Journal of Nuclear Cardiology

, 18:966

Noninvasive stem cell tracking

From Bench to Imaging

References

  1. 1.
    Dimmeler S, Zeiher AM, Schneider MD. Unchain my heart: The scientific foundations of cardiac repair. J Clin Invest 2005;115:572-83.PubMedGoogle Scholar
  2. 2.
    Forrester JS, Price MJ, Makkar RR. Stem cell repair of infarcted myocardium: An overview for clinicians. Circulation 2003;108:1139-45.PubMedCrossRefGoogle Scholar
  3. 3.
    Losordo DW, Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease: Part ii: Cell-based therapies. Circulation 2004;109:2692-7.PubMedCrossRefGoogle Scholar
  4. 4.
    Wollert KC, Drexler H. Clinical applications of stem cells for the heart. Circ Res 2005;96:151-63.PubMedCrossRefGoogle Scholar
  5. 5.
    Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006;355:1210-21.PubMedCrossRefGoogle Scholar
  6. 6.
    Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: The boost randomised controlled clinical trial. Lancet 2004;364:141-8.PubMedCrossRefGoogle Scholar
  7. 7.
    Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001;108:407-14.PubMedGoogle Scholar
  8. 8.
    Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 2004;95:911-21.PubMedCrossRefGoogle Scholar
  9. 9.
    Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, et al. Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 2003;100:12313-8.PubMedCrossRefGoogle Scholar
  10. 10.
    Mauritz C, Schwanke K, Reppel M, Neef S, Katsirntaki K, Maier LS, et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation 2008;118:507-17.PubMedCrossRefGoogle Scholar
  11. 11.
    Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, et al. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 2006;355:1199-209.PubMedCrossRefGoogle Scholar
  12. 12.
    Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 2006;355:1222-32.PubMedCrossRefGoogle Scholar
  13. 13.
    Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, et al. Autologous bone marrow-derived stem-cell transfer in patients with st-segment elevation myocardial infarction: Double-blind, randomised controlled trial. Lancet 2006;367:113-21.PubMedCrossRefGoogle Scholar
  14. 14.
    Murry CE, Reinecke H, Pabon LM. Regeneration gaps: Observations on stem cells and cardiac repair. J Am Coll Cardiol 2006;47:1777-85.PubMedCrossRefGoogle Scholar
  15. 15.
    Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004;428:664-8.PubMedCrossRefGoogle Scholar
  16. 16.
    Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-5.PubMedCrossRefGoogle Scholar
  17. 17.
    Bartunek J, Vanderheyden M, Vandekerckhove B, Mansour S, De Bruyne B, De Bondt P, et al. Intracoronary injection of cd133-positive enriched bone marrow progenitor cells promotes cardiac recovery after recent myocardial infarction: Feasibility and safety. Circulation 2005;112:I178-83.PubMedGoogle Scholar
  18. 18.
    Beeres SL, Bax JJ, Dibbets P, Stokkel MP, Zeppenfeld K, Fibbe WE, et al. Effect of intramyocardial injection of autologous bone marrow-derived mononuclear cells on perfusion, function, and viability in patients with drug-refractory chronic ischemia. J Nucl Med 2006;47:574-80.PubMedGoogle Scholar
  19. 19.
    Beeres SL, Bax JJ, Kaandorp TA, Zeppenfeld K, Lamb HJ, Dibbets-Schneider P, et al. Usefulness of intramyocardial injection of autologous bone marrow-derived mononuclear cells in patients with severe angina pectoris and stress-induced myocardial ischemia. Am J Cardiol 2006;97:1326-31.PubMedCrossRefGoogle Scholar
  20. 20.
    Seeger FH, Zeiher AM, Dimmeler S. Cell-enhancement strategies for the treatment of ischemic heart disease. Nat Clin Pract Cardiovasc Med 2007;4:S110-3.PubMedCrossRefGoogle Scholar
  21. 21.
    Fuchs S, Satler LF, Kornowski R, Okubagzi P, Weisz G, Baffour R, et al. Catheter-based autologous bone marrow myocardial injection in no-option patients with advanced coronary artery disease: A feasibility study. J Am Coll Cardiol 2003;41:1721-4.PubMedCrossRefGoogle Scholar
  22. 22.
    Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003;107:2294-302.PubMedCrossRefGoogle Scholar
  23. 23.
    Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, et al. Paracrine action accounts for marked protection of ischemic heart by akt-modified mesenchymal stem cells. Nat Med 2005;11:367-8.PubMedCrossRefGoogle Scholar
  24. 24.
    Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 2005;111:2198-202.PubMedCrossRefGoogle Scholar
  25. 25.
    Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, et al. Mesenchymal stem cells modified with akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;9:1195-201.PubMedCrossRefGoogle Scholar
  26. 26.
    Wang QD, Sjoquist PO. Myocardial regeneration with stem cells: Pharmacological possibilities for efficacy enhancement. Pharmacol Res 2006;53:331-40.PubMedCrossRefGoogle Scholar
  27. 27.
    Aicher A, Brenner W, Zuhayra M, Badorff C, Massoudi S, Assmus B, et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation 2003;107:2134-9.PubMedCrossRefGoogle Scholar
  28. 28.
    Brenner W, Aicher A, Eckey T, Massoudi S, Zuhayra M, Koehl U, et al. 111in-labeled cd34+ hematopoietic progenitor cells in a rat myocardial infarction model. J Nucl Med 2004;45:512-8.PubMedGoogle Scholar
  29. 29.
    Jin Y, Kong H, Stodilka RZ, Wells RG, Zabel P, Merrifield PA, et al. Determining the minimum number of detectable cardiac-transplanted 111in-tropolone-labelled bone-marrow-derived mesenchymal stem cells by SPECT. Phys Med Biol 2005;50:4445-55.PubMedCrossRefGoogle Scholar
  30. 30.
    Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003;108:863-8.PubMedCrossRefGoogle Scholar
  31. 31.
    Chin BB, Nakamoto Y, Bulte JW, Pittenger MF, Wahl R, Kraitchman DL. 111in oxine labelled mesenchymal stem cell SPECT after intravenous administration in myocardial infarction. Nucl Med Commun 2003;24:1149-54.PubMedCrossRefGoogle Scholar
  32. 32.
    Blackwood KJ, Lewden B, Wells RG, Sykes J, Stodilka RZ, Wisenberg G, et al. In vivo SPECT quantification of transplanted cell survival after engraftment using (111)in-tropolone in infarcted canine myocardium. J Nucl Med 2009;50:927-35.PubMedCrossRefGoogle Scholar
  33. 33.
    Kraitchman DL, Tatsumi M, Gilson WD, Ishimori T, Kedziorek D, Walczak P, et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 2005;112:1451-61.PubMedCrossRefGoogle Scholar
  34. 34.
    Mitchell AJ, Sabondjian E, Sykes J, Deans L, Zhu W, Lu X, et al. Comparison of initial cell retention and clearance kinetics after subendocardial or subepicardial injections of endothelial progenitor cells in a canine myocardial infarction model. J Nucl Med 2010;51:413-7.PubMedCrossRefGoogle Scholar
  35. 35.
    Terrovitis J, Lautamaki R, Bonios M, Fox J, Engles JM, Yu J, et al. 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;54:1619-26.PubMedCrossRefGoogle Scholar
  36. 36.
    Bonios M, Terrovitis J, Chang CY, Engles JM, Higuchi T, Lautamaki R, et al. Myocardial substrate and route of administration determine acute cardiac retention and lung bio-distribution of cardiosphere-derived cells. J Nucl Cardiol 2011;18:443-50.PubMedCrossRefGoogle Scholar
  37. 37.
    Schachinger V, Aicher A, Dobert N, Rover R, Diener J, Fichtlscherer S, et al. Pilot trial on determinants of progenitor cell recruitment to the infarcted human myocardium. Circulation 2008;118:1425-32.PubMedCrossRefGoogle Scholar
  38. 38.
    Bengel FM, Schachinger V, Dimmeler S. Cell-based therapies and imaging in cardiology. Eur J Nucl Med Mol Imaging 2005;32:S404-16.PubMedCrossRefGoogle Scholar
  39. 39.
    Bulte JW. In vivo MRI cell tracking: Clinical studies. AJR Am J Roentgenol 2009;193:314-25.PubMedCrossRefGoogle Scholar
  40. 40.
    Hill JM, Dick AJ, Raman VK, Thompson RB, Yu ZX, Hinds KA, et al. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 2003;108:1009-14.PubMedCrossRefGoogle Scholar
  41. 41.
    Kraitchman DL, Heldman AW, Atalar E, Amado LC, Martin BJ, Pittenger MF, et al. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 2003;107:2290-3.PubMedCrossRefGoogle Scholar
  42. 42.
    Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, et al. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 2008;117:1555-62.PubMedCrossRefGoogle Scholar
  43. 43.
    Higuchi T, Anton M, Dumler K, Seidl S, Pelisek J, Saraste A, et al. Combined reporter gene PET and iron oxide MRI for monitoring survival and localization of transplanted cells in the rat heart. J Nucl Med 2009;50:1088-94.PubMedCrossRefGoogle Scholar
  44. 44.
    Wu JC, Chen IY, Sundaresan G, Min JJ, De A, Qiao JH, et al. Molecular imaging of cardiac cell transplantation in living animals using optical bioluminescence and positron emission tomography. Circulation 2003;108:1302-5.PubMedCrossRefGoogle Scholar
  45. 45.
    Wu JC, Spin JM, Cao F, Lin S, Xie X, Gheysens O, et al. Transcriptional profiling of reporter genes used for molecular imaging of embryonic stem cell transplantation. Physiol Genomics 2006;25:29-38.PubMedCrossRefGoogle Scholar
  46. 46.
    Bengel FM, Anton M, Avril N, Brill T, Nguyen N, Haubner R, et al. Uptake of radiolabeled 2′-fluoro-2′-deoxy-5-iodo-1-beta-d-arabinofuranosyluracil in cardiac cells after adenoviral transfer of the herpesvirus thymidine kinase gene: The cellular basis for cardiac gene imaging. Circulation 2000;102:948-50.PubMedGoogle Scholar
  47. 47.
    Cao F, Lin S, Xie X, Ray P, Patel M, Zhang X, et al. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 2006;113:1005-14.PubMedCrossRefGoogle Scholar
  48. 48.
    Miyagawa M, Beyer M, Wagner B, Anton M, Spitzweg C, Gansbacher B, et al. Cardiac reporter gene imaging using the human sodium/iodide symporter gene. Cardiovasc Res 2005;65:195-202.PubMedCrossRefGoogle Scholar
  49. 49.
    Terrovitis J, Kwok KF, Lautamaki R, Engles JM, Barth AS, Kizana E, et al. 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;52:1652-60.PubMedCrossRefGoogle Scholar
  50. 50.
    Zhang WY, Ebert AD, Narula J, Wu JC. Imaging cardiac stem cell therapy: Translations to human clinical studies. J Cardiovasc Transl Res 2011;4:514–22.PubMedCrossRefGoogle Scholar
  51. 51.
    Rodriguez-Porcel M, Brinton TJ, Chen IY, Gheysens O, Lyons J, Ikeno F, et al. Reporter gene imaging following percutaneous delivery in swine moving toward clinical applications. J Am Coll Cardiol 2008;51:595-7.PubMedCrossRefGoogle Scholar
  52. 52.
    Willmann JK, Paulmurugan R, Rodriguez-Porcel M, Stein W, Brinton TJ, Connolly AJ, et al. Imaging gene expression in human mesenchymal stem cells: From small to large animals. Radiology 2009;252:117-27.PubMedCrossRefGoogle Scholar
  53. 53.
    Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 2003;362:697-703.PubMedCrossRefGoogle Scholar
  54. 54.
    Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, et al. Progenitor cell trafficking is regulated by hypoxic gradients through hif-1 induction of sdf-1. Nat Med 2004;10:858-64.PubMedCrossRefGoogle Scholar
  55. 55.
    Lu L, Zhang JQ, Ramires FJ, Sun Y. Molecular and cellular events at the site of myocardial infarction: From the perspective of rebuilding myocardial tissue. Biochem Biophys Res Commun 2004;320:907-13.PubMedCrossRefGoogle Scholar
  56. 56.
    Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, et al. Hypoxia response elements in the aldolase a, enolase 1, and lactate dehydrogenase a gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 1996;271:32529-37.PubMedCrossRefGoogle Scholar
  57. 57.
    Wang GL, Semenza GL. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem 1993;268:21513-8.PubMedGoogle Scholar
  58. 58.
    Lodge MA, Bengel FM. Methodology for quantifying absolute myocardial perfusion with PET and SPECT. Curr Cardiol Rep 2007;9:121-8.PubMedCrossRefGoogle Scholar
  59. 59.
    Lautamaki R, Terrovitis J, Bonios M, Yu J, Tsui BM, Abraham MR, et al. Perfusion defect size predicts engraftment but not early retention of intra-myocardially injected cardiosphere-derived cells after acute myocardial infarction. Basic Res Cardiol 2011. doi:10.1007/s00395-011-0197-5. [Epub ahead of print].
  60. 60.
    Rodriguez-Porcel M, Cai W, Gheysens O, Willmann JK, Chen K, Wang H, et al. Imaging of VEGF receptor in a rat myocardial infarction model using PET. J Nucl Med 2008;49:667-73.PubMedCrossRefGoogle Scholar
  61. 61.
    Taki J, Higuchi T, Kawashima A, Tait JF, Muramori A, Matsunari I, et al. (99m)tc-annexin-v uptake in a rat model of variable ischemic severity and reperfusion time. Circ J 2007;71:1141-6.PubMedCrossRefGoogle Scholar
  62. 62.
    Su H, Spinale FG, Dobrucki LW, Song J, Hua J, Sweterlitsch S, et al. Noninvasive targeted imaging of matrix metalloproteinase activation in a murine model of postinfarction remodeling. Circulation 2005;112:3157-67.PubMedCrossRefGoogle Scholar
  63. 63.
    Higuchi T, Fukushima K, Xia J, Mathews WB, Lautamaki R, Bravo PE, et al. Radionuclide imaging of angiotensin ii type 1 receptor upregulation after myocardial ischemia-reperfusion injury. J Nucl Med 2010;51:1956-61.PubMedCrossRefGoogle Scholar
  64. 64.
    Sasano T, Abraham MR, Chang KC, Ashikaga H, Mills KJ, Holt DP, et al. Abnormal sympathetic innervation of viable myocardium and the substrate of ventricular tachycardia after myocardial infarction. J Am Coll Cardiol 2008;51:2266-75.PubMedCrossRefGoogle Scholar
  65. 65.
    Higuchi T, Bengel FM, Seidl S, Watzlowik P, Kessler H, Hegenloh R, et al. Assessment of alphavbeta3 integrin expression after myocardial infarction by positron emission tomography. Cardiovasc Res 2008;78:395-403.PubMedCrossRefGoogle Scholar

Copyright information

© American Society of Nuclear Cardiology 2011

Authors and Affiliations

  1. 1.Department of Nuclear MedicineHannover Medical SchoolHannoverGermany

Personalised recommendations