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

References

• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD . Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.
   PubMed Web of Science ®Google Scholar
• Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R. Mesenchymal stem cells for clinical application. Vox Sang. 2009;98:93–107.
   PubMedGoogle Scholar
• Abdallah BM, Kassem M. The use of mesenchymal (skeletal) stem cells for treatment of degenerative diseases: current status and future perspectives. J Cell Physiol. 2009; 218:9–12.
   PubMedGoogle Scholar
• Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105: 1815–22.
   PubMed Web of Science ®Google Scholar
• Granero-Molto F, Weis JA, Miga MI, Landis B, Myers TJ, O'Rear L . Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells. 2009;27: 1887–98.
   PubMed Web of Science ®Google Scholar
• LeBlanc K., Ringden O. Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr Opin Immunol. 2006;18:586–91.
   PubMed Web of Science ®Google Scholar
• Satija NK, Singh VK, Verma YK, Gupta P, Sharma S, Afrin F . Mesenchymal Stem Cell-based Therapy: A New Paradigm in Regenerative Medicine. J Cell Mol Med. 2009;13:4385–402.
   PubMed Web of Science ®Google Scholar
• Song L, Baksh D, Tuan RS. Mesenchymal stem cell-based cartilage tissue engineering: cells, scaffold and biology. Cytotherapy. 2004;6:596–601.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le Blanc K., Mueller I, Slaper-Cortenbach I, Marini F, Krause D . Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–17.
   PubMed Web of Science ®Google Scholar
• Bieback K, Kern S, Kocaomer A, Ferlik K, Bugert P. Comparing mesenchymal stromal cells from different human tissues: bone marrow, adipose tissue and umbilical cord blood. Biomed Mater Eng. 2008;18(Suppl 1):S71–6.
   Google Scholar
• Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, Silberstein LE. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006;24:1030–41.
   PubMed Web of Science ®Google Scholar
• Horwitz EM, Prather WR. Cytokines as the major mechanism of mesenchymal stem cell clinical activity: expanding the spectrum of cell therapy. Isr Med Assoc J. 2009;11:209–11.
   PubMed Web of Science ®Google Scholar
• Prather WR, Toren A, Meiron M, Ofir R, Tschope C, Horwitz EM. The role of placental-derived adherent stromal cell (PLX-PAD) in the treatment of critical limb ischemia. Cytotherapy. 2009;11:427–34.
   PubMed Web of Science ®Google Scholar
• Chen L, Tredget EE, Wu PY, Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS ONE. 2008;3:e1886.
   PubMed Web of Science ®Google Scholar
• Kassem M, Abdallah BM. Human bone-marrow-derived mesenchymal stem cells: biological characteristics and potential role in therapy of degenerative diseases. Cell Tissue Res. 2008;331:157–63.
   PubMed Web of Science ®Google Scholar
• European Comission. Directive 2001/83/EC of the European Parliament and of the Council of 6 November 2001 on the community code relating to medicinal products for human use. Offic J Eur Union. 2001;L311:67–128.
   Google Scholar
• European Comission. Commission Directive 2009/120/EC of 14 September 2009 amending Directive 2001/83/EC of the European Parliament and of the Council on the Community code relating to medicinal products for human use as regards advanced therapy medicinal products. Offic J Eur Union. 2009;52:3–12.
   Google Scholar
• Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H . 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
• 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
• Arbab AS, Yocum GT, Kalish H, Jordan EK, Anderson SA, Khakoo AY . Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood. 2004;104:1217–23.
   PubMed Web of Science ®Google Scholar
• Babic M, Horak D, Trchova M, Jendelova P, Glogarova K, Lesny P . Poly(L-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconjug Chem. 2008;19:740–50.
   PubMed Web of Science ®Google Scholar
• Bulte JW, Douglas T, Witwer B, Zhang SC, Strable E, Lewis BK . Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol. 2001;19:1141–7.
   PubMed Web of Science ®Google Scholar
• Bulte JW, Douglas T, Witwer B, Zhang SC, Lewis BK, van GP . Monitoring stem cell therapy in vivo using magnetodendrimers as a new class of cellular MR contrast agents. Acad Radiol. 2002;9 (Suppl 2):S332–5.
   Google Scholar
• Lorenz MR, Holzapfel V, Musyanovych A, Nothelfer K, Walther P, Frank H . Uptake of functionalized, fluorescent-labeled polymeric particles in different cell lines and stem cells. Biomaterials. 2006;27:2820–8.
   PubMed Web of Science ®Google Scholar
• Lorenz MR, Kohnle MV, Dass M, Walther P, Hocherl A, Ziener U . Synthesis of fluorescent polyisoprene nanoparticles and their uptake into various cells. Macromol Biosci. 2008;8:711–27.
   PubMed Web of Science ®Google Scholar
• Mailander V, Lorenz MR, Holzapfel V, Musyanovych A, Fuchs K, Wiesneth M . Carboxylated superparamagnetic iron oxide particles label cells intracellularly without transfection agents. Mol Imaging Biol. 2008;10:138–46.
   PubMed Web of Science ®Google Scholar
• Uchida M, Terashima M, Cunningham CH, Suzuki Y, Willits DA, Willis AF . A human ferritin iron oxide nano-composite magnetic resonance contrast agent. Magn Reson Med. 2008;60:1073–81.
   PubMed Web of Science ®Google Scholar
• Wilhelm C, Gazeau F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials. 2008;29:3161–74.
   PubMed Web of Science ®Google Scholar
• Nohroudi K, Arnhold S, Berhorn T, Addicks K, Hoehn M, Himmelreich U. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability. Cell Transplant. 2010;19:431–41.
   PubMedGoogle Scholar
• Wang HH, Wang YX, Leung KC, Au DW, Xuan S, Chak CP . Durable mesenchymal stem cell labelling by using polyhedral superparamagnetic iron oxide nanoparticles. Chemistry. 2009;15:12417–25.
   PubMedGoogle Scholar
• Schafer R, Kehlbach R, Wiskirchen J, Bantleon R, Pintaske J, Brehm BR . Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology. 2007;244:514–23.
   PubMed Web of Science ®Google Scholar
• Schafer R, Ayturan M, Bantleon R, Kehlbach R, Siegel G, Pintaske J . The use of clinically approved small particles of iron oxide (SPIO) for labeling of mesenchymal stem cells aggravates clinical symptoms in experimental autoimmune encephalomyelitis and influences their in vivo distribution. Cell Transplant. 2008;17:923–41.
   PubMed Web of Science ®Google Scholar
• Schafer R, Kehlbach R, Muller M, Bantleon R, Kluba T, Ayturan M . Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy. 2009;11:68–78.
   PubMed Web of Science ®Google Scholar
• Pawelczyk E, Arbab AS, Pandit S, Hu E, Frank JA. Expression of transferrin receptor and ferritin following ferumoxides-protamine sulfate labeling of cells: implications for cellular magnetic resonance imaging. NMR Biomed. 2006;19:581–92.
   PubMedGoogle Scholar
• Landfester K. Miniemulsion polymerization and the structure of polymer and hybrid nanoparticles. Angew Chem Int Ed Engl. 2009;48:4488–507.
   PubMed Web of Science ®Google Scholar
• Urban M, Musyanovych A, Landfester K. Fluorescent Superparamagnetic Polylactide Nanoparticles by Combination of Miniemulsion and Emulsion/Solvent Evaporation Techniques. Macromol Chem Phys. 2009;210:961–70.
   Web of Science ®Google Scholar
• Blackwood KA, McKean R, Canton I, Freeman CO, Franklin KL, Cole D . Development of biodegradable electrospun scaffolds for dermal replacement. Biomaterials. 2008;29: 3091–104.
   PubMed Web of Science ®Google Scholar
• Simamora P, Chern W. Poly-L-lactic acid: an overview. J Drugs Dermatol. 2006;5:436–40.
   PubMed Web of Science ®Google Scholar
• Jana NR, Chen Y, Peng X. Size- and Shape-Controlled Magnetic (Cr, Mn, Fe, Co, Ni) oxide nanocrystals via a simple and general approach. Chemistry of Materials. 2004;16:3931–5.
   Web of Science ®Google Scholar
• Rojewski M, Fekete N, Fürst D, Bourin P, Lotfi R, Mailander V . GMP-grade large scale expansion of bone marrow-derived human mesenchymal stem/stroma cells (MSC): Comparison of efficacy of different expansion systems and role of cytokines/chemokines. Blood. 2010;116:152.
   Google Scholar
• Rüster B, Gottig S, Ludwig RJ, Bistrian R, Muller S, Seifried E . Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood. 2006;108:3938–44.
   PubMed Web of Science ®Google Scholar
• Maby-El HH, Ame-Thomas P, Pangault C, Tribut O, DeVos J, Jean R . Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine-2,3 dioxygenase. Cancer Res. 2009;69:3228–37.
   PubMedGoogle Scholar
• Kuhlpeter R, Dahnke H, Matuszewski L, Persigehl T, von WA, Allkemper T . R2 and R2* mapping for sensing cell-bound superparamagnetic nanoparticles: in vitro and murine in vivo testing. Radiology. 2007;245:449–57.
   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
• Musyanovych A, Schmitz-Wienke J, Mailander V, Walther P, Landfester K. Preparation of biodegradable polymer nanoparticles by miniemulsion technique and their cell interactions. Macromol Biosci. 2008;8:127–39.
   PubMed Web of Science ®Google Scholar
• Weiss CK, Lorenz MR, Landfester K, Mailander V. Cellular uptake behavior of unfunctionalized and functionalized PBCA particles prepared in a miniemulsion. Macromol Biosci. 2007; 7:883–96.
   PubMedGoogle Scholar
• Dausend J, Musyanovych A, Dass M, Walther P, Schrezenmeier H, Landfester K . Uptake mechanism of oppositely charged fluorescent nanoparticles in HeLa cells. Macromol Biosci. 2008;8:1135–43.
   PubMed Web of Science ®Google Scholar
• JJu 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;24:611–17.
   PubMedGoogle Scholar
• Bulte JW, Zhang S, van GP, Herynek V, Jordan EK, Duncan ID . Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci USA. 1999;96:15256–61.
   PubMed Web of Science ®Google Scholar
• Bulte JW, Duncan ID, Frank JA. In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J Cereb Blood Flow Metab. 2002;22:899–907.
   PubMed Web of Science ®Google Scholar
• de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC . 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
• Walczak P, Kedziorek DA, Gilad AA, Barnett BP, Bulte JW. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: the case of the shiverer dysmyelinated mouse brain. Magn Reson Med. 2007;58:261–9.
   PubMed Web of Science ®Google Scholar
• Schafer R, Kehlbach R, Wiskirchen J, Bantleon R, Pintaske J, Brehm BR . Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology. 2007;244:514–23.
   PubMed Web of Science ®Google Scholar
• Wang J, Chen G, Pantopoulos K. Inhibition of transferrin receptor 1 transcription by a cell density response element. Biochem J. 2005;392:383–8.
   PubMedGoogle Scholar
• Boult J, Roberts K, Brookes MJ, Hughes S, Bury JP, Cross SS . Overexpression of cellular iron import proteins is associated with malignant progression of esophageal adenocarcinoma. Clin Cancer Res. 2008;14:379–87.
   PubMedGoogle Scholar
• Schaar DG, Medina DJ, Moore DF, Strair RK, Ting Y. miR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation. Exp Hematol. 2009;37:245–55.
   PubMed Web of Science ®Google Scholar
• Terszowski G, Waskow C, Conradt P, Lenze D, Koenigsmann J, Carstanjen D . Prospective isolation and global gene expression analysis of the erythrocyte colony-forming unit (CFU-E). Blood. 2005;105:1937–45.
   PubMed Web of Science ®Google Scholar
• Terunuma A, Kapoor V, Yee C, Telford WG, Udey MC, Vogel JC. Stem cell activity of human side population and alpha6 integrin-bright keratinocytes defined by a quantitative in vivo assay. Stem Cells. 2007;25:664–9.
   PubMedGoogle Scholar
• Beckmann J, Scheitza S, Wernet P, Fischer JC, Giebel B. Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood. 2007;109: 5494–501.
   PubMed Web of Science ®Google Scholar
• Hemadi M, Ha-Duong NT, El Hage Chahine JM. The mechanism of iron release from the transferrin-receptor 1 adduct. J Mol Biol. 2006;358:1125–36.
   PubMedGoogle Scholar
• Bayer Schering Pharma. Summary of Product Characteristics Resovist. 2007. http://www.fachinfo.de/data/fi/jsearch?praep. (visited on 2-8-2008).
   Google Scholar
• Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG . Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke. 2008;39:1569–74.
   PubMed Web of Science ®Google Scholar