Advertisement

Imaging Cardiac Stem Cell Therapy

  • Xulei Qin
  • Ian Y. Chen
  • Joseph C. WuEmail author
Chapter
Part of the Cardiac and Vascular Biology book series (Abbreviated title: Card. vasc. biol.)

Abstract

Cardiac stem cell therapy is a promising approach to repair an injured heart. Noninvasive imaging can be tremendously useful for characterizing its therapeutic mechanisms and efficacy. In this chapter, we summarize the roles of various imaging modalities in assessing cell fate and cardiac function following stem cell therapy. The advancement of these imaging technologies is crucial for the full clinical translation of cardiac stem cell therapy.

Keywords

Myocardial infarction Cardiac stem cell therapy Noninvasive imaging 

Notes

Acknowledgment

We thank funding support from American Heart Association 13EIA14420025, National Institutes of Health (NIH) R01 HL123968-03S1, NIH R01 HL133272, NIH R01 HL132875, NIH R01 HL130020, California Institute of Regenerative Medicine (CIRM) DR2A-05394, TR3-05556, and RT3-07798 (JCW), American Heart Association 17SDG33460212 (XQ), and NIH T32 EB009035 (IYC).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Budde MD, Frank JA (2009) Magnetic tagging of therapeutic cells for MRI. J Nucl Med 50(2):171–174. doi: 10.2967/jnumed.108.053546 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Cao F, Li Z, Lee A, Liu Z, Chen K, Wang H, Cai W, Chen X, Wu JC (2009) Noninvasive de novo imaging of human embryonic stem cell-derived teratoma formation. Cancer Res 69(7):2709–2713. doi: 10.1158/0008-5472.CAN-08-4122 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cao F, Lin S, Xie X, Ray P, Patel M, Zhang X, Drukker M, Dylla SJ, Connolly AJ, Chen X, Weissman IL, Gambhir SS, Wu JC (2006) In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 113(7):1005–1014. doi: 10.1161/circulationaha.105.588954 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Castellani M, Colombo A, Giordano R, Pusineri E, Canzi C, Longari V, Piccaluga E, Palatresi S, Dellavedova L, Soligo D, Rebulla P, Gerundini P (2010) The role of PET with 13N-ammonia and 18F-FDG in the assessment of myocardial perfusion and metabolism in patients with recent AMI and intracoronary stem cell injection. J Nucl Med 51(12):1908–1916. doi: 10.2967/jnumed.110.078469 CrossRefPubMedGoogle Scholar
  5. Chan AT, Karakas MF, Vakrou S, Afzal J, Rittenbach A, Lin X, Wahl RL, Pomper MG, Steenbergen CJ, Tsui BM, Elisseeff JH, Abraham MR (2015) Hyaluronic acid-serum hydrogels rapidly restore metabolism of encapsulated stem cells and promote engraftment. Biomaterials 73:1–11. doi: 10.1016/j.biomaterials.2015.09.001 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chen IY, Wu JC (2011) Cardiovascular molecular imaging: focus on clinical translation. Circulation 123(4):425–443. doi: 10.1161/CIRCULATIONAHA.109.916338 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen J, Hsieh AF, Dharmarajan K, Masoudi FA, Krumholz HM (2013) National trends in heart failure hospitalization after acute myocardial infarction for Medicare beneficiaries: 1998–2010. Circulation 128(24):2577–2584. doi: 10.1161/CIRCULATIONAHA.113.003668 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen Y, Ye L, Zhong J, Li X, Yan C, Chandler MP, Calvin S, Xiao F, Negia M, Low WC, Zhang J, Yu X (2015) The structural basis of functional improvement in response to human umbilical cord blood stem cell transplantation in hearts with postinfarct LV remodeling. Cell Transplant 24(6):971–983. doi: 10.3727/096368913x675746 CrossRefPubMedGoogle Scholar
  9. Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ, Mahoney WM, Van Biber B, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem HP, Laflamme MA, Murry CE (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510(7504):273–277. doi: 10.1038/nature 13233 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Choudry F, Hamshere S, Saunders N, Veerapen J, Bavnbek K, Knight C, Pellerin D, Locca D, Westwood M, Rakhit R, Crake T, Kastrup J, Parmar M, Agrawal S, Jones D, Martin J, Mathur A (2015) A randomized double-blind control study of early intra-coronary autologous bone marrow cell infusion in acute myocardial infarction: the REGENERATE-AMI clinical trialdagger. Eur Heart J. doi: 10.1093/eurheartj/ehv493 Google Scholar
  11. Chung J, Kee K, Barral JK, Dash R, Kosuge H, Wang X, Weissman I, Robbins RC, Nishimura D, Quertermous T, Reijo-Pera RA, Yang PC (2011) In vivo molecular MRI of cell survival and teratoma formation following embryonic stem cell transplantation into the injured murine myocardium. Magn Reson Med 66(5):1374–1381. doi: 10.1002/mrm.22929 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Emmert MY, Weber B, Wolint P, Frauenfelder T, Zeisberger SM, Behr L, Sammut S, Scherman J, Brokopp CE, Schwartlander R, Vogel V, Vogt P, Grunenfelder J, Alkadhi H, Falk V, Boss A, Hoerstrup SP (2013a) Intramyocardial transplantation and tracking of human mesenchymal stem cells in a novel intra-uterine pre-immune fetal sheep myocardial infarction model: a proof of concept study. PLoS One 8(3):e57759. doi: 10.1371/journal.pone.0057759 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Emmert MY, Wolint P, Winklhofer S, Stolzmann P, Cesarovic N, Fleischmann T, Nguyen TD, Frauenfelder T, Boni R, Scherman J, Bettex D, Grunenfelder J, Schwartlander R, Vogel V, Gyongyosi M, Alkadhi H, Falk V, Hoerstrup SP (2013b) Transcatheter based electromechanical mapping guided intramyocardial transplantation and in vivo tracking of human stem cell based three dimensional microtissues in the porcine heart. Biomaterials 34(10):2428–2441. doi: 10.1016/j.biomaterials.2012.12.021 CrossRefPubMedGoogle Scholar
  14. Freeman BT, Kouris NA, Ogle BM (2015) Tracking fusion of human mesenchymal stem cells after transplantation to the heart. Stem Cells Transl Med 4(6):685–694. doi: 10.5966/sctm.2014-0198 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Friedrich MG, Marcotte F (2013) Cardiac magnetic resonance assessment of myocarditis. Circ Cardiovasc Imaging 6(5):833–839. doi: 10.1161/CIRCIMAGING.113.000416 CrossRefPubMedGoogle Scholar
  16. Godier-Furnemont AF, Tekabe Y, Kollaros M, Eng G, Morales A, Vunjak-Novakovic G, Johnson LL (2013) Noninvasive imaging of myocyte apoptosis following application of a stem cell-engineered delivery platform to acutely infarcted myocardium. J Nucl Med 54(6):977–983. doi: 10.2967/jnumed.112.112979 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Golpanian S, El-Khorazaty J, Mendizabal A, DiFede DL, Suncion VY, Karantalis V, Fishman JE, Ghersin E, Balkan W, Hare JM (2015) Effect of aging on human mesenchymal stem cell therapy in ischemic cardiomyopathy patients. J Am Coll Cardiol 65(2):125–132. doi: 10.1016/j.jacc.2014.10.040 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gowdak LH, Schettert IT, Rochitte CE, Lisboa LA, Dallan LA, Cesar LA, de Oliveira SA, Krieger JE (2011) Early increase in myocardial perfusion after stem cell therapy in patients undergoing incomplete coronary artery bypass surgery. J Cardiovasc Transl Res 4(1):106–113. doi: 10.1007/s12265-010-9234-2 CrossRefPubMedGoogle Scholar
  19. Grajek S, Popiel M, Gil L, Breborowicz P, Lesiak M, Czepczynski R, Sawinski K, Straburzynska-Migaj E, Araszkiewicz A, Czyz A, Kozlowska-Skrzypczak M, Komarnicki M (2010) Influence of bone marrow stem cells on left ventricle perfusion and ejection fraction in patients with acute myocardial infarction of anterior wall: randomized clinical trial: impact of bone marrow stem cell intracoronary infusion on improvement of microcirculation. Eur Heart J 31(6):691–702. doi: 10.1093/eurheartj/ehp536 CrossRefPubMedGoogle Scholar
  20. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H (2005) Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111(17):2198–2202. doi: 10.1161/01.Cir.0000163546.27639.Aa CrossRefPubMedGoogle Scholar
  21. Hou D, Youssef EA, Brinton TJ, Zhang P, Rogers P, Price ET, Yeung AC, Johnstone BH, Yock PG, March KL (2005) Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation 112(9 Suppl):I150–I156. doi: 10.1161/CIRCULATIONAHA.104.526749 PubMedGoogle Scholar
  22. Hu S, Huang M, Nguyen PK, Gong Y, Li Z, Jia F, Lan F, Liu J, Nag D, Robbins RC, Wu JC (2011) Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation 124(11 Suppl):S27–S34. doi: 10.1161/circulationaha.111.017954 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Huikuri HV, Kervinen K, Niemela M, Ylitalo K, Saily M, Koistinen P, Savolainen ER, Ukkonen H, Pietila M, Airaksinen JK, Knuuti J, Makikallio TH, Investigators F (2008) Effects of intracoronary injection of mononuclear bone marrow cells on left ventricular function, arrhythmia risk profile, and restenosis after thrombolytic therapy of acute myocardial infarction. Eur Heart J 29(22):2723–2732. doi: 10.1093/eurheartj/ehn436 CrossRefPubMedGoogle Scholar
  24. Jokerst JV, Khademi C, Gambhir SS (2013) Intracellular aggregation of multimodal silica nanoparticles for ultrasound-guided stem cell implantation. Sci Transl Med 5(177):177ra135–177ra135. doi: 10.1126/scitranslmed.3005228 CrossRefGoogle Scholar
  25. Kammili RK, Taylor DG, Xia JX, Osuala K, Thompson K, Menick DR, Ebert SN (2010) Generation of novel reporter stem cells and their application for molecular imaging of cardiac-differentiated stem cells in vivo. Stem Cells Dev 19(9):1437–1448. doi: 10.1089/scd.2009.0308 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kang HJ, Kim MK, Lee HY, Park KW, Lee W, Cho YS, Koo BK, Choi DJ, Park YB, Kim HS (2012) Five-year results of intracoronary infusion of the mobilized peripheral blood stem cells by granulocyte colony-stimulating factor in patients with myocardial infarction. Eur Heart J 33(24):3062–3069. doi: 10.1093/eurheartj/ehs231 CrossRefPubMedGoogle Scholar
  27. Kim PJ, Mahmoudi M, Ge X, Matsuura Y, Toma I, Metzler S, Kooreman NG, Ramunas J, Holbrook C, McConnell MV, Blau H, Harnish P, Rulifson E, Yang PC (2015) Direct evaluation of myocardial viability and stem cell engraftment demonstrates salvage of the injured myocardium. Circ Res 116(7):e40–e50. doi: 10.1161/circresaha.116.304668 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kraehenbuehl TP, Ferreira LS, Hayward AM, Nahrendorf M, van der Vlies AJ, Vasile E, Weissleder R, Langer R, Hubbell JA (2011) Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 32(4):1102–1109. doi: 10.1016/j.biomaterials.2010.10.005 CrossRefPubMedGoogle Scholar
  29. Kwong RY, Farzaneh-Far A (2011) Measuring myocardial scar by CMR. JACC Cardiovasc Imaging 4(2):157–160. doi: 10.1016/j.jcmg.2010.12.004 CrossRefPubMedGoogle Scholar
  30. La Gerche A, Claessen G, Van de Bruaene A, Pattyn N, Van Cleemput J, Gewillig M, Bogaert J, Dymarkowski S, Claus P, Heidbuchel H (2013) Cardiac MRI: a new gold standard for ventricular volume quantification during high-intensity exercise. Circ Cardiovasc Imaging 6(2):329–338. doi: 10.1161/CIRCIMAGING.112.980037 CrossRefPubMedGoogle Scholar
  31. 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 (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25(9):1015–1024. doi: 10.1038/nbt1327 CrossRefPubMedGoogle Scholar
  32. Lang C, Lehner S, Todica A, Boening G, Franz WM, Bartenstein P, Hacker M, David R (2013) Positron emission tomography based in-vivo imaging of early phase stem cell retention after intramyocardial delivery in the mouse model. Eur J Nucl Med Mol Imaging 40(11):1730–1738. doi: 10.1007/s00259-013-2480-1 CrossRefPubMedGoogle Scholar
  33. Lang C, Lehner S, Todica A, Boening G, Zacherl M, Franz WM, Krause BJ, Bartenstein P, Hacker M, David R (2014) In-vivo comparison of the acute retention of stem cell derivatives and fibroblasts after intramyocardial transplantation in the mouse model. Eur J Nucl Med Mol Imaging 41(12):2325–2336. doi: 10.1007/s00259-014-2858-8 CrossRefPubMedGoogle Scholar
  34. Lee AR, Woo SK, Kang SK, Lee SY, Lee MY, Park NW, Song SH, Lee SY, Nahm SS, JE Y, Kim MH, Yoo RJ, Kang JH, Lee YJ, Eom KD (2015) Adenovirus-mediated expression of human sodium-iodide symporter gene permits in vivo tracking of adipose tissue-derived stem cells in a canine myocardial infarction model. Nucl Med Biol 42(7):621–629. doi: 10.1016/j.nucmedbio.2015.03.006 CrossRefPubMedGoogle Scholar
  35. Lee AS, Tang C, Rao MS, Weissman IL, JC W (2013) Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat Med 19(8):998–1004. doi: 10.1038/nm.3267 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Li Z, Wu JC, Sheikh AY, Kraft D, Cao F, Xie X, Patel M, Gambhir SS, Robbins RC, Cooke JP, Wu JC (2007) Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116(11 Suppl):I46–I54. doi: 10.1161/circulationaha.106.680561 PubMedPubMedCentralGoogle Scholar
  37. Li ZJ, Suzuki Y, Huang M, Cao F, Xie XY, Connolly AJ, Yang PC, JC W (2008) Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells 26(4):864–873. doi: 10.1634/stemcells.2007-0843 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Liu J, Narsinh KH, Lan F, Wang L, Nguyen PK, Hu S, Lee A, Han L, Gong Y, Huang M, Nag D, Rosenberg J, Chouldechova A, Robbins RC, Wu JC (2012) Early stem cell engraftment predicts late cardiac functional recovery: preclinical insights from molecular imaging. Circ Cardiovasc Imaging 5(4):481–490. doi: 10.1161/circimaging.111.969329 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Macarthur JW Jr, Cohen JE, McGarvey JR, Shudo Y, Patel JB, Trubelja A, Fairman AS, Edwards BB, Hung G, Hiesinger W, Goldstone AB, Atluri P, Wilensky RL, Pilla JJ, Gorman JH 3rd, Gorman RC, Woo YJ (2014) Preclinical evaluation of the engineered stem cell chemokine stromal cell-derived factor 1alpha analog in a translational ovine myocardial infarction model. Circ Res 114(4):650–659. doi: 10.1161/circresaha.114.302884 CrossRefPubMedGoogle Scholar
  40. Menasche P, Vanneaux V, Hagege A, Bel A, Cholley B, Cacciapuoti I, Parouchev A, Benhamouda N, Tachdjian G, Tosca L, Trouvin JH, Fabreguettes JR, Bellamy V, Guillemain R, Suberbielle Boissel C, Tartour E, Desnos M, Larghero J (2015) Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Eur Heart J 36(30):2011–2017. doi: 10.1093/eurheartj/ehv189 CrossRefPubMedGoogle Scholar
  41. Naumova AV, Yarnykh VL, Balu N, Reinecke H, Murry CE, Yuan C (2012) Quantification of MRI signal of transgenic grafts overexpressing ferritin in murine myocardial infarcts. NMR Biomed 25(10):1187–1195. doi: 10.1002/nbm.2788 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Neofytou E, O'Brien CG, Couture LA, Wu JC (2015) Hurdles to clinical translation of human induced pluripotent stem cells. J Clin Invest 125(7):2551–2557. doi: 10.1172/JCI80575 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nguyen PK, Neofytou E, Rhee JW, Wu JC (2016a) Potential strategies to address the major clinical hurdles facing stem cell regenerative therapy for cardiovascular disease: a review. JAMA Cardiol 1(8):953–962. doi: 10.1001/jamacardio.2016.2750
  44. Nguyen PK, Rhee JW, Wu JC (2016b) Adult stem cell therapy and heart failure, 2000 to 2016: a systematic review. JAMA Cardiol 1(7):831–841. doi: 10.1001/jamacardio.2016.2225
  45. Nguyen PK, Riegler J,Wu JC (2014) Stem cell imaging: from bench to bedside. Cell Stem Cell 14(4):431–444. doi: 10.1016/j.stem.2014.03.009 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ong SG, Huber BC, Hee Lee W, Kodo K, Ebert AD, Ma Y, Nguyen PK, Diecke S, Chen WY, Wu JC (2015) Microfluidic single-cell analysis of transplanted human induced pluripotent stem cell-derived cardiomyocytes after acute myocardial infarction. Circulation 132(8):762–771. doi: 10.1161/circulationaha.114.015231 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Oommen S, Yamada S, Cantero Peral S, Campbell KA, Bruinsma ES, Terzic A, Nelson TJ (2015) Human umbilical cord blood-derived mononuclear cells improve murine ventricular function upon intramyocardial delivery in right ventricular chronic pressure overload. Stem Cell Res Ther 6:50. doi: 10.1186/s13287-015-0044-y CrossRefPubMedPubMedCentralGoogle Scholar
  48. Partlow KC, Chen JJ, Brant JA, Neubauer AM, Meyerrose TE, Creer MH, Nolta JA, Caruthers SD, Lanza GM, Wickline SA (2007) F-19 magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J 21(8):1647–1654. doi: 10.1096/fj.06-6505com CrossRefPubMedGoogle Scholar
  49. Pei Z, Lan X, Cheng Z, Qin C, Xia X, Yuan H, Ding Z, Zhang Y (2014) Multimodality molecular imaging to monitor transplanted stem cells for the treatment of ischemic heart disease. PLoS One 9(3):e90543. doi: 10.1371/journal.pone.0090543 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Peng C, Yang K, Xiang P, Zhang C, Zou L, Wu X, Gao Y, Kang Z, He K, Liu J, Cheng M, Wang J, Chen L (2013) Effect of transplantation with autologous bone marrow stem cells on acute myocardial infarction. Int J Cardiol 162(3):158–165. doi: 10.1016/j.ijcard.2011.05.077 CrossRefPubMedGoogle Scholar
  51. Penheiter AR, Russell SJ, Carlson SK (2012) The sodium iodide symporter (NIS) as an imaging reporter for gene, viral, and cell-based therapies. Curr Gene Ther 12(1):33–47. doi: 10.2174/156652312799789235 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Qiao H, Zhang H, Zheng Y, Ponde DE, Shen D, Gao F, Bakken AB, Schmitz A, Kung HF, Ferrari VA, Zhou R (2009) Embryonic stem cell grafting in normal and infarcted myocardium: serial assessment with MR imaging and PET dual detection. Radiology 250(3):821–829. doi: 10.1148/radiol.2503080205 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Riegler J, Ebert A, Qin X, Shen Q, Wang M, Ameen M, Kodo K, Ong SG, Lee WH, Lee G, Neofytou E, Gold JD, Connolly AJ, Wu JC (2016) Comparison of magnetic resonance imaging and serum biomarkers for detection of human pluripotent stem cell-derived teratomas. Stem Cell Rep. doi: 10.1016/j.stemcr.2015.12.008 Google Scholar
  54. Riegler J, Tiburcy M, Ebert A, Tzatzalos E, Raaz U, Abilez OJ, Shen Q, Kooreman NG, Neofytou E, Chen VC, Wang M, Meyer T, Tsao PS, Connolly AJ, Couture LA, Gold JD, Zimmermann WH, Wu JC (2015) Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ Res 117(8):720–730. doi: 10.1161/circresaha.115.306985 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schneider C, Jaquet K, Geidel S, Rau T, Malisius R, Boczor S, Zienkiewicz T, Kuck KH, Krause K (2009) Transplantation of bone marrow-derived stem cells improves myocardial diastolic function: strain rate imaging in a model of hibernating myocardium. J Am Soc Echocardiogr 22(10):1180–1189. doi: 10.1016/j.echo.2009.06.011 CrossRefPubMedGoogle Scholar
  56. Sheikh AY, Huber BC, Narsinh KH, Spin JM, van der Bogt K, de Almeida PE, Ransohoff KJ, Kraft DL, Fajardo G, Ardigo D, Ransohoff J, Bernstein D, Fischbein MP, Robbins RC, Wu JC (2012) In vivo functional and transcriptional profiling of bone marrow stem cells after transplantation into ischemic myocardium. Arterioscler Thromb Vasc Biol 32(1):92–102. doi: 10.1161/atvbaha.111.238618 CrossRefPubMedGoogle Scholar
  57. Sosnovik DE, Mekkaoui C, Huang S, Chen HH, Dai G, Stoeck CT, Ngoy S, Guan J, Wang R, Kostis WJ, Jackowski MP, Wedeen VJ, Kozerke S, Liao R (2014) Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo. Circulation 129(17):1731–1741. doi: 10.1161/CIRCULATIONAHA.113.005841 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sun N, Lee A, Wu JC (2009) Long term non-invasive imaging of embryonic stem cells using reporter genes. Nat Protoc 4(8):1192–1201. doi: 10.1038/nprot.2009.100 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Surder D, Manka R, Lo Cicero V, Moccetti T, Rufibach K, Soncin S, Turchetto L, Radrizzani M, Astori G, Schwitter J, Erne P, Zuber M, Auf der Maur C, Jamshidi P, Gaemperli O, Windecker S, Moschovitis A, Wahl A, Buhler I, Wyss C, Kozerke S, Landmesser U, Luscher TF, Corti R (2013) Intracoronary injection of bone marrow-derived mononuclear cells early or late after acute myocardial infarction: effects on global left ventricular function. Circulation 127(19):1968–1979. doi: 10.1161/CIRCULATIONAHA.112.001035 CrossRefPubMedGoogle Scholar
  60. Vallee JP, Hauwel M, Lepetit-Coiffe M, Bei W, Montet-Abou K, Meda P, Gardier S, Zammaretti P, Kraehenbuehl TP, Herrmann F, Hubbell JA, Jaconi ME (2012) Embryonic stem cell-based cardiopatches improve cardiac function in infarcted rats. Stem Cells Transl Med 1(3):248–260. doi: 10.5966/sctm.2011-0028 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Vrtovec B, Poglajen G, Lezaic L, Sever M, Socan A, Domanovic D, Cernelc P, Torre-Amione G, Haddad F, Wu JC (2013) Comparison of transendocardial and intracoronary CD34+ cell transplantation in patients with nonischemic dilated cardiomyopathy. Circulation 128(11 Suppl 1):S42–S49. doi: 10.1161/CIRCULATIONAHA.112.000230 CrossRefPubMedGoogle Scholar
  62. Wang J, Najjar A, Zhang S, Rabinovich B, Willerson JT, Gelovani JG, Yeh ET (2012) Molecular imaging of mesenchymal stem cell: mechanistic insight into cardiac repair after experimental myocardial infarction. Circ Cardiovasc Imaging 5(1):94–101. doi: 10.1161/circimaging.111.966424 CrossRefPubMedGoogle Scholar
  63. Wendel JS, Ye L, Zhang P, Tranquillo RT, Zhang JJ (2014) Functional consequences of a tissue-engineered myocardial patch for cardiac repair in a rat infarct model. Tissue Eng Part A 20(7–8):1325–1335. doi: 10.1089/ten.TEA.2013.0312 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Williams AR, Suncion VY, McCall F, Guerra D, Mather J, Zambrano JP, Heldman AW, Hare JM (2013) Durable scar size reduction due to allogeneic mesenchymal stem cell therapy regulates whole-chamber remodeling. J Am Heart Assoc 2(3):e000140. doi: 10.1161/jaha.113.000140 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Winter EM, Hogers B, van der Graaf LM, Gittenberger-de Groot AC, Poelmann RE, van der Weerd L (2010) Cell tracking using iron oxide fails to distinguish dead from living transplanted cells in the infarcted heart. Magn Reson Med 63(3):817–821. doi: 10.1002/mrm.22094 CrossRefPubMedGoogle Scholar
  66. Wyles SP, Yamada S, Oommen S, Maleszewski JJ, Beraldi R, Martinez-Fernandez A, Terzic A, Nelson TJ (2014) Inhibition of DNA topoisomerase II selectively reduces the threat of tumorigenicity following induced pluripotent stem cell-based myocardial therapy. Stem Cells Dev 23(19):2274–2282. doi: 10.1089/scd.2014.0259 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Xiong Q, Ye L, Zhang P, Lepley M, Tian J, Li J, Zhang L, Swingen C, Vaughan JT, Kaufman DS, Zhang J (2013) Functional consequences of human induced pluripotent stem cell therapy: myocardial ATP turnover rate in the in vivo swine heart with postinfarction remodeling. Circulation 127(9):997–1008. doi: 10.1161/CIRCULATIONAHA.112.000641 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yaghoubi SS, Jensen MC, Satyamurthy N, Budhiraja S, Paik D, Czernin J, Gambhir SS (2009) Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma. Nat Clin Pract Oncol 6(1):53–58. doi: 10.1038/ncponc1278 CrossRefPubMedGoogle Scholar
  69. Yamada S, Nelson TJ, Kane GC, Martinez-Fernandez A, Crespo-Diaz RJ, Ikeda Y, Perez-Terzic C, Terzic A (2013) Induced pluripotent stem cell intervention rescues ventricular wall motion disparity, achieving biological cardiac resynchronization post-infarction. J Physiol 591(Pt 17):4335–4349. doi: 10.1113/jphysiol.2013.252288 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ye L, Chang YH, Xiong Q, Zhang P, Zhang L, Somasundaram P, Lepley M, Swingen C, Su L, Wendel JS, Guo J, Jang A, Rosenbush D, Greder L, Dutton JR, Zhang J, Kamp TJ, Kaufman DS, Ge Y, Zhang J (2014) Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 15(6):750–761. doi: 10.1016/j.stem.2014.11.009 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zheng B, Vazin T, Goodwill PW, Conway A, Verma A, Saritas EU, Schaffer D, Conolly SM (2015) Magnetic Particle Imaging tracks the long-term fate of in vivo neural cell implants with high image contrast. Sci Rep 5:14055. doi: 10.1038/srep14055 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zimmermann WH, Melnychenko I, Wasmeier G, Didie M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T (2006) Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12(4):452–458. doi: 10.1038/nm1394 CrossRefPubMedGoogle Scholar
  73. Zipes DP, Jalife J (2009) Cardiac electrophysiology: from cell to bedside. Saunders/Elsevier, PhiladelphiaGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Stanford Cardiovascular Institute, Stanford University School of MedicineStanfordUSA
  2. 2.Departments of Medicine and RadiologyStanford University School of MedicineStanfordUSA
  3. 3.Institute of Stem Cell Biology and Regenerative Medicine, Stanford University School of MedicineStanfordUSA

Personalised recommendations