Adult and Pluripotent Stem Cells pp 21-35 | Cite as
Resident Cardiac Progenitor Cells
Abstract
Resident cardiac stem/progenitor cells are implicated in cell replacement, repair and maintenance of the myocardium. These cells are already committed to a specific cardiomyogenic pathway. Stimulation of these cells in injured hearts can open new options in cardiovascular regenerative medicine, and advance our approach to patients with end-stage heart failure. This chapter reviews some of the recent discoveries in the field of resident cardiac stem/progenitor cells, focusing first on human cardiac stem cell characteristics and reparative potential, including the concept of myocardial regeneration. In addition, we will briefly review recent clinical trials, controversies and unresolved issues.
Keywords
Cardiac progenitor cells Clinical stem cell trials Intermyocardial injection Repair of myocardium Resident cardiac stem cells Self-renewal of cardiomyocytes Stem cell transplantationNotes
Source of Funding
This work was supported by an EC grant (FP7 HEALTH-F2–2009-222995 INELPY) to JL.
References
- Aghila Rani KG, Jayakumar K, Sarma PS, Kartha CC (2009) Clinical determinants of ckit-positive cardiac cell yield in coronary disease. Asian Cardiovasc Thorac Ann 17(2):139–142. doi:10.1177/0218492309103292PubMedCrossRefGoogle Scholar
- Anversa P, Rota M, Urbanek K, Hosoda T, Sonnenblick E, Leri A, Kajstura J, Bolli R (2005) Myocardial aging. Basic Res Cardio 100(6):482–493CrossRefGoogle Scholar
- Anversa P, Kajstura J, Leri A, Bolli R (2006) Life and death of cardiac stem cells: a paradigm shift in cardiac biology. Circulation 113(11):1451–1463. doi:113/11/1451 [pii] 10.1161/CIRCULATIONAHA.105.595181PubMedCrossRefGoogle Scholar
- Argentin S, Ardati A, Tremblay S, Lihrmann I, Robitaille L, Drouin J, Nemer M (1994) Developmental stage-specific regulation of atrial natriuretic factor gene transcription in cardiac cells. Mol Cell Biol 14(1):777–790PubMedCentralPubMedGoogle Scholar
- Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3):221–228. doi:10.1161/01.res.85.3.221PubMedCrossRefGoogle Scholar
- Bearzi C, Rota M, Hosoda T, Tillmanns J, Nascimbene A, De Angelis A, Yasuzawa-Amano S, Trofimova I, Siggins RW, LeCapitaine N, Cascapera S, Beltrami AP, D’Alessandro DA, Zias E, Quaini F, Urbanek K, Michler RE, Bolli R, Kajstura J, Leri A, Anversa P (2007) Human cardiac stem cells. Proc Natl Acad Sci U S A 104(35):14068–14073. doi:10.1073/pnas.0706760104PubMedCentralPubMedCrossRefGoogle Scholar
- Beltrami AP, Urbanek K, Kajstura J, Yan S-M, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA, Anversa P (2001) Evidence that human cardiac Myocytes divide after myocardial infarction. N Engl J Med 344(23):1750–1757. doi:10.1056/nejm200106073442303PubMedCrossRefGoogle Scholar
- Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114(6):763–776. doi:S0092867403006871 [pii]PubMedCrossRefGoogle Scholar
- Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J (2009) Evidence for cardiomyocyte renewal in humans. Science 324(5923):98–102. doi:10.1126/science.1164680PubMedCentralPubMedCrossRefGoogle Scholar
- Bock-Marquette I, Saxena A, White MD, Dimaio JM, Srivastava D (2004) Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432(7016):466–472. doi:10.1038/nature03000PubMedCrossRefGoogle Scholar
- Bolli R, Chugh AR, D’Amario D, Loughran JH, Stoddard MF, Ikram S, Beache GM, Wagner SG, Leri A, Hosoda T, Sanada F, Elmore JB, Goichberg P, Cappetta D, Solankhi NK, Fahsah I, Rokosh DG, Slaughter MS, Kajstura J, Anversa P (2011) Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378(9806):1847–1857. doi:10.1016/S0140-6736(11)61590-0PubMedCentralPubMedCrossRefGoogle Scholar
- Chien KR (2005) Alchemy and the new age of cardiac muscle cell biology. PLoS Biol 3(4):e131PubMedCentralPubMedCrossRefGoogle Scholar
- Chimenti C, Kajstura J, Torella D, Urbanek K, Heleniak H, Colussi C, Di Meglio F, Nadal-Ginard B, Frustaci A, Leri A, Maseri A, Anversa P (2003) Senescence and death of primitive cells and myocytes lead to premature cardiac aging and heart failure. Circ Res 93(7):604–613. doi:10.1161/01.res.0000093985.76901.afPubMedCrossRefGoogle Scholar
- Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, Marban E (2010) Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res 106(5):971–980. doi:10.1161/CIRCRESAHA.109.210682PubMedCrossRefGoogle Scholar
- D’Amario D, Cabral-Da-Silva MC, Zheng H, Fiorini C, Goichberg P, Steadman E, Ferreira-Martins J, Sanada F, Piccoli M, Cappetta D, D’Alessandro DA, Michler RE, Hosoda T, Anastasia L, Rota M, Leri A, Anversa P, Kajstura J (2011) Insulin-like growth factor-1 receptor identifies a pool of human cardiac stem cells with superior therapeutic potential for myocardial regeneration. Circ Res 108(12):1467–1481. doi:10.1161/CIRCRESAHA.111.240648PubMedCentralPubMedCrossRefGoogle Scholar
- Davis ME, Hsieh PC, Takahashi T, Song Q, Zhang S, Kamm RD, Grodzinsky AJ, Anversa P, Lee RT (2006) Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci U S A 103(21):8155–8160. doi:0602877103 [pii] 10.1073/pnas.0602877103PubMedCentralPubMedCrossRefGoogle Scholar
- Etzion S, Battler A, Barbash IM, Cagnano E, Zarin P, Granot Y, Kedes LH, Kloner RA, Leor J (2001) Influence of embryonic cardiomyocyte transplantation on the progression of heart failure in a rat model of extensive myocardial infarction. J Mol Cell Cardiol 33(7):1321–1330PubMedCrossRefGoogle Scholar
- Ferreira-Martins J, Ogorek B, Cappetta D, Matsuda A, Signore S, D’Amario D, Kostyla J, Steadman E, Ide-Iwata N, Sanada F, Iaffaldano G, Ottolenghi S, Hosoda T, Leri A, Kajstura J, Anversa P, Rota M (2012) Cardiomyogenesis in the developing heart is regulated by c-kit-positive cardiac stem cells. Circ Res 110(5):701–715. doi:10.1161/CIRCRESAHA.111.259507PubMedCentralPubMedCrossRefGoogle Scholar
- Forrester JS, Makkar RR, Marban E (2009) Long-term outcome of stem cell therapy for acute myocardial infarction: right results, wrong reasons. J Am Coll Cardiol 53(24):2270–2272. doi:S0735-1097(09)01063-8 [pii] 10.1016/j.jacc.2009.03.023PubMedCrossRefGoogle Scholar
- Gambini E, Pesce M, Persico L, Bassetti B, Gambini A, Alamanni F, Agrifoglio M, Capogrossi MC, Pompilio G (2012) Patient profile modulates cardiac c-kit+ progenitor cell availability and amplification potential. Transl Res 160(5):1–11CrossRefGoogle Scholar
- Gonzalez A, Rota M, Nurzynska D, Misao Y, Tillmanns J, Ojaimi C, Padin-Iruegas ME, Muller P, Esposito G, Bearzi C, Vitale S, Dawn B, Sanganalmath SK, Baker M, Hintze TH, Bolli R, Urbanek K, Hosoda T, Anversa P, Kajstura J, Leri A (2008) Activation of cardiac progenitor cells reverses the failing heart senescent phenotype and prolongs lifespan. Circ Res 102(5):597–606. doi:10.1161/circresaha.107.165464PubMedCrossRefGoogle Scholar
- Goumans M-J, de Boer TP, Smits AM, van Laake LW, van Vliet P, Metz CHG, Korfage TH, Kats KP, Hochstenbach R, Pasterkamp G, Verhaar MC, van der Heyden MAG, de Kleijn D, Mummery CL, van Veen TAB, Sluijter JPG, Doevendans PA (2008) TGF-[beta]1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 1(2):138–149CrossRefGoogle Scholar
- Hatzistergos KE, Quevedo H, Oskouei BN, Hu Q, Feigenbaum GS, Margitich IS, Mazhari R, Boyle AJ, Zambrano JP, Rodriguez JE, Dulce R, Pattany PM, Valdes D, Revilla C, Heldman AW, McNiece I, Hare JM (2010) Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 107(7):913–922. doi:10.1161/CIRCRESAHA.110.222703PubMedCentralPubMedCrossRefGoogle Scholar
- Hsieh PCH, Segers VFM, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT (2007) Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13(8):970–974PubMedCentralPubMedCrossRefGoogle Scholar
- Itzhaki-Alfia A, Leor J, Raanani E, Sternik L, Spiegelstein D, Netser S, Holbova R, Pevsner-Fischer M, Lavee J, Barbash IM (2009) Patient characteristics and cell source determine the number of isolated human cardiac progenitor cells. Circulation 120(25):2559–2566. doi:CIRCULATIONAHA.109.849588 [pii] 10.1161/CIRCULATIONAHA.109.849588PubMedCrossRefGoogle Scholar
- Kajstura J, Leri A, Finato N, Di Loreto C, Beltrami CA, Anversa P (1998) Myocyte proliferation in end-stage cardiac failure in humans. Proc Natl Acad Sci U S A 95(15):8801–8805. doi:10.1073/pnas.95.15.8801PubMedCentralPubMedCrossRefGoogle Scholar
- Kubin T, Poling J, Kostin S, Gajawada P, Hein S, Rees W, Wietelmann A, Tanaka M, Lorchner H, Schimanski S, Szibor M, Warnecke H, Braun T (2011) Oncostatin M is a major mediator of cardiomyocyte dedifferentiation and remodeling. Cell Stem Cell 9(5):420–432. doi:S1934-5909(11)00394-8 [pii] 10.1016/j.stem.2011.08.013PubMedCrossRefGoogle Scholar
- Kubo H, Jaleel N, Kumarapeli A, Berretta RM, Bratinov G, Shan X, Wang H, Houser SR, Margulies KB (2008) Increased cardiac myocyte progenitors in failing human hearts. Circulation 118(6):649–657. doi:10.1161/circulationaha.107.761031PubMedCentralPubMedCrossRefGoogle Scholar
- Laflamme MA, Murry CE (2005) Regenerating the heart. Nat Biotech 23 (7):845–856CrossRefGoogle Scholar
- Laflamme MA, Murry CE (2011) Heart regeneration. Nature 473 (7347):326–335. doi:10.1038/nature10147PubMedCrossRefGoogle Scholar
- Landa N, Miller L, Feinberg MS, Holbova R, Shachar M, Freeman I, Cohen S, Leor J (2008) Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117(11):1388–1396. doi:10.1161/circulationaha.107.727420PubMedCrossRefGoogle Scholar
- Laugwitz K-L, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin L-Z, Cai C-L, Lu MM, Reth M, Platoshyn O, Yuan JXJ, Evans S, Chien KR (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433(7026):647–653PubMedCrossRefGoogle Scholar
- Leor J, Patterson M, Quinones MJ, Kedes LH, Kloner RA (1996) Transplantation of fetal myocardial tissue into the infarcted myocardium of rat. A potential method for repair of infarcted myocardium? Circulation 94(9 Suppl):II332–336Google Scholar
- Loffredo FS, Steinhauser ML, Gannon J, Lee RT (2011) Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 8(4):389–398. doi:10.1016/j.stem.2011.02.002PubMedCrossRefGoogle Scholar
- Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marban L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marban E (2012) Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379(9819):895–904. doi:10.1016/S0140-6736(12)60195-0PubMedCrossRefGoogle Scholar
- Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MVG, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95(9):911–921. doi:10.1161/01.res.0000147315.71699.51PubMedCrossRefGoogle Scholar
- Mohsin S, Khan M, Toko H, Bailey B, Cottage CT, Wallach K, Nag D, Lee A, Siddiqi S, Lan F, Fischer KM, Gude N, Quijada P, Avitabile D, Truffa S, Collins B, Dembitsky W, Wu JC, Sussman MA (2012) Human cardiac progenitor cells engineered with pim-i kinase enhance myocardial repair. J Am Coll Cardiol 60(14):1278–1287. doi:10.1016/j.jacc.2012.04.047Google Scholar
- Morrison SJ, Wandycz AM, Hemmati HD, Wright DE, Weissman IL (1997) Identification of a lineage of multipotent hematopoietic progenitors. Development 124(10):1929–1939PubMedGoogle Scholar
- Muller-Sieburg CE, Cho RH, Thoman M, Adkins B, Sieburg HB (2002) Deterministic regulation of hematopoietic stem cell self-renewal and differentiation. Blood 100(4):1302–1309PubMedGoogle Scholar
- Nelson WD, Zenovich AG, Ott HC, Stolen C, Caron GJ, Panoskaltsis-Mortari A, Barnes SA III, Xin X, Taylor DA (2007) Sex-dependent attenuation of plaque growth after treatment with bone marrow mononuclear cells. Circ Res 101(12):1319–1327. doi:10.1161/circresaha.107.155564PubMedCrossRefGoogle Scholar
- Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD (2003) Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A 100(21):12313–12318. doi:10.1073/pnas.2132126100PubMedCentralPubMedCrossRefGoogle Scholar
- Olivetti G, Giordano G, Corradi D, Melissari M, Lagrasta C, Gambert SR, Anversa P (1995) Gender differences and aging: effects on the human heart. J Am Coll Cardiol 26(4):1068–1079PubMedCrossRefGoogle Scholar
- Orlic D, Fischer R, Nishikawa S, Nienhuis AW, Bodine DM (1993) Purification and characterization of heterogeneous pluripotent hematopoietic stem cell populations expressing high levels of c-kit receptor. Blood 82(3):762–770PubMedGoogle Scholar
- Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701–705PubMedCrossRefGoogle Scholar
- Oskouei BN, Lamirault G, Joseph C, Treuer AV, Landa S, Da Silva J, Hatzistergos K, Dauer M, Balkan W, McNiece I, Hare JM (2012) Increased potency of cardiac stem cells compared with bone marrow mesenchymal stem cells in cardiac repair. Stem Cells Transl Med 1(2):116–124. doi:10.5966/sctm.2011-0015PubMedCentralPubMedCrossRefGoogle Scholar
- Ott HC, Matthiesen TS, Brechtken J, Grindle S, Goh SK, Nelson W, Taylor DA (2007) The adult human heart as a source for stem cells: repair strategies with embryonic-like progenitor cells. Nat Clin Pract Cardiovasc Med 4(Suppl 1):S27–S39PubMedCrossRefGoogle Scholar
- Parker TG, Chow KL, Schwartz RJ, Schneider MD (1990a) Differential regulation of skeletal alpha-actin transcription in cardiac muscle by two fibroblast growth factors. Proc Natl Acad Sci U S A 87(18):7066–7070CrossRefGoogle Scholar
- Parker TG, Packer SE, Schneider MD (1990b) Peptide growth factors can provoke “fetal” contractile protein gene expression in rat cardiac myocytes. J Clin Invest 85(2):507–514. doi:10.1172/JCI114466CrossRefGoogle Scholar
- Passier R, Mummery C (2003) Origin and use of embryonic and adult stem cells in differentiation and tissue repair. Cardiovasc Res 58(2):324–335PubMedCrossRefGoogle Scholar
- Penn MS, Francis GS, Ellis SG, Young JB, McCarthy PM, Topol EJ (2002) Autologous cell transplantation for the treatment of damaged myocardium. Prog Cardiovasc Dis 45(1):21–32PubMedCrossRefGoogle Scholar
- Penn MS, Mangi AA (2008) Genetic enhancement of stem cell engraftment, survival, and efficacy. Circ Res 102(12):1471–1482. doi:102/12/1471 [pii] 10.1161/CIRCRESAHA.108.175174PubMedCentralPubMedCrossRefGoogle Scholar
- Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA (2011) Transient regenerative potential of the neonatal mouse heart. Science 331(6020):1078–1080. doi:331/6020/1078 [pii] 10.1126/science.1200708PubMedCentralPubMedCrossRefGoogle Scholar
- Pouly J, Bruneval P, Mandet C, Proksch S, Peyrard S, Amrein C, Bousseaux V, Guillemain R, Deloche A, Fabiani J-N, Menaschי P (2008) Cardiac stem cells in the real world. J Thorac Cardiovasc Surg 135(3):673–678PubMedCrossRefGoogle Scholar
- Quaini F, Urbanek K, Graiani G, Lagrasta C, Maestri R, Monica M, Boni A, Ferraro F, Delsignore R, Tasca G, Leri A, Kajstura J, Quaini E, Anversa P (2004) The regenerative potential of the human heart. Int J Cardiol 95(Suppl 1):S26–S28. doi:S0167527304900083 [pii]Google Scholar
- Rota M, Padin-Iruegas ME, Misao Y, De Angelis A, Maestroni S, Ferreira-Martins J, Fiumana E, Rastaldo R, Arcarese ML, Mitchell TS, Boni A, Bolli R, Urbanek K, Hosoda T, Anversa P, Leri A, Kajstura J (2008) Local activation or implantation of cardiac progenitor cells rescues scarred infarcted myocardium improving cardiac function. Circ Res 103(1):107–116. doi:CIRCRESAHA.108.178525 [pii] 10.1161/CIRCRESAHA.108.178525PubMedCentralPubMedCrossRefGoogle Scholar
- Ruvinov E, Leor J, Cohen S (2011) The promotion of myocardial repair by the sequential delivery of IGF-1 and HGF from an injectable alginate biomaterial in a model of acute myocardial infarction. Biomaterials 32(2):565–578. doi:10.1016/j.biomaterials.2010.08.097PubMedCrossRefGoogle Scholar
- Shneyvays V, Nawrath H, Jacobson KA, Shainberg A (1998) Induction of apoptosis in cardiac myocytes by an A3 adenosine receptor agonist. Exp Cell Res 243(2):383–397. doi:S0014-4827(98)94134-9 [pii] 10.1006/excr.1998.4134PubMedCrossRefGoogle Scholar
- Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR (2007) Thymosin beta-4 is essential for coronary vessel development and promotes neovascularization via adult epicardium. Ann N Y Acad Sci 1112:171–188. doi:annals.1415.000 [pii] 10.1196/annals.1415.000PubMedCrossRefGoogle Scholar
- Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marban E (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7):896–908. doi:10.1161/circulationaha.106.655209PubMedCrossRefGoogle Scholar
- Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisen J (2005) Retrospective birth dating of cells in humans. Cell 122(1):133–143. doi:10.1016/j.cell.2005.04.028PubMedCrossRefGoogle Scholar
- Sussman MA, Anversa P (2004) Myocardial aging and senescence: where have the stem cells gone? Ann Rev Physiol 66(1):29–48. doi:10.1146/annurev.physiol.66.032102.140723CrossRefGoogle Scholar
- Takehara N, Tsutsumi Y, Tateishi K, Ogata T, Tanaka H, Ueyama T, Takahashi T, Takamatsu T, Fukushima M, Komeda M, Yamagishi M, Yaku H, Tabata Y, Matsubara H, Oh H (2008) Controlled delivery of basic fibroblast growth factor promotes human cardiosphere-derived cell engraftment to enhance cardiac repair for chronic myocardial infarction. J Am Coll Cardiol 52(23):1858–1865PubMedCrossRefGoogle Scholar
- Tang XL, Rokosh G, Sanganalmath SK, Yuan F, Sato H, Mu J, Dai S, Li C, Chen N, Peng Y, Dawn B, Hunt G, Leri A, Kajstura J, Tiwari S, Shirk G, Anversa P, Bolli R (2010) Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 121(2):293–305. doi:CIRCULATIONAHA.109.871905 [pii] 10.1161/CIRCULATIONAHA.109.871905PubMedCentralPubMedCrossRefGoogle Scholar
- Urbanek K, Quaini F, Tasca G, Torella D, Castaldo C, Nadal-Ginard B, Leri A, Kajstura J, Quaini E, Anversa P (2003) From the cover: intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. PNAS 100(18):10440–10445. doi:10.1073/pnas.1832855100PubMedCentralPubMedCrossRefGoogle Scholar
- Urbanek K, Rota M, Cascapera S, Bearzi C, Nascimbene A, De Angelis A, Hosoda T, Chimenti S, Baker M, Limana F, Nurzynska D, Torella D, Rotatori F, Rastaldo R, Musso E, Quaini F, Leri A, Kajstura J, Anversa P (2005a) Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res 97(7):663–673. doi:10.1161/01.res.0000183733.53101.11CrossRefGoogle Scholar
- Urbanek K, Torella D, Sheikh F, De Angelis A, Nurzynska D, Silvestri F, Beltrami CA, Bussani R, Beltrami AP, Quaini F, Bolli R, Leri A, Kajstura J, Anversa P (2005b) Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. PNAS 102(24):8692–8697. doi:10.1073/pnas.0500169102CrossRefGoogle Scholar
- Zaruba MM, Soonpaa M, Reuter S, Field LJ (2010) Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 121(18):1992–2000. doi:10.1161/CIRCULATIONAHA.109.909093PubMedCentralPubMedCrossRefGoogle Scholar
- Zhou YY, Wang SQ, Zhu WZ, Chruscinski A, Kobilka BK, Ziman B, Wang S, Lakatta EG, Cheng H, Xiao RP (2000) Culture and adenoviral infection of adult mouse cardiac myocytes: methods for cellular genetic physiology. Am J Physiol Heart Circ Physiol 279(1):H429–H436Google Scholar
- Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, Pu WT (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454(7200):109–113. doi:nature07060 [pii] 10.1038/nature07060PubMedCentralPubMedCrossRefGoogle Scholar
- Zimmet H, Krum H (2008) Using adult stem cells to treat heart failure-fact or fiction? Heart Lung Circ 17(Suppl 4):S48–S54PubMedCrossRefGoogle Scholar