Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: Assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression

Circulation

Volumn 126, Issue 4, 2012, Pages 430-439

  Templin, Christian ^a   Zweigerdt, Robert ^a   Schwanke, Kristin ^a   Olmer, Ruth ^a   Ghadri, Jelena Rima ^b   Emmert, Maximilian Y ^b   Müller, Ennio ^b   Küest, Silke M ^b   Cohrs, Susan ^c   Schibli, Roger ^c   Kronen, Peter ^d,e,f   Hilbe, Monika ^f   Reinisch, Andreas ^g   Strunk, Dirk ^g   Haverich, Axel ^a   Hoerstrup, Simon ^b   Lüscher, Thomas F ^a   Kaufmann, Philipp A ^b   Landmesser, Ulf ^a   Martin, Ulrich ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b Department of Surgical Research ^*  (Switzerland)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d ETH Zurich   (Switzerland)

^e Veterinary Anesthesia Services International   (Switzerland)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

imaging; induced pluripotent stem cells; iPS cell; myocardial infarction in pig; sodium iodide symporter (NIS)

Indexed keywords

IODINE 123; SODIUM IODIDE SYMPORTER; TETROFOSMIN TC 99M;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY OCCLUSION; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CELL TRACKING; CELL VIABILITY; CELLULAR DISTRIBUTION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENGRAFTMENT; FEMALE; GENE EXPRESSION; HEART INFARCTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MYOCARDIAL PERFUSION IMAGING; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REPORTER GENE; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; STEM CELL TRANSPLANTATION; SWINE; TRANSGENE;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEASIBILITY STUDIES; GENE EXPRESSION; GRAFT SURVIVAL; HEART; HUMANS; INJECTIONS; MYOCARDIAL INFARCTION; MYOCARDIUM; PLURIPOTENT STEM CELLS; POSITRON-EMISSION TOMOGRAPHY AND COMPUTED TOMOGRAPHY; STEM CELL TRANSPLANTATION; SWINE; SYMPORTERS; TRANSGENES; TREATMENT OUTCOME;

EID: 84864288972     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.087684     Document Type: Article

References (34)

1. Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, Zweigerdt R, Gruh I, Meyer J, Wagner S, Maier LS, Han DW, Glage S, Miller K, Fischer P, Scholer HR, Martin U. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell. 2009;5: 434-441.
2. Mauritz C, Martens A, Rojas SV, Schnick T, Rathert C, Schecker N, Menke S, Glage S, Zweigerdt R, Haverich A, Martin U, Kutschka I. Induced pluripotent stem cell (iPSC)-derived flk-1 progenitor cells engraft, differentiate, and improve heart function in a mouse model of acute myocardial infarction. Eur Heart J. 2011;32:2634-2641.
3. Mauritz C, Schwanke K, Reppel M, Neef S, Katsirntaki K, Maier LS, Nguemo F, Menke S, Haustein M, Hescheler J, Hasenfuss G, Martin U. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation. 2008;118:507-517.
4. Zhang SJ, Wu JC. Comparison of imaging techniques for tracking cardiac stem cell therapy. J Nucl Med. 2007;48:1916-1919. (Pubitemid 350232321)
5. Olmer R, Haase A, Merkert S, Cui W, Palecek J, Ran C, Kirschning A, Scheper T, Glage S, Miller K, Curnow EC, Hayes ES, Martin U. Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res. 2010;5:51-64.
6. Zweigerdt R, Olmer R, Singh H, Haverich A, Martin U. Scalable expansion of human pluripotent stem cells in suspension culture. Nat Protoc. 2011;6:689-700.
7. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008; 132:661-680. (Pubitemid 351260059)
8. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, O'Sullivan C, Collins L, Chen Y, Minami E, Gill EA, Ueno S, Yuan C, Gold J, Murry CE. Cardiomyocytes derived from human embryonic stem cells in prosurvival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007;25:1015-1024. (Pubitemid 47517637)
9. Muller-Ehmsen J, Krausgrill B, Burst V, Schenk K, Neisen UC, Fries JW, Fleischmann BK, Hescheler J, Schwinger RH. Effective engraftment but poor mid-term persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. J Mol Cell Cardiol. 2006;41:876-884. (Pubitemid 44635568)
10. Teng CJ, Luo J, Chiu RC, Shum-Tim D. Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty. J Thorac Cardiovasc Surg. 2006;132:628-632. (Pubitemid 44278933)
11. van Laake LW, Passier R, Doevendans PA, Mummery CL. Human embryonic stem cell-derived cardiomyocytes and cardiac repair in rodents. Circ Res. 2008;102:1008-1010. (Pubitemid 351667854)
12. Templin C, Luscher TF, Landmesser U. Cell-based cardiovascular repair and regeneration in acute myocardial infarction and chronic ischemic cardiomyopathy-current status and future developments. Int J Dev Biol. 2011;55:407-417.
13. Gandolfi F, Vanelli A, Pennarossa G, Rahaman M, Acocella F, Brevini TA. Large animal models for cardiac stem cell therapies. Theriogenology. 2011;75:1416-1425.
14. Bengel FM, Schachinger V, Dimmeler S. Cell-based therapies and imaging in cardiology. Eur J Nucl Med Mol Imaging. 2005;32(suppl 2):S404-S416. (Pubitemid 41796403)
15. de Almeida PE, van Rappard JR, Wu JC. In vivo bioluminescence for tracking cell fate and function. Am J Physiol. 2011;301:H663-H671.
16. Ruggiero A, Thorek DL, Guenoun J, Krestin GP, Bernsen MR. Cell tracking in cardiac repair: what to image and how to image. Eur Radiol. 2012;22:189-204.
17. Lee AS, Xu D, Plews JR, Nguyen PK, Nag D, Lyons JK, Han L, Hu S, Lan F, Liu J, Huang M, Narsinh KH, Long CT, de Almeida PE, Levi B, Kooreman N, Bangs C, Pacharinsak C, Ikeno F, Yeung AC, Gambhir SS, Robbins RC, Longaker MT, Wu JC. Preclinical derivation and imaging of autologously transplanted canine induced pluripotent stem cells. J Biol Chem. 2011;286:32697-32704.
18. Willmann JK, Paulmurugan R, Rodriguez-Porcel M, Stein W, Brinton TJ, Connolly AJ, Nielsen CH, Lutz AM, Lyons J, Ikeno F, Suzuki Y, Rosenberg J, Chen IY, Wu JC, Yeung AC, Yock P, Robbins RC, Gambhir SS. Imaging gene expression in human mesenchymal stem cells: from small to large animals. Radiology. 2009;252:117-127.
19. 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 sodiumiodide 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.
20. Dohan O, De la Vieja A, Paroder V, Riedel C, Artani M, Reed M, Ginter CS, Carrasco N. The sodium/iodide symporter (NIS): characterization, regulation, and medical significance. Endocr Rev. 2003;24:48-77. (Pubitemid 36223279)
21. Stodilka RZ, Blackwood KJ, Kong H, Prato FS. A method for quantitative cell tracking using SPECT for the evaluation of myocardial stem cell therapy. Nucl Med Commun. 2006;27:807-813. (Pubitemid 44401250)
22. Gyongyosi M, Dib N. Diagnostic and prognostic value of 3D NOGA mapping in ischemic heart disease. Nat Rev Cardiol. 2011;8:393-404.
23. Buechel RR, Husmann L, Herzog BA, Pazhenkottil AP, Nkoulou R, Ghadri JR, Treyer V, von Schulthess P, Kaufmann PA. Low-dose computed tomography coronary angiography with prospective electrocardiogram triggering: feasibility in a large population. J Am Coll Cardiol. 2011;57:332-336.
24. Buechel RR, Herzog BA, Husmann L, Burger IA, Pazhenkottil AP, Treyer V, Valenta I, von Schulthess P, Nkoulou R, Wyss CA, Kaufmann PA. Ultrafast nuclear myocardial perfusion imaging on a new gamma camera with semiconductor detector technique: first clinical validation. Eur J Nucl Med Mol Imaging. 2010;37:773-778.
25. Herzog BA, Buechel RR, Husmann L, Pazhenkottil AP, Burger IA, Wolfrum M, Nkoulou RN, Valenta I, Ghadri JR, Treyer V, Kaufmann PA. Validation of CT attenuation correction for high-speed myocardial perfusion imaging using a novel cadmium-zinc-telluride detector technique. J Nucl Med. 2010;51:1539-1544.
26. Xu XQ, Zweigerdt R, Soo SY, Ngoh ZX, Tham SC, Wang ST, Graichen R, Davidson B, Colman A, Sun W. Highly enriched cardiomyocytes from human embryonic stem cells. Cytotherapy. 2008;10:376-389. (Pubitemid 351983161)
27. Wai LE, Fujiki M, Takeda S, Martinez OM, Krams SM. Rapamycin, but not cyclosporine or fk506, alters natural killer cell function. Transplantation. 2008;85:145-149.
28. Drukker M, Benvenisty N. The immunogenicity of human embryonic stem-derived cells. Trends Biotechnol. 2004;22:136-141. (Pubitemid 38230392)
29. Chiossone L, Vitale C, Cottalasso F, Moretti S, Azzarone B, Moretta L, Mingari MC. Molecular analysis of the methylprednisolone-mediated inhibition of NK-cell function: evidence for different susceptibility of IL-2-versus IL-15-activated NK cells. Blood. 2007;109:3767-3775. (Pubitemid 46641727)
30. Xu XQ, Soo SY, Sun W, Zweigerdt R. Global expression profile of highly enriched cardiomyocytes derived from human embryonic stem cells. Stem Cells. 2009;27:2163-2174.
31. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol. 2011;29: 731-734.
32. Al Kindi A, Ge Y, Shum-Tim D, Chiu RC. Cellular cardiomyoplasty: routes of cell delivery and retention. Front Biosci. 2008;13: 2421-2434. (Pubitemid 351599695)
33. Wen Z, Zheng S, Zhou C, Wang J, Wang T. Repair mechanisms of bone marrow mesenchymal stem cells in myocardial infarction. J Cell Mol Med. 2011;15:1032-1043.
34. Shi M, Liu ZW, Wang FS. Immunomodulatory properties and therapeutic application of mesenchymal stem cells. Clin Exp Immunol. 2011;164: 1-8.