Safety and efficacy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells

Circulation

Volumn 125, Issue 1, 2012, Pages 100-112

  Malliaras, Konstantinos ^a   Li, Tao Sheng ^a   Luthringer, Daniel ^a   Terrovitis, John ^a   Cheng, Ke ^a   Chakravarty, Tarun ^a   Galang, Giselle ^a   Zhang, Yiqiang ^a   Schoenhoff, Florian ^b   Van Eyk, Jennifer ^b   Marbán, Linda ^a   Marbán, Eduardo ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

allogeneic transplantation; paracrine communication; regeneration; stem cells

Indexed keywords

CD45 ANTIGEN; ENDOGLIN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SCATTER FACTOR; SOMATOMEDIN C; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ALLOTRANSPLANTATION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CARDIOSPHERE DERIVED CELL TRANSPLANTATION; CELL TRANSPLANTATION; CELLULAR IMMUNITY; CLINICAL EFFECTIVENESS; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INTERMETHOD COMPARISON; ISOGRAFT; LYMPHOCYTE PROLIFERATION; MALE; MIXED LYMPHOCYTE CULTURE; NONHUMAN; PATIENT SAFETY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SURVIVAL RATE; TISSUE REGENERATION; TISSUE STRUCTURE; TRANSPLANTATION TOLERANCE;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; FEMALE; GRAFT SURVIVAL; HUMANS; MALE; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; RATS, INBRED BN; RATS, INBRED WKY; SPHEROIDS, CELLULAR; TRANSPLANTATION, HOMOLOGOUS; TREATMENT OUTCOME;

EID: 84855370658     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.042598     Document Type: Article

References (42)

1. Wollert KC, Drexler H. Cell therapy for the treatment of coronary heart disease: a critical appraisal. Nat Rev Cardiol. 2010;7:204-215.
2. Malliaras K, Marbán E. Cardiac cell therapy: where we've been, where we are, and where we should be headed. Br Med Bull. 2011;98:161-185.
3. CADUCEUS. CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction (NCT00893360). www.clinicaltrials.gov. Accessed November 17, 2011.
4. Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res. 2008;102:1319-1330.
5. Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, Marbán E. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 2010;106:971-980.
6. 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. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation. 2010;121:293-305.
7. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marbán E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007;115:896-908. (Pubitemid 46294730)
8. Davis DR, Zhang Y, Smith RR, Cheng K, Terrovitis J, Malliaras K, Li TS, White A, Makkar R, Marbán E. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One. 2009;4:e7195.
9. 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.
10. Ruggeri L, Capanni M, Martelli MF, Velardi A. Cellular therapy: exploiting NK cell alloreactivity in transplantation. Curr Opin Hematol. 2001;8:355-359. (Pubitemid 33032916)
11. Atoui R, Shum-Tim D, Chiu RC. Myocardial regenerative therapy: immunologic basis for the potential universal donor cells. Ann Thorac Surg. 2008;86:327-334.
12. Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, Schär M, Gerstenblith G, Weiss RG, Marbán E, Abraham MR. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation. 2008;117:1555-1562. (Pubitemid 351444664)
13. Kreisel D, Krupnick AS, Gelman AE, Engels FH, Popma SH, Krasinskas AM, Balsara KR, Szeto WY, Turka LA, Rosengard BR. Nonhematopoietic allograft cells directly activate CD8- T cells and trigger acute rejection: an alternative mechanism of allorecognition. Nat Med. 2002;8:233-239. (Pubitemid 34250100)
14. Poncelet AJ, Vercruysse J, Saliez A, Gianello P. Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro, intracardiac injection elicits an immune response in vivo. Transplantation. 2007;83: 783-790. (Pubitemid 46569198)
15. Davis DR, Ruckdeschel Smith R, Marbán E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells. 2010;28: 903-904.
16. Bersell K, Arab S, Haring B, Kühn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell. 2009;138:257-270.
17. Loffredo FS, Steinhauser ML, Gannon J, Lee RT. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell. 2011;8:389-398.
18. 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. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res. 2010;107:913-922.
19. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Tsutsumi Y, Ozono R, Masaki H, Mori Y, Iba O, Tateishi E, Kosaki A, Shintani S, Murohara T, Imaizumi T, Iwasaka T. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation. 2001;104:1046-1052. (Pubitemid 32803883)
20. Cho HJ, Lee N, Lee JY, Choi YJ, Ii M, Wecker A, Jeong JO, Curry C, Qin G, Yoon YS. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med. 2007;204:3257-3269.
21. Li TS, Cheng K, Lee ST, Matsushita S, Davis D, Malliaras K, Zhang Y, Matsushita N, Smith RR, Marbán E. Cardiospheres recapitulate a niche-like microenvironment rich in stemness and cell-matrix interactions, rationalizing their enhanced functional potency for myocardial repair. Stem Cells. 2010;28:2088-2098.
22. Davis DR, Kizana E, Terrovitis, Barth AS, Zhang Y, Smith RR, Miake J, Marbán E. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol. 2010; 49:312-321.
23. Terrovitis J, Lautamäki R, Bonios, 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.
24. Lee ST, White AJ, Matsushita, Malliaras K, Steenbergen C, Zhang Y, Li TS, Terrovitis J, Yee K, Simsir S, Makkar R, Marbán E. Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure post-myocardial infarction. J Am Coll Cardiol. 2011; 57:455-465.
25. Johnston PV, Sasano T, Mills, Evers R, Lee ST, Smith RR, Lardo AC, Lai S, Steenbergen C, Gerstenblith G, Lange R, Marbán E. Engraftment, differentiation, and functional benefits of autologous cardiospherederived cells in porcine ischemic cardiomyopathy. Circulation. 2009;120: 1075-1083.
26. Aghila Rani KG, Kartha CC. Effects of epidermal growth factor on proliferation and migration of cardiosphere-derived cells expanded from adult human heart. Growth Factors. 2010;28:157-165.
27. Gaetani R, Ledda M, Barile L, Chimenti I, De Carlo F, Forte E, Ionta V, Giuliani L, D'Emilia E, Frati G, Miraldi F, Pozzi D, Messina E, Grimaldi S, Giacomello A, Lisi A. Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc Res. 2009;82:411-420.
28. Mishra R, Vijayan K, Colletti E, Harrington DA, Matthiesen TS, Simpson D, Goh SK, Walker BL, Almeida-Porada G, Wang D, Backer CL, Dudley SC Jr, Wold LE, Kaushal S. Characterization and functionality of cardiac progenitor cells in congenital heart patients. Circulation. 2011;123: 364-373.
29. Takehara N, Tsutsumi Y, Tateishi, Ogata T, Tanaka H, Ueyama T, Takahashi T, Takamatsu T, Fukushima M, Komeda M, Yamagishi M, Yaku H, Tabata Y, Matsubara H, Oh H. 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. 2008;52:1858-1865.
30. Tang YL, Zhu W, Cheng, Chen L, Zhang J, Sun T, Kishore R, Phillips MI, Losordo DW, Qin G. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ Res. 2009;104:1209-1216.
31. Zakharova L, Mastroeni D, Mutlu N, Molina M, Goldman S, Diethrich E, Gaballa MA. Transplantation of cardiac progenitor cell sheet onto infarcted heart promotes cardiogenesis and improves function. Cardiovasc Res. 2010;87:40-49.
32. Koninckx R, Daniëls A, Windmolders S, Carlotti F, Mees U, Steels P, Rummens JL, Hendrikx M, Hensen K. Mesenchymal stem cells or cardiac progenitors for cardiac repair? A comparative study. Cell Mol Life Sci. 2011;68:2141-2156.
33. Andersen DC, Andersen P, Schneider M, Jensen HB, Sheikh SP. Murine cardiospheres are not a source of stem cells with cardiomyogenic potential. Stem Cells. 2009;27:1571-1581.
34. Shenje LT, Field LJ, Pritchard C, Guerin CJ, Rubart M, Soonpaa MH, Ang KL, Galinëanes M. Lineage tracing of cardiac explant derived cells. PLoS One. 2008;3:e1929.
35. Makkar R, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman DS, Czer L, Marbán L, Mendizabal A, Johnston PV, Russell S, Schuleri KH, Lardo AC, Gerstenblith G, Marbán E. The CADUCEUS (CArdiosphere-Derived aUtologous stem CElls to reverse ventricUlar dySfunction) Trial [abstract]. http://my.americanheart.org/professional/Sessions/ScientificSessions/ ScienceNews/SS11-Clinical-Science-Special-Reports-UCM-433393-Article.jsp. Accessed November 17, 2011.
36. Lefaucheur C, Suberbielle-Boissel C, Hill GS, Nochy D, Andrade J, Antoine C, Gautreau C, Charron D, Glotz D. Clinical relevance of preformed HLA donor-specific antibodies in kidney transplantation. Am J Transplant. 2008;8:324-331.
37. 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 U S A. 2005;102: 8966-8971. (Pubitemid 40881062)
38. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204-1219.
39. Stastna M, Chimenti I, Marbán E, Van Eyk JE. Identification and functionality of proteomes secreted by rat cardiac stem cells and neonatal cardiomyocytes. Proteomics. 2010;10:245-253.
40. Xie Y, Cheng K, Cho HC, Malliaras K, Ibrahim A, Sun B, Galang G, Ionta V, Shen D, Zhang Y, Marban E. Human Cardiosphere-Derived Cells Stimulate Cardiomyocyte Proliferation in vivo and in Co-Culture [abstract]. Circulation. 2011;124:A16688.
41. Steinbrook R. Organ donation after cardiac death. N Engl J Med. 2007; 357:209-213. (Pubitemid 47080384)
42. The 2009 annual report of the OPTN and SRTR: transplant data 1999-2008. www.ustransplant.org. Accessed November 17, 2011.