115. Tao Z Chen B Tan X Zhao YWang L Zhu T Cao K Yang Z Kan YW Su H. Coexpression of VEGF and angiopoietin-1 promotes angiogenesis and cardiomyocyte proliferation reduces apoptosis in porcine myocardial infarction (MI) heart. Proc Natl Acad Sci USA 2011;108:2064-2069
116. Tang JM Wang JN Zhang L Zheng F Yang JY Kong X Guo LY Chen L Huang YZ Wan Y Chen SY. VEGF/SDF-1 promotes cardiac stem cell mobilization and myocardial repair in the infarcted heart. Cardiovasc Res 2011;91:402-411
117. Zangi L Lui KO von Gise A Ma Q Ebina W Ptaszek LM Spater D Xu H Tabebordbar M Gorbatov R Sena B Nahrendorf M Briscoe DM Li RA Wagers AJ Rossi DJ Pu WT Chien KR. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol 2013;31:898-907
118. Jo JO Kang YJ Ock MS Kleinman HK Chang HK Cha HJ. Thymosin beta4 expression in human tissues and in tumors using tissue microarrays. Appl Immunohistochem Mol Morphol 2011;19:160-167
119. McDonnell TJ Oberpriller JO. The atrial proliferative response following partial ventricular amputation in the heart of the adult newt. A light and electron microscopic autoradiographic study. Tissue Cell 1983;15:351-363
120. Bettencourt-Dias M Mittnacht S Brockes JP. Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J Cell Sci 2003;116:4001-4009
121. 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 2006;103:15546-15551