Paracrine engineering of human cardiac stem cells with insulin-like growth factor 1 enhances myocardial repair

Journal of the American Heart Association

Volumn 4, Issue 9, 2015, Pages

  Jackson, Robyn ^a   Tilokee, Everad L ^a   Latham, Nicholas ^a   Mount, Seth ^a   Rafatian, Ghazaleh ^a   Strydhorst, Jared ^a   Ye, Bin ^a   Boodhwani, Munir ^a   Chan, Vincent ^a   Ruel, Marc ^a   Ruddy, Terrence D ^a   Suuronen, Erik J ^a   Stewart, Duncan J ^b   Davis, Darryl R ^a  

^a UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Cell survival; Cell therapy; Heart failure; Insulin like growth factor 1

Indexed keywords

GREEN FLUORESCENT PROTEIN; SOMATOMEDIN C; IGF1 PROTEIN, HUMAN; SOMATOMEDIN C RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CELL CULTURE; CELL ENGINEERING; CELL PARACRINE ENGINEERING; CELL SURVIVAL; CELL THERAPY; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; GENE TRANSFER; HEART INFARCTION; HEART PROTECTION; HUMAN; HUMAN CELL; MOUSE; MUSCLE REGENERATION; MYOCARDIAL REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCAR FORMATION; VENTRICULAR CARDIOMYOCYTE; AGED; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CARDIAC MUSCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; DISEASE MODEL; GENE THERAPY; GENETIC TRANSFECTION; GENETICS; METABOLISM; MIDDLE AGED; MYOCARDIAL INFARCTION; NONOBESE DIABETIC MOUSE; PARACRINE SIGNALING; PATHOLOGY; PROCEDURES; REGENERATION; SCID MOUSE; STEM CELL; STEM CELL TRANSPLANTATION; TIME FACTOR; UPREGULATION;

AGED; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; GENETIC THERAPY; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; PARACRINE COMMUNICATION; RATS; RECEPTOR, IGF TYPE 1; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84991520711     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.115.002104     Document Type: Article

References (39)

1. 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. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet. 2012;379:895-904.
2. Terrovitis J, Kwok KF, Lautamaki R, Engles JM, Barth AS, Kizana E, Miake J, Leppo MK, Fox J, Seidel J, Pomper M, Wahl RL, Tsui B, Bengel F, Marban E, Abraham MR. Ectopic expression of the sodium-iodide symporter enables imaging of transplanted cardiac stem cells in vivo by single-photon emission computed tomography or positron emission tomography. J Am Coll Cardiol. 2008;52:1652-1660.
3. Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, Marban E. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 2010;106:971-980.
4. Malliaras K, Zhang Y, Seinfeld J, Galang G, Tseliou E, Cheng K, Sun B, Aminzadeh M, Marban E. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med. 2013;5:191-209.
5. Malliaras K, Ibrahim A, Tseliou E, Liu W, Sun B, Middleton RC, Seinfeld J, Wang L, Sharifi BG, Marban E. Stimulation of endogenous cardioblasts by exogenous cell therapy after myocardial infarction. EMBO Mol Med. 2014;6:760-777.
6. Bonios M, Chang CY, Terrovitis J, Pinheiro A, Barth A, Dong P, Santaularia M, Foster DB, Raman V, Abraham TP, Abraham MR. Constitutive HIF-1alpha expression blunts the beneficial effects of cardiosphere-derived cell therapy in the heart by altering paracrine factor balance. J Cardiovasc Transl Res. 2011;4:363-372.
7. Laron Z. Insulin-like growth factor 1 (IGF-1): a growth hormone. Mol Pathol. 2001;54:311-316.
8. Liu JL, LeRoith D. Insulin-like growth factor I is essential for postnatal growth in response to growth hormone. Endocrinology. 1999;140:5178-5184.
9. Ellison GM, Torella D, Dellegrottaglie S, Perez-Martinez C, de Perez PA, Vicinanza C, Purushothaman S, Galuppo V, Iaconetti C, Waring CD, Smith A, Torella M, Cuellas RC, Gonzalo-Orden JM, Agosti V, Indolfi C, Galinanes 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.
10. Koudstaal S, Bastings MM, Feyen DA, Waring CD, van Slochteren FJ, Dankers PY, Torella D, Sluijter JP, Nadal-Ginard B, Doevendans PA, Ellison GM, Chamuleau SA. Sustained delivery of insulin-like growth factor-1/hepatocyte growth factor stimulates endogenous cardiac repair in the chronic infarcted pig heart. J Cardiovasc Transl Res. 2014;7:232-241.
11. Haider HK, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103:1300-1308.
12. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marban E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007;115:896-908.
13. 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. Human cardiac stem cells. Proc Natl Acad Sci USA. 2007;104:14068-14073.
14. Gago-Lopez N, Awaji O, Zhang Y, Ko C, Nsair A, Liem D, Stempien-Otero A, Maclellan WR. THY-1 receptor expression differentiates cardiosphere-derived cells with divergent cardiogenic differentiation potential. Stem Cell Reports. 2014;2:576-591.
15. Sen S, Merchan J, Dean J, Ii M, Gavin M, Silver M, Tkebuchava T, Yoon YS, Rasko JE, Aikawa R. Autologous transplantation of endothelial progenitor cells genetically modified by adeno-associated viral vector delivering insulin-like growth factor-1 gene after myocardial infarction. Hum Gene Ther. 2010;21:1327-1334.
16. Cheng K, Ibrahim A, Hensley MT, Shen D, Sun B, Middleton R, Liu W, Smith RR, Marban E. Relative roles of CD90 and c-kit to the regenerative efficacy of cardiosphere-derived cells in humans and in a mouse model of myocardial infarction. JAmHeart Assoc. 2014;3:e001260 doi: 10.1161/JAHA.114.001260.
17. Davis DR, Kizana E, Terrovitis J, Barth AS, Zhang Y, Smith RR, Miake J, Marban E. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol. 2010;49:312-321.
18. Latham N, Ye B, Jackson R, Lam B, Kuraitis D, Ruel M, Suuronen EJ, Stewart DJ, Davis DR. Human blood and cardiac stem cells synergize to enhance cardiac repair when cotransplanted into ischemic myocardium. Circulation. 2013;128:S1-S8.
19. Mayfield AE, Tilokee EL, Latham N, McNeill B, Lam BK, Ruel M, Suuronen EJ, Courtman DW, Stewart DJ, Davis DR. The effect of encapsulation of cardiac stem cells within matrix-enriched hydrogel capsules on cell survival, post-ischemic cell retention and cardiac function. Biomaterials. 2014;35:133-142.
20. Davis DR, Smith RR, Marban E. Human cardiospheres are a source of stem cells with cardiomyogenic potential. Stem Cells. 2010;28:903-904.
21. Davis DR, Zhang Y, Smith RR, Cheng K, Terrovitis J, Malliaras K, Li TS, White A, Makkar R, Marban E. Validation of the cardiosphere method to culture cardiac progenitor cells from myocardial tissue. PLoS One. 2009;4:e7195.
22. Tiscornia G, Singer O, Verma IM. Production and purification of lentiviral vectors. Nat Protoc. 2006;1:241-245.
23. Sastry L, Johnson T, Hobson MJ, Smucker B, Cornetta K. Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods. Gene Ther. 2002;9:1155-1162.
24. Molgat AS, Tilokee EL, Rafatian G, Vulesevic B, Ruel M, Milne R, Suuronen EJ, Davis DR. Hyperglycemia inhibits cardiac stem cell-mediated cardiac repair and angiogenic capacity. Circulation. 2014;130:S70-S76.
25. Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ. Human stem/ progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci USA. 2005;102:18171-18176.
26. Li T-S, Lee S-T, Matsushita S, Davis DR, Zhang Y, Smith RR, Marban 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;105:2088-2098.
27. Brown RD, Ambler SK, Mitchell MD, Long CS. The cardiac fibroblast:therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol. 2005;45:657-687.
28. Bryant JE, Shamhart PE, Luther DJ, Olson ER, Koshy JC, Costic DJ, Mohile MV, Dockry M, Doane KJ, Meszaros JG. Cardiac myofibroblast differentiation is attenuated by alpha(3) integrin blockade: potential role in post-MI remodeling. J Mol Cell Cardiol. 2009;46:186-192.
29. Fedak PW, Bai L, Turnbull J, Ngu J, Narine K, Duff HJ. Cell therapy limits myofibroblast differentiation and structural cardiac remodeling: basic fibroblast growth factor-mediated paracrine mechanism. Circ Heart Fail. 2012;5:349-356.
30. Shavlakadze T, White J, Hoh JF, Rosenthal N, Grounds MD. Targeted expression of insulin-like growth factor-I reduces early myofiber necrosis in dystrophic mdx mice. Mol Ther. 2004;10:829-843.
31. Taki J, Higuchi T, Kawashima A, Tait JF, Kinuya S, Muramori A, Matsunari I, Nakajima K, Tonami N, Strauss HW. Detection of cardiomyocyte death in a rat model of ischemia and reperfusion using 99 mTc-labeled annexin V. J Nucl Med. 2004;45:1536-1541.
32. Taki J, Higuchi T, Kawashima A, Fukuoka M, Kayano D, Tait JF, Matsunari I, Nakajima K, Kinuya S, Strauss HW. Effect of postconditioning on myocardial 99 mTc-annexin-V uptake: comparison with ischemic preconditioning and caspase inhibitor treatment. J Nucl Med. 2007;48:1301-1307.
33. Taki J, Higuchi T, Kawashima A, Tait JF, Muramori A, Matsunari I, Nakajima K, Vanderheyden JL, Strauss HW. (99m)Tc-annexin-V uptake in a rat model of variable ischemic severity and reperfusion time. Circ J. 2007;71:1141-1146.
34. Zhao Y, Zhao S, Kuge Y, Strauss HW, Blankenberg FG, Tamaki N. Attenuation of apoptosis by telmisartan in atherosclerotic plaques of apolipoprotein E_/_ mice: evaluation using technetium 99m-annexin A5. Mol Imaging. 2013;12:300-309.
35. 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. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet. 2011;378:1847-1857.
36. Anversa P, Cheng W, Liu Y, Leri A, Redaelli G, Kajstura J. Apoptosis and myocardial infarction. Basic Res Cardiol. 1998;93(suppl 3):8-12.
37. Fujiwara H, Matsuda M, Fujiwara Y, Ishida M, Kawamura A, Takemura G, Kida M, Uegaito T, Tanaka M, Horike K. Infarct size and the protection of ischemic myocardium in pig, dog and human. Jpn Circ J. 1989;53:1092-1097.
38. Nian M, Lee P, Khaper N, Liu P. Inflammatory cytokines and postmyocardial infarction remodeling. Circ Res. 2004;94:1543-1553.
39. D'Amario D, Fiorini C, Campbell PM, Goichberg P, Sanada F, Zheng H, Hosoda T, Rota M, Connell JM, Gallegos RP, Welt FG, Givertz MM, Mitchell RN, Leri A, Kajstura J, Pfeffer MA, Anversa P. Functionally competent cardiac stem cells can be isolated from endomyocardial biopsies of patients with advanced cardiomyopathies. Circ Res. 2011;108:857-861.