The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation

European Heart Journal

Volumn 35, Issue 39, 2014, Pages 2722-2731

  Waring, Cheryl D ^a   Vicinanza, Carla ^a,b   Papalamprou, Angela ^a,c   Smith, Andrew J ^a   Purushothaman, Saranya ^a,d   Goldspink, David F ^a   Nadal Ginard, Bernardo ^a   Torella, Daniele ^a,b   Ellison, Georgina M ^a,b  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Marriott Heart Disease Research Program   (United States)

Author keywords

Cardiac stem cells; Cardiomyogenesis; Exercise; Growth factors; Myocyte hyperplasia; Physiological remodelling

Indexed keywords

SIGNAL PEPTIDE; STEM CELL FACTOR RECEPTOR;

ANGIOGENESIS; ANIMAL; CAPILLARY; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CARDIOMEGALY; CELL DIFFERENTIATION; CYTOLOGY; EXERCISE; MALE; METABOLISM; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; STEM CELL; UPREGULATION; VASCULAR REMODELING; WISTAR RAT;

ANIMALS; CAPILLARIES; CARDIOMEGALY; CELL DIFFERENTIATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MYOCARDIUM; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; OXYGEN CONSUMPTION; PHYSICAL EXERTION; PROTO-ONCOGENE PROTEINS C-KIT; RATS, WISTAR; STEM CELLS; UP-REGULATION; VASCULAR REMODELING;

EID: 84922450324     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehs338     Document Type: Article

References (30)

1. Tam SK, Gu W, Mahdavi V, Nadal-Ginard B. Cardiac myocyte terminal differentiation. Potential for cardiac regeneration. Ann N Y Acad Sci 1995;752:72-79.
2. Nadal-Ginard B, Kajstura J, Leri A, Anversa P. Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ Res 2003;92: 139-150.
3. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA, Anversa P. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 2001;344:1750-1757.
4. Anversa P, Nadal-Ginard B. Myocyte renewal and ventricular remodelling. Nature 2002;415:240-243.
5. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J. Evidence for cardiomyocyte renewal in humans. Science 2009;324:98-102.
6. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med 2008;358:1370-1380.
7. Ellison GM, Torella D, Karakikes I, Nadal-Ginard B. Myocyte death and renewal: modern concepts of cardiac cellular homeostasis. Nat Clin Pract Cardiovasc Med 2007;4(Suppl. 1):S52-S59.
8. Torella D, Ellison GM, Karakikes L, Nadal-Ginard B. Resident cardiac stem cells. Cell Mol Life Sci 2007;64:661-673.
9. Ellison GM, Galuppo V, Vicinanza C, Aquila I, Waring CD, Leone A, Indolfi C, Torella D. Cardiac stem and progenitor cell identification: different markers for the same cell? Front Biosci (Schol Ed) 2010;2:641-652.
10. Boström P, Mann N, Wu J, Quintero PA, Plovie ER, Panáková D, Gupta RK, Xiao C, MacRae CA, Rosenzweig A, Spiegelman BM. C/EBPb controls exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell 2010;143:1072-1083.
11. Ellison GM, Torella D, Karakikes I, Purushothaman S, Curcio A, Gasparri C, Indolfi C, Cable NT, Goldspink DF, Nadal-Ginard B. Acute beta-adrenergic overload produces myocyte damage through calcium leakage from the ryanodine receptor 2 but spares cardiac stem cells. JBC 2007;282:11397-11409.
12. Catalucci D, Latronico MV, Ellingsen O, Condorelli G. Physiological myocardial hypertrophy: how and why? Front Biosci 2008;13:312-324.
13. Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, Zias E, Walsh K, Rosenzweig A, Sussman MA, Urbanek K, Nadal-Ginard B, Kajstura J, Anversa P, Leri A. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res 2004;94:514-524.
14. Goumans MJ, de Boer TP, Smits AM, van Laake LW, van Vliet P, Metz CH, Korfage TH, Kats KP, Hochstenbach R, Pasterkamp G, Verhaar MC, van der Heyden MA, de Kleijn D, Mummery CL, van Veen TA, Sluijter JP, Doevendans PA. TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 2007;1: 138-149.
15. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW II, Conway SJ, Aronow BJ, Robbins J, Molkentin JD. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 2007;101:313-321.
16. Zhou YY, Sawyer DR, Baliga RR, Opel DJ, Han X, Marchionni MA, 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.
17. Bersell K, Arab S, Haring B, Kuhn B. Neuregulin1/erbb4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009;138:257-270.
18. 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.
19. Suzuki Y, Ohga N, Morishita Y, Hida K, Miyazono K, Watabe T. Bmp-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J Cell Sci 2010;123:1684-1692.
20. Niwa H, Burdon T, Chambers I, Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998;12:2048-2060.
21. Paling NR, Wheadon H, Bone HK,Welham MJ. Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling. J Biol Chem 2004; 279:48063-48070.
22. Teekakirikul P, Eminaga S, Toka O, Alcalai R, Wang L, Wakimoto H, Nayor M, Konno T, Gorham JM, Wolf CM, Kim JB, Schmitt JP, Molkentin JD, Norris RA, Tager AM, Hoffman SR, Markwald RR, Seidman CE, Seidman JG. Cardiac fibrosis in mice with hypertrophic cardiomyopathy is mediated by non-myocyte proliferation and requires tgf-beta. J Clin Invest 2010;120:3520-3529.
23. 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.
24. Wang Z, Xu G, Wu Y, Guan Y, Cui L, Lei X, Zhang J, Mou L, Sun B, Dai Q. Neuregulin-1 enhances differentiation of cardiomyocytes from embryonic stem cells. Med Biol Eng Comput 2009;47:41-48.
25. Ellison GM, Waring CD, Vicinanza C, Torella D. Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart 2012;98:5-10.
26. Noseda M, Peterkin T, Simões FC, Patient R, Schneider MD. Cardiopoietic factors: extracellular signals for cardiac lineage commitment. Circ Res 2011;108: 129-152.
27. 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, Galinañes 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 Am Coll Cardiol 2011;58:977-986.
28. Chong JJ, Chandrakanthan V, Xaymardan M, Asli NS, Li J, Ahmed I, Heffernan C, Menon MK, Scarlett CJ, Rashidianfar A, Biben C, Zoellner H, Colvin EK, Pimanda JE, Biankin AV, Zhou B, Pu WT, Prall OW, Harvey RP. Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 2011;9:527-540.
29. Smart N, Bollini S, Dubé KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu W, Riley PR. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011;474:640-644.
30. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003;100:12313-12318.