Repeated Administrations of Cardiac Progenitor Cells Are Markedly More Effective Than a Single Administration: A New Paradigm in Cell Therapy

Circulation Research

Volumn 119, Issue 5, 2016, Pages 635-651

  Tokita, Yukichi ^a   Tang, Xian Liang ^a   Li, Qianhong ^a   Wysoczynski, Marcin ^a   Hong, Kyung U ^a   Nakamura, Shunichi ^a   Wu, Wen Jian ^a   Xie, Wei ^a   Li, Ding ^a   Hunt, Greg ^a   Ou, Qinghui ^a   Stowers, Heather ^a   Bolli, Roberto ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

cardiac progenitor cells; cell therapy; collagen; left ventricular function; myocardial infarction; reperfusion injury; ventricular remodeling

Indexed keywords

COLLAGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC STEM CELL; CELL DENSITY; CONTROLLED STUDY; FEMALE; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RAT MODEL; STEM CELL TRANSPLANTATION; THERAPY EFFECT; ANIMAL; BIOLOGICAL THERAPY; CARDIAC MUSCLE CELL; CELL SURVIVAL; FISCHER 344 RAT; MALE; MYOCARDIAL INFARCTION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; STEM CELL; TRENDS;

ANIMALS; CELL SURVIVAL; CELL- AND TISSUE-BASED THERAPY; FEMALE; MALE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; RATS, INBRED F344; STEM CELL TRANSPLANTATION; STEM CELLS; VENTRICULAR FUNCTION, LEFT;

EID: 84978120379     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.308937     Document Type: Article

References (46)

1. Keith MC, Bolli R, "String theory" of c-kit(pos) cardiac cells: a new paradigm regarding the nature of these cells that may reconcile apparently discrepant results. Circ Res 2015 116 1216 1230. doi: 10.1161/CIRCRESAHA.116.305557
2. 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. doi: 10.1161/CIRCRESAHA.113.300219
3. Dawn B, Stein AB, Urbanek K, Cardiac stem cells delivered intravascularly traverse the vessel barrier, regenerate infarcted myocardium, and improve cardiac function. Proc Natl Acad Sci USA 2005 102 3766 3771. doi: 10.1073/pnas.0405957102
4. -POS cardiac progenitor cells after acute myocardial infarction: transplanted cells do not become cardiomyocytes, but structural and functional improvement and proliferation of endogenous cells persist for at least one year. Circ Res 2016 118 1091 1105. doi: 10.1161/CIRCRESAHA.115.307647
5. Tang XL, Rokosh G, Sanganalmath SK, Tokita Y, Keith MC, Shirk G, Stowers H, Hunt GN, Wu W, Dawn B, Bolli R, Effects of intracoronary infusion of escalating doses of cardiac stem cells in rats with acute myocardial infarction. Circ Heart Fail 2015 8 757 765. doi: 10.1161/CIRCHEARTFAILURE.115.002210
6. Tang XL, Rokosh G, Sanganalmath SK, Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation 2010 121 293 305. doi: 10.1161/CIRCULATIONAHA.109.871905
7. Li Q, Guo Y, Ou Q, Chen N, Wu WJ, Yuan F, O'Brien E, Wang T, Luo L, Hunt GN, Zhu X, Bolli R, Intracoronary administration of cardiac stem cells in mice: a new, improved technique for cell therapy in murine models. Basic Res Cardiol 2011 106 849 864. doi: 10.1007/s00395-011-0180-1
8. Williams AR, Hatzistergos KE, Addicott B, McCall F, Carvalho D, Suncion V, Morales AR, Da Silva J, Sussman MA, Heldman AW, Hare JM, Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation 2013 127 213 223. doi: 10.1161/CIRCULATIONAHA.112.131110
9. Oskouei BN, Lamirault G, Joseph C, Treuer AV, Landa S, Da Silva J, Hatzistergos K, Dauer M, Balkan W, McNiece I, Hare JM, Increased potency of cardiac stem cells compared with bone marrow mesenchymal stem cells in cardiac repair. Stem Cells Transl Med 2012 1 116 124. doi: 10.5966/sctm.2011-0015
10. Fischer KM, Cottage CT, Wu W, Din S, Gude NA, Avitabile D, Quijada P, Collins BL, Fransioli J, Sussman MA, Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 2009 120 2077 2087. doi: 10.1161/CIRCULATIONAHA.109.884403
11. Duran JM, Makarewich CA, Sharp TE, Starosta T, Zhu F, Hoffman NE, Chiba Y, Madesh M, Berretta RM, Kubo H, Houser SR, Bone-derived stem cells repair the heart after myocardial infarction through transdifferentiation and paracrine signaling mechanisms. Circ Res 2013 113 539 552. doi: 10.1161/CIRCRESAHA.113.301202
12. Zaruba MM, Soonpaa M, Reuter S, Field LJ, Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 2010 121 1992 2000. doi: 10.1161/CIRCULATIONAHA.109.909093
13. Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT, Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 2007 13 970 974. doi: 10.1038/nm1618
14. Laflamme MA, Murry CE, Regenerating the heart. Nat Biotechnol 2005 23 845 856. doi: 10.1038/nbt1117
15. Parmacek MS, Epstein JA, Pursuing cardiac progenitors: regeneration redux. Cell 2005 120 295 298. doi: 10.1016/j.cell.2005.01.025
16. Gerbin KA, Murry CE, The winding road to regenerating the human heart. Cardiovasc Pathol 2015 24 133 140. doi: 10.1016/j.carpath.2015.02.004
17. Hong KU, Guo Y, Li QH, Cao P, Al-Maqtari T, Vajravelu BN, Du J, Book MJ, Zhu X, Nong Y, Bhatnagar A, Bolli R, c-kit+ Cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PLoS One 2014 9 e96725. doi: 10.1371/journal.pone.0096725
18. Hong KU, Li QH, Guo Y, Patton NS, Moktar A, Bhatnagar A, Bolli R, A highly sensitive and accurate method to quantify absolute numbers of c-kit+ cardiac stem cells following transplantation in mice. Basic Res Cardiol 2013 108 346. doi: 10.1007/s00395-013-0346-0
19. Bolli R, Tang XL, Sanganalmath SK, Rimoldi O, Mosna F, Abdel-Latif A, Jneid H, Rota M, Leri A, Kajstura J, Intracoronary delivery of autologous cardiac stem cells improves cardiac function in a porcine model of chronic ischemic cardiomyopathy. Circulation 2013 128 122 131. doi: 10.1161/CIRCULATIONAHA.112.001075
20. Keith MC, Tang XL, Tokita Y, Safety of intracoronary infusion of 20 million C-kit positive human cardiac stem cells in pigs. PLoS One 2015 10 e0124227. doi: 10.1371/journal.pone.0124227
21. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H, Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005 111 2198 2202. doi: 10.1161/01.CIR.0000163546.27639.AA
22. Blocklet D, Toungouz M, Berkenboom G, Lambermont M, Unger P, Preumont N, Stoupel E, Egrise D, Degaute JP, Goldman M, Goldman S, Myocardial homing of nonmobilized peripheral-blood CD34+ cells after intracoronary injection. Stem Cells 2006 24 333 336. doi: 10.1634/stemcells.2005-0201
23. Aicher A, Brenner W, Zuhayra M, Badorff C, Massoudi S, Assmus B, Eckey T, Henze E, Zeiher AM, Dimmeler S, Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation 2003 107 2134 2139. doi: 10.1161/01.CIR.0000062649.63838.C9
24. Yu J, Du KT, Fang Q, Gu Y, Mihardja SS, Sievers RE, Wu JC, Lee RJ, The use of human mesenchymal stem cells encapsulated in RGD modified alginate microspheres in the repair of myocardial infarction in the rat. Biomaterials 2010 31 7012 7020. doi: 10.1016/j.biomaterials.2010.05.078
25. Hou D, Youssef EA, Brinton TJ, Zhang P, Rogers P, Price ET, Yeung AC, Johnstone BH, Yock PG, March KL, Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 2005 112 I150 I156. doi: 10.1161/CIRCULATIONAHA.104.526749
26. Panda NC, Zuckerman ST, Mesubi OO, Rosenbaum DS, Penn MS, Donahue JK, Alsberg E, Laurita KR, Improved conduction and increased cell retention in healed MI using mesenchymal stem cells suspended in alginate hydrogel. J Interv Card Electrophysiol 2014 41 117 127. doi: 10.1007/s10840-014-9940-9
27. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, Miller L, Guetta E, Zipori D, Kedes LH, Kloner RA, Leor J, Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 2003 108 863 868. doi: 10.1161/01.CIR.0000084828.50310.6A
28. Al Kindi A, Ge Y, Shum-Tim D, Chiu RC, Cellular cardiomyoplasty: routes of cell delivery and retention. Front Biosci 2008 13 2421 2434
29. Terrovitis J, Lautamäki R, Bonios M, Fox J, Engles JM, Yu J, Leppo MK, Pomper MG, Wahl RL, Seidel J, Tsui BM, Bengel FM, Abraham MR, Marbán E, Noninvasive quantification and optimization of acute cell retention by in vivo positron emission tomography after intramyocardial cardiac-derived stem cell delivery. J Am Coll Cardiol 2009 54 1619 1626. doi: 10.1016/j.jacc.2009.04.097
30. Robey TE, Saiget MK, Reinecke H, Murry CE, Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 2008 45 567 581. doi: 10.1016/j.yjmcc.2008.03.009
31. Cheng K, Li TS, Malliaras K, Davis DR, Zhang Y, Marbán E, Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction. Circ Res 2010 106 1570 1581. doi: 10.1161/CIRCRESAHA.109.212589
32. Yao K, Huang R, Sun A, Qian J, Liu X, Ge L, Zhang Y, Zhang S, Niu Y, Wang Q, Zou Y, Ge J, Repeated autologous bone marrow mononuclear cell therapy in patients with large myocardial infarction. Eur J Heart Fail 2009 11 691 698. doi: 10.1093/eurjhf/hfp062
33. Zhang Y, Sievers RE, Prasad M, Mirsky R, Shih H, Wong ML, Angeli FS, Ye J, Takagawa J, Koskenvuo JW, Springer ML, Grossman W, Boyle AJ, Yeghiazarians Y, Timing of bone marrow cell therapy is more important than repeated injections after myocardial infarction. Cardiovasc Pathol 2011 20 204 212. doi: 10.1016/j.carpath.2010.06.007
34. Gavira JJ, Nasarre E, Abizanda G, Pérez-Ilzarbe M, de Martino-Rodriguez A, García de Jalón JA, Mazo M, Macias A, García-Bolao I, Pelacho B, Martínez-Caro D, Prósper F, Repeated implantation of skeletal myoblast in a swine model of chronic myocardial infarction. Eur Heart J 2010 31 1013 1021. doi: 10.1093/eurheartj/ehp342
35. Premaratne GU, Tambara K, Fujita M, Lin X, Kanemitsu N, Tomita S, Sakaguchi G, Nakajima H, Ikeda T, Komeda M, Repeated implantation is a more effective cell delivery method in skeletal myoblast transplantation for rat myocardial infarction. Circ J 2006 70 1184 1189
36. Mann I, Rodrigo SF, van Ramshorst J, Beeres SL, Dibbets-Schneider P, de Roos A, Wolterbeek R, Zwaginga JJ, Fibbe WE, Bax JJ, Schalij MJ, Atsma DE, Repeated intramyocardial bone marrow cell Injection in previously responding patients with refractory angina again improves myocardial perfusion, anginal complaints, and quality of life. Circ Cardiovasc Interv 2015 8 e002740. doi: 10.1161/CIRCINTERVENTIONS.115.002740
37. Siegel G, Kluba T, Hermanutz-Klein U, Bieback K, Northoff H, Schäfer R, Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Med 2013 11 146. doi: 10.1186/1741-7015-11-146
38. Ernst C, Christie BR, Isolectin-IB 4 as a vascular stain for the study of adult neurogenesis. J Neurosci Methods 2006 150 138 142. doi: 10.1016/j.jneumeth.2005.06.018
39. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ, Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001 105 369 377
40. Tang XL, Qiu Y, Park SW, Sun JZ, Kalya A, Bolli R, Time course of late preconditioning against myocardial stunning in conscious pigs. Circ Res 1996 79 424 434
41. Li XY, McCay PB, Zughaib M, Jeroudi MO, Triana JF, Bolli R, Demonstration of free radical generation in the "stunned" myocardium in the conscious dog and identification of major differences between conscious and open-chest dogs. J Clin Invest 1993 92 1025 1041. doi: 10.1172/JCI116608
42. Bolli R, Zughaib M, Li XY, Tang XL, Sun JZ, Triana JF, McCay PB, Recurrent ischemia in the canine heart causes recurrent bursts of free radical production that have a cumulative effect on contractile function. A pathophysiological basis for chronic myocardial "stunning". J Clin Invest 1995 96 1066 1084. doi: 10.1172/JCI118093
43. Sutton MG, Sharpe N, Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 2000 101 2981 2988
44. Rejman J, Colombo C, Conese M, Engraftment of bone marrow-derived stem cells to the lung in a model of acute respiratory infection by Pseudomonas aeruginosa. Mol Ther 2009 17 1257 1265. doi: 10.1038/mt.2009.96
45. Durnam DM, Anders KR, Fisher L, O'Quigley J, Bryant EM, Thomas ED, Analysis of the origin of marrow cells in bone marrow transplant recipients using a Y-chromosome-specific in situ hybridization assay. Blood 1989 74 2220 2226
46. Mellough CB, Cui Q, Spalding KL, Symons NA, Pollett MA, Snyder EY, Macklis JD, Harvey AR, Fate of multipotent neural precursor cells transplanted into mouse retina selectively depleted of retinal ganglion cells. Exp Neurol 2004 186 6 19. doi: 10.1016/j.expneurol.2003.10.021