Ultrastructural characterization of mesenchymal stromal cells labeled with ultrasmall superparamagnetic iron-oxide nanoparticles for clinical tracking studies

References

• Mathiasen AB, Haack-Sorensen M, Kastrup J. Mesenchymal stromal cells for cardiovascular repair: current status and future challenges. Future Cardiol 2009;5:605–17.
   PubMedGoogle Scholar
• Li L, Jiang W, Luo K, Song H, Lan F, Wu Y, Gu Z. Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking. Theranostics 2013;3:595–615.
   PubMed Web of Science ®Google Scholar
• Mathiasen AB, Kastrup J. Non-invasive in-vivo imaging of stem cells after transplantation in cardiovascular tissue. Theranostics 2013;3:561–72.
   PubMed Web of Science ®Google Scholar
• Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 2004;14:311–24.
   PubMed Web of Science ®Google Scholar
• Gangenahalli GU, Singh VK, Verma YK, Gupta P, Sharma RK, Chandra R, Luthra PM. Hematopoietic stem cell antigen CD34: role in adhesion or homing. Stem Cells Dev 2006;15:305–13.
   PubMed Web of Science ®Google Scholar
• Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H, Frank JA. Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 2003;229:838–46.
   PubMed Web of Science ®Google Scholar
• Song M, Moon WK, Kim Y, Lim D, Song IC, Yoon BW. Labeling efficacy of superparamagnetic iron oxide nanoparticles to human neural stem cells: comparison of ferumoxides, monocrystalline iron oxide, cross-linked iron oxide (CLIO)-NH2 and tat-CLIO. Korean J Radiol 2007;8:365–71.
   PubMed Web of Science ®Google Scholar
• Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JW, Frank JA. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation 2003;76:1123–30.
   PubMed Web of Science ®Google Scholar
• Frank JA, Miller BR, Arbab AS, Zywicke HA, Jordan EK, Lewis BK, Bryant LH, Jr., Bulte JW. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003;228:480–7.
   PubMed Web of Science ®Google Scholar
• Kaplan IM, Wadia JS, Dowdy SF. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 2005;102:247–53.
   PubMed Web of Science ®Google Scholar
• Rapoport M, Lorberboum-Galski H. TAT-based drug delivery system – new directions in protein delivery for new hopes? Expert Opin Drug Deliv 2009;6:453–63.
   PubMed Web of Science ®Google Scholar
• Pisanic TR, Blackwell JD, Shubayev VI, Finones RR, Jin S. Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials 2007;28:2572–81.
   PubMed Web of Science ®Google Scholar
• Wu X, Tan Y, Mao H, Zhang M. Toxic effects of iron oxide nanoparticles on human umbilical vein endothelial cells. Int J Nanomedicine 2010;5:385–99.
   PubMed Web of Science ®Google Scholar
• Josephson L, Tung CH, Moore A, Weissleder R. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug Chem 1999;10:186–91.
   PubMed Web of Science ®Google Scholar
• Friis T, Hansen AB, Houen G, Engel AM. Influence of angiogenesis inhibitors on endothelial cell morphology in vitro. APMIS 2006;114:211–24.
   PubMed Web of Science ®Google Scholar
• Eberl T, Salvenmoser W, Rieger G, Gorny I, Heiss V, Kumpitsch B, Gnaiger E, Margreiter R. Ultrastructural analysis of human endothelial cells after hypothermic storage in organ preservation solutions. J Surg Res 1999; 82:253–60.
   PubMed Web of Science ®Google Scholar
• Neil DA, Lynch SV, Hardie IR, Effeney DJ. Cold storage preservation and warm ischaemic injury to isolated arterial segments: endothelial cell injury. Am J Transplant 2002;2:400–9.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le BK, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8:315–7.
   PubMed Web of Science ®Google Scholar
• Mathiasen AB, Hansen L, Friis T, Thomsen C, Bhakoo K, Kastrup J. Optimal labeling dose, labeling time, and magnetic resonance imaging detection limits of ultrasmall superparamagnetic iron-oxide nanoparticle labeled mesenchymal stromal cells. Stem Cells Int 2013;2013:353105.
   PubMed Web of Science ®Google Scholar
• Auletta JJ, Bartholomew AM, Maziarz RT, Deans RJ, Miller RH, Lazarus HM, Cohen JA. The potential of mesenchymal stromal cells as a novel cellular therapy for multiple sclerosis. Immunotherapy 2012;4:529–47.
   PubMed Web of Science ®Google Scholar
• Friis T, Haack-Sorensen M, Mathiasen AB, Ripa RS, Kristoffersen US, Jorgensen E, Hansen L, Bindslev L, Kjaer A, Hesse B, Dickmeiss E, Kastrup J. Mesenchymal stromal cell derived endothelial progenitor treatment in patients with refractory angina. Scand Cardiovasc J 2011; 45:161–8.
   PubMed Web of Science ®Google Scholar
• Haack-Sorensen M, Friis T, Mathiasen AB, Jorgensen E, Hansen L, Dickmeiss E, Ekblond A, Kastrup J. Direct intramyocardial mesenchymal stromal cell injections in patients with severe refractory angina: one-year follow- up. Cell Transplant 2013;22:521–8.
   PubMed Web of Science ®Google Scholar
• Si YL, Zhao YL, Hao HJ, Fu XB, Han WD. MSCs: biological characteristics, clinical applications and their outstanding concerns. Ageing Res Rev 2011;10:93–103.
   PubMed Web of Science ®Google Scholar
• He G, Zhang H, Wei H, Wang Y, Zhang X, Tang Y, Wei Y, Hu S. In vivo imaging of bone marrow mesenchymal stem cells transplanted into myocardium using magnetic resonance imaging: a novel method to trace the transplanted cells. Int J Cardiol 2007;114:4–10.
   PubMed Web of Science ®Google Scholar
• Callera F, de Melo CM. Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells’ migration into the injured site. Stem Cells Dev 2007;16:461–6.
   PubMed Web of Science ®Google Scholar
• de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, Bulte JW, Scheenen TW, Punt CJ, Heerschap A, Figdor CG. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 2005;23:1407–13.
   PubMed Web of Science ®Google Scholar
• Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010;67:1187–94.
   PubMed Web of Science ®Google Scholar
• Toso C, Vallee JP, Morel P, Ris F, Demuylder-Mischler S, Lepetit-Coiffe M, Marangon N, Saudek F, James Shapiro AM, Bosco D, Berney T. Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant 2008;8:701–6.
   PubMed Web of Science ®Google Scholar
• Boutry S, Brunin S, Mahieu I, Laurent S, Vander EL, Muller RN. Magnetic labeling of non-phagocytic adherent cells with iron oxide nanoparticles: a comprehensive study. Contrast Media Mol Imaging 2008;3:223–32.
   PubMed Web of Science ®Google Scholar
• Chapon C, Jackson JS, Aboagye EO, Herlihy AH, Jones WA, Bhakoo KK. An in vivo multimodal imaging study using MRI and PET of stem cell transplantation after myocardial infarction in rats. Mol Imaging Biol 2009;11:31–8.
   PubMed Web of Science ®Google Scholar
• Ju S, Teng G, Zhang Y, Ma M, Chen F, Ni Y. In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magn Reson Imaging 2006;24:611–7.
   PubMed Web of Science ®Google Scholar
• Sun R, Dittrich J, Le-Huu M, Mueller MM, Bedke J, Kartenbeck J, Lehmann WD, Krueger R, Bock M, Huss R, Seliger C, Grone HJ, Misselwitz B, Semmler W, Kiessling F. Physical and biological characterization of superparamagnetic iron oxide- and ultrasmall superparamagnetic iron oxide-labeled cells: a comparison. Invest Radiol 2005;40:504–13.
   PubMed Web of Science ®Google Scholar
• Schmidtke-Schrezenmeier G, Urban M, Musyanovych A, Mailander V, Rojewski M, Fekete N, Menard C, Deak E, Tarte K, Rasche V, Landfester K, Schrezenmeier H. Labeling of mesenchymal stromal cells with iron oxide-poly(L-lactide) nanoparticles for magnetic resonance imaging: uptake, persistence, effects on cellular function and magnetic resonance imaging properties. Cytotherapy 2011;13:962–75.
   PubMed Web of Science ®Google Scholar
• Weissleder R, Stark DD, Engelstad BL, Bacon BR, Compton CC, White DL, Jacobs P, Lewis J. Superparamagnetic iron oxide: pharmacokinetics and toxicity. AJR Am J Roentgenol 1989;152:167–73.
   PubMed Web of Science ®Google Scholar
• Maia L, Landim-Alvarenga FC, Da Mota LS, De Assis GM, Laufer-Amorim R, De VB, Barberini DJ, Listoni AJ, De Moraes CN, Heckler MC, Amorim RM. Immunophenotypic, immunocytochemistry, ultrastructural, and cytogenetic characterization of mesenchymal stem cells from equine bone marrow. Microsc Res Tech 2013;76:618–24.
   PubMed Web of Science ®Google Scholar
• Schafer R, Bantleon R, Kehlbach R, Siegel G, Wiskirchen J, Wolburg H, Kluba T, Eibofner F, Northoff H, Claussen CD, Schlemmer HP. Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol 2010;11:22.
   PubMedGoogle Scholar
• Huang DM, Hsiao JK, Chen YC, Chien LY, Yao M, Chen YK, Ko BS, Hsu SC, Tai LA, Cheng HY, Wang SW, Yang CS, Chen YC. The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles. Biomaterials 2009;30:3645–51.
   PubMed Web of Science ®Google Scholar