Cardiac stem cell biology: Glimpse of the past, present, and future

Circulation Research

Volumn 114, Issue 1, 2014, Pages 21-27

  Matsa, Elena ^a   Sallam, Karim ^a   Wu, Joseph C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE   (United States)

Author keywords

adult stem cells; embryonic stem cells; induced pluripotent stem cells

Indexed keywords

ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM CHANNEL BLOCKING AGENT; CD34 ANTIGEN;

ADULT STEM CELL; ARTICLE; CARDIAC REGENERATION; CARDIAC STEM CELL; CELL POPULATION; CELL THERAPY; CELL TRANSDIFFERENTIATION; CELL VIABILITY; DRUG SCREENING; EMBRYONIC STEM CELL; EX VIVO STUDY; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE; HEART VENTRICLE FUNCTION; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; ISCHEMIC CARDIOMYOPATHY; ISCHEMIC HEART DISEASE; MONONUCLEAR CELL; MULTIPOTENT STEM CELL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); STEM CELL; THERAPY EFFECT; TISSUE REPAIR;

EID: 84892930341     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.302895     Document Type: Article

References (73)

1. Laslett LJ, Alagona P, Clark BA, Drozda JP, Saldivar F, Wilson SR, Poe C, Hart M. The worldwide environment of cardiovascular disease: Prevalence, diagnosis, therapy, and policy issuesa report from the American College of Cardiology. J Am Coll Cardiol. 2012;60:S1-S49.
2. Milan DJ, MacRae CA. Animal models for arrhythmias. Cardiovasc Res. 2005;67:426-437.
3. Rajamohan D, Matsa E, Kalra S, Crutchley J, Patel A, George V, Denning C. Current status of drug screening and disease modelling in human plu-ripotent stem cells. Bioessays. 2013;35:281-298.
4. Anversa P, Kajstura J. Ventricular myocytes are not terminally differentiated in the adult mammalian heart. Circ Res. 1998;83:1-14.
5. D'Amario D, Fiorini C, Campbell PM, et al. Functionally competent cardiac stem cells can be isolated from endomyocardial biopsies of patients with advanced cardiomyopathies. Circ Res. 2011;108:857-861.
6. Rota M, Padin-Iruegas ME, Misao Y, et al. Local activation or implantation of cardiac progenitor cells rescues scarred infarcted myocardium improving cardiac function. Circ Res. 2008;103:107-116.
7. Bolli R, Chugh AR, D'Amario D, et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet. 2011;378:1847-1857.
8. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res. 2004;95:911-921.
9. Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marbán L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marbán E. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet. 2012;379:895-904.
10. Dey D, Han L, Bauer M, Sanada F, Oikonomopoulos A, Hosoda T, Unno K, De Almeida P, Leri A, Wu JC. Dissecting the molecular relationship among various cardiogenic progenitor cells. Circ Res. 2013;112:1253-1262.
11. Kucia M, Dawn B, Hunt G, Guo Y, Wysoczynski M, Majka M, Ratajczak J, Rezzoug F, Ildstad ST, Bolli R, Ratajczak MZ. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res. 2004;95:1191-1199.
12. Sheikh AY, Lin SA, Cao F, Cao Y, van der Bogt KE, Chu P, Chang CP, Contag CH, Robbins RC, Wu JC. Molecular imaging of bone marrow mononuclear cell homing and engraftment in ischemic myocardium. Stem Cells. 2007;25:2677-2684.
13. Sanganalmath SK, Bolli R. Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res. 2013;113:810-834.
14. Assmus B, Fischer-Rasokat U, Honold J, Seeger FH, Fichtlscherer S, Tonn T, Seifried E, Schächinger V, Dimmeler S, Zeiher AM; TOPCARE-CHD Registry. Transcoronary transplantation of functionally competent BMCs is associated with a decrease in natriuretic peptide serum levels and improved survival of patients with chronic postinfarction heart failure: results of the TOPCARE-CHD Registry. Circ Res. 2007;100:1234-1241.
15. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204-1219.
16. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res. 2004;95:9-20.
17. Suzuki G, Iyer V, Lee TC, Canty JM Jr. Autologous mesenchymal stem cells mobilize cKit+ and CD133+ bone marrow progenitor cells and improve regional function in hibernating myocardium. Circ Res. 2011;109:1044-1054.
18. Houtgraaf JH, de Jong R, Kazemi K, de Groot D, van der Spoel TI, Arslan F, Hoefer I, Pasterkamp G, Itescu S, Zijlstra F, Geleijnse ML, Serruys PW, Duckers HJ. Intracoronary infusion of allogeneic mesenchymal precursor cells directly after experimental acute myocardial infarction reduces infarct size, abrogates adverse remodeling, and improves cardiac function. Circ Res. 2013;113:153-166.
19. Williams AR, Trachtenberg B, Velazquez DL, McNiece I, Altman P, Rouy D, Mendizabal AM, Pattany PM, Lopera GA, Fishman J, Zambrano JP, Heldman AW, Hare JM. Intramyocardial stem cell injection in patients with ischemic cardiomyopathy: functional recovery and reverse remodeling. Circ Res. 2011;108:792-796.
20. Hare JM, Fishman JE, Gerstenblith G, et al. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA. 2012;308:2369-2379.
21. Reinecke H, Minami E, Zhu WZ, Lafamme MA. Cardiogenic differentiation and transdifferentiation of progenitor cells. Circ Res. 2008;103:1058-1071.
22. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, Dimmeler S. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation. 2001;103:2885-2890.
23. Wang J, Zhang S, Rabinovich B, Bidaut L, Soghomonyan S, Alauddin MM, Bankson JA, Shpall E, Willerson JT, Gelovani JG, Yeh ET. Human CD34+ cells in experimental myocardial infarction: long-term survival, sustained functional improvement, and mechanism of action. Circ Res. 2010;106:1904-1911.
24. Losordo DW, Henry TD, Davidson C, et al; ACT34-CMI Investigators. Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ Res. 2011;109:428-436.
25. Sahoo S, Klychko E, Thorne T, Misener S, Schultz KM, Millay M, Ito A, Liu T, Kamide C, Agrawal H, Perlman H, Qin G, Kishore R, Losordo DW. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res. 2011;109:724-728.
26. Vrtovec B, Poglajen G, Lezaic L, Sever M, Domanovic D, Cernelc P, Socan A, Schrepfer S, Torre-Amione G, Haddad F, Wu JC. Effects of in-tracoronary CD34+ stem cell transplantation in nonischemic dilated car-diomyopathy patients: 5-year follow-up. Circ Res. 2013;112:165-173.
27. Planat-Bénard V, Menard C, André M, Puceat M, Perez A, Garcia-Verdugo JM, Pénicaud L, Casteilla L. Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res. 2004;94:223-229.
28. Menasché P, Hagège AA, Scorsin M, Pouzet B, Desnos M, Duboc D, Schwartz K, Vilquin J-T, Marolleau J-P. Myoblast transplantation for heart failure. The Lancet. 2001;357:279-280.
29. Müller-Ehmsen J, Whittaker P, Kloner RA, Dow JS, Sakoda T, Long TI, Laird PW, Kedes L. Survival and development of neonatal rat car-diomyocytes transplanted into adult myocardium. J Mol Cell Cardiol. 2002;34:107-116.
30. Fujii T, Yau TM, Weisel RD, Ohno N, Mickle DA, Shiono N, Ozawa T, Matsubayashi K, Li RK. Cell transplantation to prevent heart failure: a comparison of cell types. Ann Thorac Surg. 2003;76:2062-2070.
31. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D. Direct reprogramming of fbroblasts into functional cardio-myocytes by defned factors. Cell. 2010;142:375-386.
32. Qian L, Huang Y, Spencer CI, Foley A, Vedantham V, Liu L, Conway SJ, Fu JD, Srivastava D. In vivo reprogramming of murine cardiac fbroblasts into induced cardiomyocytes. Nature. 2012;485:593-598.
33. Chen JX, Krane M, Deutsch MA, Wang L, Rav-Acha M, Gregoire S, Engels MC, Rajarajan K, Karra R, Abel ED, Wu JC, Milan D, Wu SM. Ineffcient reprogramming of fbroblasts into cardiomyocytes using Gata4, Mef2c, and Tbx5. Circ Res. 2012;111:50-55.
34. Fu J-D, Stone Nicole R, Liu L, Spencer CI, Qian L, Hayashi Y, Delgado-Olguin P, Ding S, Bruneau Benoit G, Srivastava D. Direct repro-gramming of human fbroblasts toward a cardiomyocyte-like state. Stem Cell Reports. 2013;1:235-247.
35. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154-156.
36. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145-1147.
37. Burridge PW, Keller G, Gold JD, Wu JC. Production of de novo cardio-myocytes: human pluripotent stem cell differentiation and direct repro-gramming. Cell Stem Cell. 2012;10:16-28.
38. Xu C, Police S, Rao N, Carpenter MK. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res. 2002;91:501-508.
39. Burridge PW, Thompson S, Millrod MA, Weinberg S, Yuan X, Peters A, Mahairaki V, Koliatsos VE, Tung L, Zambidis ET. A universal system for highly effcient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One. 2011;6:e18293.
40. Zhang J, Klos M, Wilson GF, et al. Extracellular matrix promotes highly effcient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ Res. 2012;111:1125-1136.
41. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fbro-blasts by defned factors. Cell. 2007;131:861-872.
42. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997;385:810-813.
43. Matsa E, Denning C. In vitro uses of human pluripotent stem cell-derived cardiomyocytes. J Cardiovasc Transl Res. 2012;5:581-592.
44. Simpson P, Savion S. Differentiation of rat myocytes in single cell cultures with and without proliferating nonmyocardial cells. Cross-striations, ultrastructure, and chronotropic response to isoproterenol. Circ Res. 1982;50:101-116.
45. Maltsev VA, Wobus AM, Rohwedel J, Bader M, Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells devel-opmentally express cardiac-specifc genes and ionic currents. Circ Res. 1994;75:233-244.
46. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003;93:32-39.
47. Narsinh K, Narsinh KH, Wu JC. Derivation of human induced plu-ripotent stem cells for cardiovascular disease modeling. Circ Res. 2011;108:1146-1156.
48. Matsa E, Rajamohan D, Dick E, Young L, Mellor I, Staniforth A, Denning C. Drug evaluation in cardiomyocytes derived from human induced plurip-otent stem cells carrying a long QT syndrome type 2 mutation. Eur Heart J. 2011;32:952-962.
49. Liang P, Lan F, Lee AS, Gong T, Sanchez-Freire V, Wang Y, Diecke S, Sallam K, Knowles JW, Wang PJ, Nguyen PK, Bers DM, Robbins RC, Wu JC. Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specifc patterns of cardiotox-icity. Circulation. 2013;127:1677-1691.
50. Navarrete EG, Liang P, Lan F, et al. Screening drug-induced arrhythmia events using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays Circulation. 2013;128:S3-S13
51. Engle SJ, Puppala D. Integrating human pluripotent stem cells into drug development. Cell Stem Cell. 2013;12:669-677.
52. Mordwinkin NM, Lee AS, Wu JC. Patient-specifc stem cells and cardiovascular drug discovery. JAMA. 2013;310:2039-2040.
53. Lan F, Lee AS, Liang P, et al. Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specifc induced pluripotent stem cells. Cell Stem Cell. 2013;12:101-113.
54. Sun N, Yazawa M, Liu J, et al. Patient-specifc induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci Transl Med. 2012;4:130ra47.
55. Moretti A, Bellin M, Welling A, Jung CB, Lam JT, Bott-Flügel L, Dorn T, Goedel A, Höhnke C, Hofmann F, Seyfarth M, Sinnecker D, Schömig A, Laugwitz KL. Patient-specifc induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med. 2010;363:1397-1409.
56. Carvajal-Vergara X, Sevilla A, D'Souza SL, et al. Patient-specifc induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature. 2010;465:808-812.
57. Kim C, Wong J, Wen J, Wang S, Wang C, Spiering S, Kan NG, Forcales S, Puri PL, Leone TC, Marine JE, Calkins H, Kelly DP, Judge DP, Chen HS. Studying arrhythmogenic right ventricular dysplasia with patient-specifc iPSCs. Nature. 2013;494:105-110.
58. Matsa E, Dixon JE, Medway C, Georgiou O, Patel MJ, Morgan K, Kemp PJ, Staniforth A, Mellor I, Denning C. Allele-specifc rna interference rescues the long-qt syndrome phenotype in human-induced pluripotency stem cell cardiomyocytes. Eur Heart J. March 6, 2013. doi: 10.1093/eurheartj/eht067. http://eurheartj.oxfordjournals.org/content/early/2013/03/06/eur-heartj.eht067. long. Accessed December 18, 2013.
59. Caspi O, Huber I, Kehat I, Habib M, Arbel G, Gepstein A, Yankelson L, Aronson D, Beyar R, Gepstein L. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J Am Coll Cardiol. 2007;50:1884-1893.
60. Shiba Y, Fernandes S, Zhu WZ, et al. Human ES-cell-derived cardio-myocytes electrically couple and suppress arrhythmias in injured hearts. Nature. 2012;489:322-325.
61. Lee AS, Tang C, Rao MS, Weissman IL, Wu JC. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med. 2013;19:998-1004.
62. Tang C, Lee AS, Volkmer JP, Sahoo D, Nag D, Mosley AR, Inlay MA, Ardehali R, Chavez SL, Pera RR, Behr B, Wu JC, Weissman IL, Drukker M. An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat Biotechnol. 2011;29:829-834.
63. de Almeida PE, Ransohoff JD, Nahid A, Wu JC. Immunogenicity of plu-ripotent stem cells and their derivatives. Circ Res. 2013;112:549-561.
64. Pearl JI, Lee AS, Leveson-Gower DB, Sun N, Ghosh Z, Lan F, Ransohoff J, Negrin RS, Davis MM, Wu JC. Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell. 2011;8:309-317.
65. Hu S, Huang M, Nguyen PK, Gong Y, Li Z, Jia F, Lan F, Liu J, Nag D, Robbins RC, Wu JC. Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation. 2011;124:S27-S34.
66. Tulloch NL, Muskheli V, Razumova MV, Korte FS, Regnier M, Hauch KD, Pabon L, Reinecke H, Murry CE. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ Res. 2011;109:47-59.
67. Zimmermann WH, Schneiderbanger K, Schubert P, Didié M, Münzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T. Tissue engineering of a differentiated cardiac muscle construct. Circ Res. 2002;90:223-230.
68. Swijnenburg R-J, Govaert JA, van der Bogt KEA, Pearl JI, Huang M, Stein W, Hoyt G, Vogel H, Contag CH, Robbins RC, Wu JC. Timing of bone marrow cell delivery has minimal effects on cell viability and cardiac recovery after myocardial infarction. Circ Cardiovasc Imaging. 2010;3:77-85.
69. Vrtovec B, Poglajen G, Lezaic L, Sever M, Socan A, Domanovic D, Cernelc P, Torre-Amione G, Haddad F, Wu JC. Comparison of transen-docardial and intracoronary CD34+ cell transplantation in patients with nonischemic dilated cardiomyopathy. Circulation. 2013;128:S42-S49.
70. Nguyen PK, Lan F, Wang Y, Wu JC. Imaging: guiding the clinical translation of cardiac stem cell therapy. Circ Res. 2011;109:962-979.
71. Cao F, Wagner RA, Wilson KD, Xie X, Fu JD, Drukker M, Lee A, Li RA, Gambhir SS, Weissman IL, Robbins RC, Wu JC. Transcriptional and functional profling of human embryonic stem cell-derived cardiomyocytes. PLoS One. 2008;3:e3474.
72. Churko JM, Mantalas GL, Snyder MP, Wu JC. Overview of high throughput sequencing technologies to elucidate molecular pathways in cardiovascular diseases. Circ Res. 2013;112:1613-1623.
73. Sanchez-Freire V, Ebert AD, Kalisky T, Quake SR, Wu JC. Microfuidic single-cell real-time PCR for comparative analysis of gene expression patterns. Nat Protocols. 2012;7:829-838.