Stem cell labeling for noninvasive delivery and tracking in cardiovascular regenerative therapy

References

• Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature451(7181), 937–942 (2008).
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science284(5411), 143–147 (1999).
   PubMed Web of Science ®Google Scholar
• Orlic D, Hill JM, Arai AE. Stem cells for myocardial regeneration. Circ. Res.91(12), 1092–1102 (2002).
   PubMed Web of Science ®Google Scholar
• Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med.9(6), 702–712 (2003).
   PubMed Web of Science ®Google Scholar
• Abdel-Latif A, Bolli R, Tleyjeh IM et al. Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis. Arch. Intern. Med.167(10), 989–997 (2007).
   PubMed Web of Science ®Google Scholar
• Fan L, Chen L, Chen X, Fu F. A meta-analysis of stem cell mobilization by granulocyte colony-stimulating factor in the treatment of acute myocardial infarction. Cardiovasc. Drugs Ther.22(1), 45–54 (2008).
   PubMed Web of Science ®Google Scholar
• Zhang SN, Sun AJ, Ge JB et al. Intracoronary autologous bone marrow stem cells transfer for patients with acute myocardial infarction: a meta-analysis of randomised controlled trials. Int. J. Cardiol. (2008).
   Google Scholar
• Singh S, Arora R, Handa K et al. Stem cells improve left ventricular function in acute myocardial infarction. Clin. Cardiol.32(4), 176–180 (2009).
   PubMed Web of Science ®Google Scholar
• Lipinski MJ, Biondi-Zoccai GG, Abbate A et al. Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials. J. Am. Coll. Cardiol.50(18), 1761–1767 (2007).
   PubMed Web of Science ®Google Scholar
• Martin-Rendon E, Brunskill S, Hyde C et al. Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review. Eur. Heart J.29, 1807–1818 (2008).
   PubMed Web of Science ®Google Scholar
• Schachinger V, Erbs S, Elsasser A et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med.355(12), 1210–1221 (2006).
   PubMed Web of Science ®Google Scholar
• Wollert KC, Meyer GP, Lotz J et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet364(9429), 141–148. (2004).
   PubMed Web of Science ®Google Scholar
• Meyer GP, Wollert KC, Lotz J et al. Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months’ follow-up data from the randomized, controlled BOOST (Bone Marrow Transfer to Enhance ST-Elevation Infarct Regeneration) trial. Circulation113(10), 1287–1294 (2006).
   PubMed Web of Science ®Google Scholar
• Schaefer A, Meyer GP, Fuchs M et al. Impact of intracoronary bone marrow cell transfer on diastolic function in patients after acute myocardial infarction: results from the BOOST trial. Eur. Heart J.27(8), 929–935 (2006).
   PubMed Web of Science ®Google Scholar
• Tendera M, Wojakowski W, Ruzyllo W et al. Intracoronary infusion of bone marrow-derived selected CD34+CXCR4+ cells and non-selected mononuclear cells in patients with acute STEMI and reduced left ventricular ejection fraction: results of the randomized, multicentre Myocardial Regeneration by Intracoronary Infusion of Selected Populations of Stem Cells in Acute Myocardial Infarction (REGENT) trial. Eur. Heart J.30, 1313–1321 (2009).
   PubMed Web of Science ®Google Scholar
• Sanchez PL, San Roman JA, Villa A, Fernandez ME, Fernandez-Aviles F. Contemplating the bright future of stem cell therapy for cardiovascular disease. Nat. Clin. Pract. Cardiovasc. Med.3(Suppl. 1), S138–S151 (2006).
   Google Scholar
• Tang YL, Zhao Q, Zhang YC et al. Autologous mesenchymal stem cell transplantation induce VEGF and neovascularization in ischemic myocardium. Regul. Pept.117(1), 3–10 (2004).
   PubMed Web of Science ®Google Scholar
• Dawn B, Bolli R. Adult bone marrow-derived cells: regenerative potential, plasticity, and tissue commitment. Basic Res. Cardiol.100(6), 494–503 (2005).
   PubMed Web of Science ®Google Scholar
• Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature410(6829), 701–705 (2001).
   PubMed Web of Science ®Google Scholar
• Zhang M, Methot D, Poppa V et al. Cardiomyocyte grafting for cardiac repair: graft cell death and anti-death strategies. J. Mol. Cell. Cardiol.33(5), 907–921 (2001).
   PubMed Web of Science ®Google Scholar
• Frank JA, Zywicke H, Jordan EK et al. Magnetic intracellular labeling of mammalian cells by combining (FDA-approved) superparamagnetic iron oxide MR contrast agents and commonly used transfection agents. Acad. Radiol.9, S484-S487 (2002).
   PubMed Web of Science ®Google Scholar
• Zhou R, Acton PD, Ferrari VA. Imaging stem cells implanted in infarcted myocardium. J. Am. Coll. Cardiol.48(10), 2094–2106 (2006).
   PubMed Web of Science ®Google Scholar
• Sutton EJ, Henning TD, Pichler BJ, Bremer C, Daldrup-Link HE. Cell tracking with optical imaging. Eur. Radiol.18(10), 2021–2032 (2008).
   PubMed Web of Science ®Google Scholar
• Lin S, Xie X, Patel MR et al. Quantum dot imaging for embryonic stem cells. BMC Biotechnol.7, 67 (2007).
   PubMed Web of Science ®Google Scholar
• Slotkin JR, Chakrabarti L, Dai HN et al. In vivo quantum dot labeling of mammalian stem and progenitor cells. Dev. Dyn.236(12), 3393–3401 (2007).
   PubMed Web of Science ®Google Scholar
• Muller-Borer BJ, Collins MC, Gunst PR, Cascio WE, Kypson AP. Quantum dot labeling of mesenchymal stem cells. J. Nanobiotechnology5, 9 (2007).
   PubMedGoogle Scholar
• Rota M, Kajstura J, Hosoda T et al. Bone marrow cells adopt the cardiomyogenic fate in vivo. Proc. Natl Acad. Sci. USA104(45), 17783–17788 (2007).
   PubMed Web of Science ®Google Scholar
• Medintz IL, Uyeda HT, Goldman ER, Mattoussi H. Quantum dot bioconjugates for imaging, labelling and sensing. Nat. Mater.4(6), 435–446 (2005).
   PubMed Web of Science ®Google Scholar
• Rosen AB, Kelly DJ, Schuldt AJ et al. Finding fluorescent needles in the cardiac haystack: tracking human mesenchymal stem cells labeled with quantum dots for quantitative in vivo three-dimensional fluorescence analysis. Stem Cells25(8), 2128–2138 (2007).
   PubMed Web of Science ®Google Scholar
• Shah BS, Clark PA, Moioli EK, Stroscio MA, Mao JJ. Labeling of mesenchymal stem cells by bioconjugated quantum dots. Nano Lett.7(10), 3071–3079 (2007).
   PubMed Web of Science ®Google Scholar
• Hoshino K, Ly HQ, Frangioni JV, Hajjar RJ. in vivo tracking in cardiac stem cell-based therapy. Prog. Cardiovasc. Dis.49(6), 414–420 (2007).
   PubMed Web of Science ®Google Scholar
• Kraitchman DL, Bulte JW. Imaging of stem cells using MRI. Basic Res. Cardiol.103(2), 105–113 (2008).
   PubMed Web of Science ®Google Scholar
• Bulte JW, Kraitchman DL. Monitoring cell therapy using iron oxide MR contrast agents. Curr. Pharm. Biotechnol.5(6), 567–584 (2004).
   PubMed Web of Science ®Google Scholar
• Arbab AS, Yocum GT, Kalish H et al. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood104(4), 1217–1223 (2004).
   PubMed Web of Science ®Google Scholar
• Walczak P, Kedziorek D, Gilad AA, Lin S, Bulte JW. Instant MR labeling of stem cells using magnetoelectroporation. Magn. Reson. Med. (54), 769–774 (2005).
   PubMed Web of Science ®Google Scholar
• Arbab AS, Bashaw LA, Miller BR et al. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation76(7), 1123–1130. (2003).
   PubMed Web of Science ®Google Scholar
• Zhu J, Zhou L, XingWu F. Tracking neural stem cells in patients with brain trauma. N. Engl. J. Med.355(22), 2376–2378 (2006).
   PubMed Web of Science ®Google Scholar
• Kraitchman DL, Heldman AW, Atalar E et al. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation107(18), 2290–2293 (2003).
   PubMed Web of Science ®Google Scholar
• Dick AJ, Guttman MA, Raman VK et al. Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in swine. Circulation108(23), 2899–2904 (2003).
   PubMed Web of Science ®Google Scholar
• Kraitchman DL, Gilson WD, Lorenz CH. Stem cell therapy: MRI guidance and monitoring. J. Magn. Reson. Imaging27(2), 299–310 (2008).
   PubMed Web of Science ®Google Scholar
• de Silva R, Gutierrez LF, Raval AN et al. X-ray fused with magnetic resonance imaging (XFM) to target endomyocardial injections. validation in a swine model of myocardial infarction. Circulation114(22), 2342–2350 (2006).
   PubMed Web of Science ®Google Scholar
• Arbab AS, Yocum GT, Rad AM et al. Labeling of cells with ferumoxides-protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR Biomed.18(8), 553–559 (2005).
   PubMed Web of Science ®Google Scholar
• Arbab AS, Bashaw LA, Miller BR et al. Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology229(3), 838–846 (2003).
   PubMed Web of Science ®Google Scholar
• Kostura L, Kraitchman DL, Mackay AM, Pittenger MF, Bulte JW. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed.17(7), 513–517 (2004).
   PubMed Web of Science ®Google Scholar
• Chen YC, Hsiao JK, Liu HM et al. The inhibitory effect of superparamagnetic iron oxide nanoparticle (Ferucarbotran) on osteogenic differentiation and its signaling mechanism in human mesenchymal stem cells. Toxicol. Appl. Pharmacol.245(2), 272–279 (2010).
   PubMed Web of Science ®Google Scholar
• Pawelczyk E, Arbab AS, Chaudhry A et al. In vitro model of bromodeoxyuridine or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: implications for cellular therapy. Stem Cells26(5), 1366–1375 (2008).
   PubMed Web of Science ®Google Scholar
• Siglienti I, Bendszus M, Kleinschnitz C, Stoll G. Cytokine profile of iron-laden macrophages: implications for cellular magnetic resonance imaging. J. Neuroimmunol.173(1–2), 166–173 (2006).
   PubMed Web of Science ®Google Scholar
• Walczak P, Kedziorek DA, Gilad AA, Lin S, Bulte JW. Instant MR labeling of stem cells using magnetoelectroporation. Magn. Reson. Med54(4), 769–774 (2005).
   PubMed Web of Science ®Google Scholar
• Kedziorek DA, Gilson WD, Stuber M et al. Mesenchymal stem cell therapy in a rabbit hindlimb ischemia model. J. Am. Coll. Cardiol.49(9), 362A (2007).
   Google Scholar
• Stuber M, Gilson WD, Schär M et al. Positive contrast visualization of iron oxide-labeled stem cells using inversion recovery with ON-resonant water suppression (IRON). Magn. Reson. Med.58, 1072–1077 (2007).
   PubMed Web of Science ®Google Scholar
• Foster-Gareau P, Heyn C, Alejski A, Rutt BK. Imaging single mammalian cells with a 1.5 T clinical MRI scanner. Magn. Reson. Med.49(5), 968–971 (2003).
   PubMed Web of Science ®Google Scholar
• Heyn C, Bowen CV, Rutt BK, Foster PJ. Detection threshold of single SPIO-labeled cells with FIESTA. Magn. Reson. Med.53(2), 312–320 (2005).
   PubMed Web of Science ®Google Scholar
• Mangi AA, Noiseux N, Kong D et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med.9(9), 1195–1201 (2003).
   PubMed Web of Science ®Google Scholar
• Ebert SN, Taylor DG, Nguyen HL et al. Noninvasive tracking of cardiac embryonic stem cells in vivo using magnetic resonance imaging techniques. Stem Cells25(11), 2936–2944 (2007).
   PubMed Web of Science ®Google Scholar
• Amsalem Y, Mardor Y, Feinberg MS et al. Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation116(Suppl. 11), I38–45 (2007).
   PubMed Web of Science ®Google Scholar
• Terrovitis J, Stuber M, Youssef A et al. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation117(12), 1555–1562 (2008).
   PubMed Web of Science ®Google Scholar
• Stuckey DJ, Carr CA, Martin-Rendon E et al. Iron particles for noninvasive monitoring of bone marrow stromal cell engraftment into, and isolation of viable engrafted donor cells from, the heart. Stem Cells24(8), 1968–1975 (2006).
   PubMed Web of Science ®Google Scholar
• Partlow KC, Chen J, Brant JA et al.19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J.21(8), 1647–1654 (2007).
   PubMed Web of Science ®Google Scholar
• Ruiz-Cabello J, Walczak P, Kedziorek DA et al. In vivo ‘hot spot’ MR imaging of neural stem cells using fluorinated nanoparticles. Magn. Reson. Med.60(6), 1506–1511 (2008).
   PubMed Web of Science ®Google Scholar
• Srinivas M, Morel PA, Ernst LA, Laidlaw DH, Ahrens ET. Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn. Reson. Med.58(4), 725–734 (2007).
   PubMed Web of Science ®Google Scholar
• Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation108(7), 863–868 (2003).
   PubMed Web of Science ®Google Scholar
• Kraitchman DL, Tatsumi M, Gilson WD et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation112(10), 1451–1461 (2005).
   PubMed Web of Science ®Google Scholar
• Simonova M, Shtanko O, Sergeyev N, Weissleder R, Bogdanov A Jr. Engineering of technetium-99m-binding artificial receptors for imaging gene expression. J. Gene Med.5(12), 1056–1066 (2003).
   PubMed Web of Science ®Google Scholar
• Thakur ML, Segal AW, Louis L et al. Indium-111-labeled cellular blood components: mechanism of labeling and intracellular location in human neutrophils. J. Nucl. Med.18(10), 1022–1026. (1977).
   PubMed Web of Science ®Google Scholar
• Thakur ML, Segal AW, Louis L et al. Indium-111-labeled cellular blood components: mechanism of labeling and intracellular location in human neutrophils. J. Nucl. Med.18(10), 1022–1026 (1977).
   PubMed Web of Science ®Google Scholar
• Jin Y, Kong H, Stodilka RZ et al. Determining the minimum number of detectable cardiac-transplanted 111In-tropolone-labelled bone-marrow-derived mesenchymal stem cells by SPECT. Phys. Med. Biol.50(19), 4445–4455 (2005).
   PubMed Web of Science ®Google Scholar
• Chin BB, Nakamoto Y, Bulte JW et al.111In oxine labelled mesenchymal stem cell SPECT after intravenous administration in myocardial infarction. Nucl. Med. Commun.24(11), 1149–1154. (2003).
   PubMed Web of Science ®Google Scholar
• Brenner W, Aicher A, Eckey T et al.111In-labeled CD34+ hematopoietic progenitor cells in a rat myocardial infarction model. J. Nucl. Med.45(3), 512–518. (2004).
   PubMed Web of Science ®Google Scholar
• Aicher A, Brenner W, Zuhayra M et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation107(16), 2134–2139 (2003).
   PubMed Web of Science ®Google Scholar
• Hou D, Youssef EA, Brinton TJ et al. Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery: implications for current clinical trials. Circulation112(Suppl. 9), I150–I156 (2005).
   PubMed Web of Science ®Google Scholar
• Doyle B, Kemp BJ, Chareonthaitawee P et al. Dynamic tracking during intracoronary injection of 18F-FDG-labeled progenitor cell therapy for acute myocardial infarction. J. Nucl. Med.48(10), 1708–1714 (2007).
   PubMed Web of Science ®Google Scholar
• Freyman T, Polin G, Osman H et al. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur. Heart J.27(9), 1114–1122 (2006).
   PubMed Web of Science ®Google Scholar
• Hofmann M, Wollert KC, Meyer GP et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation111(17), 2198–2202 (2005).
   PubMed Web of Science ®Google Scholar
• Kang WJ, Kang HJ, Kim HS et al. Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction. J. Nucl. Med.47(8), 1295–1301 (2006).
   PubMed Web of Science ®Google Scholar
• Gholamrezanezhad A, Mirpour S, Ardekani JM et al. Cytotoxicity of 111In-oxine on mesenchymal stem cells: a time-dependent adverse effect. Nucl. Med. Commun.30(3), 210–216 (2009).
   PubMed Web of Science ®Google Scholar
• Adonai N, Nguyen KN, Walsh J et al. Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography. Proc. Natl Acad. Sci. USA99(5), 3030–3035 (2002).
   PubMed Web of Science ®Google Scholar
• Pawelczyk E, Jordan EK, Balakumaran A et al. In vivo transfer of intracellular labels from locally implanted bone marrow stromal cells to resident tissue macrophages. PLoS One4(8), e6712 (2009).
   PubMed Web of Science ®Google Scholar
• Lim F, Sun AM. Microencapsulated islets as bioartificial endocrine pancreas. Science210(4472), 908–910 (1980).
   PubMed Web of Science ®Google Scholar
• Willmann JK, Paulmurugan R, Rodriguez-Porcel M et al. Imaging gene expression in human mesenchymal stem cells: from small to large animals. Radiology252(1), 117–127 (2009).
   PubMed Web of Science ®Google Scholar
• Barnett BP, Arepally A, Karmarkar PV et al. Magnetic resonance-guided, real-time targeted delivery and imaging of magnetocapsules immunoprotecting pancreatic islet cells. Nat. Med.13(8), 986–991 (2007).
   PubMed Web of Science ®Google Scholar
• Barnett BP, Kraitchman DL, Lauzon C et al. Radiopaque alginate microcapsules for x-ray visualization and immunoprotection of cellular therapeutics. Mol. Pharm.3(5), 531–538 (2006).
   PubMedGoogle Scholar
• Fu YL, Kedziorek D, Crisostomo V et al. Perfluorocarbon microcapsules for x-ray visualization of mesenchymal stem cell delivery and engraftment. Circulation118, S519 (2008).
   Google Scholar
• Cosby KM, Hofmann LV, Barnett BP et al. A novel radio-opaque barium/alginate microencapsulation technique for allogeneic mesenchymal stem cell delivery and localization. J. Cardiovasc. Magn. Reson.9(2) (2007).
   Google Scholar
• Kraitchman DL, Arepally A, Barnett BP et al. An x-ray visible microencapsulation method to enhance delivery and engraftment of allogeneic stem cells for cardiovascular applications. Contrast Media Mol. Imaging2(6), 294 (2007).
   Google Scholar
• Fu Y, Kedziorek D, Ouwerkerk R et al. Multifunctional perfluorooctylbromide alginate microcapsules for monitoring of mesenchymal stem cell delivery using CT and MRI. J. Cardiovasc. Magn. Reson.11(Suppl. 1), O7 (2009).
   PubMedGoogle Scholar
• Nahrendorf M, Sosnovik D, French B et al. Multimodality cardiovascular molecular imaging – part II. Circ. Cardiovasc. Imaging2, 56–70 (2009).
   PubMed Web of Science ®Google Scholar
• Khattak SF, Chin KS, Bhatia SR, Roberts SC. Enhancing oxygen tension and cellular function in alginate cell encapsulation devices through the use of perfluorocarbons. Biotechnol. Bioeng.96(1), 156–166 (2007).
   PubMed Web of Science ®Google Scholar
• Leor J, Gerecht S, Cohen S et al. Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart93(10), 1278–1284 (2007).
   PubMed Web of Science ®Google Scholar
• Crisostomo PR, Wang M, Markel TA et al. Stem cell mechanisms and paracrine effects: potential in cardiac surgery. Shock28(4), 375–383 (2007).
   PubMed Web of Science ®Google Scholar
• Du YY, Zhou SH, Zhou T et al. Immuno-inflammatory regulation effect of mesenchymal stem cell transplantation in a rat model of myocardial infarction. Cytotherapy10(5), 469–478 (2008).
   PubMed Web of Science ®Google Scholar
• Doyle B, Sorajja P, Hynes B et al. Progenitor cell therapy in a porcine acute myocardial infarction model induces cardiac hypertrophy, mediated by paracrine secretion of cardiotrophic factors including TGFβ1. Stem Cells Dev.17(5), 941–951 (2008).
   PubMed Web of Science ®Google Scholar
• Zhang SJ, Wu JC. Comparison of imaging techniques for tracking cardiac stem cell therapy. J. Nucl. Med.48(12), 1916–1919 (2007).
   PubMed Web of Science ®Google Scholar