Labeling of mesenchymal stromal cells with iron oxidepoly(l-lactide) nanoparticles for magnetic resonance imaging: Uptake, persistence, effects on cellular function and magnetic resonance imaging properties

Cytotherapy

Volumn 13, Issue 8, 2011, Pages 962-975

  Schmidtke Schrezenmeier, Gerlinde ^a   Urban, Markus ^b   Musyanovych, Anna ^b   Mailänder, Volker ^a,b   Rojewski, Markus ^a   Fekete, Natalie ^a   Menard, Cedric ^c,d   Deak, Erika ^e   Tarte, Karin ^c,d   Rasche, Volker ^a   Landfester, Katharina ^b   Schrezenmeier, Hubert ^a  

^a UNIVERSITY OF ULM   (Germany)

^b MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^c INSERM U917   (France)

^d PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

^e Institute of Transfusion Medicine and Immunohaematology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; AGAROSE; CD11B ANTIGEN; CD14 ANTIGEN; CD16 ANTIGEN; CD19 ANTIGEN; CD3 ANTIGEN; CD45 ANTIGEN; CD9 ANTIGEN; ENDOGLIN; HLA A ANTIGEN; HLA B ANTIGEN; HLA DR ANTIGEN; IRON OXIDE; IRON OXIDE POLYLACTIDE NANOPARTICLE; MICROSOMAL AMINOPEPTIDASE; NANOPARTICLE; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; POLYLACTIDE; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL FUNCTION; CELL LABELING; CELL PROLIFERATION; CELL VIABILITY; CLONOGENESIS; COLONY FORMING UNIT F; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOCHEMISTRY; ENDOSOME; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOASSAY; MESENCHYMAL STEM CELL; NONHUMAN; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARTICLE SIZE; PHANTOM; PHENOTYPE; PRIORITY JOURNAL; RAT; SHEAR STRESS; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL;

EID: 80051872276     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.3109/14653249.2011.571246     Document Type: Article

References (62)

1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-7. (Pubitemid 29282067)
2. Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R. Mesenchymal stem cells for clinical application. Vox Sang. 2009;98:93-107.
3. 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.
4. Aggarwal S, Pittenger MF. Human mesenchymal stem cellsmodulate allogeneic immune cell responses. Blood. 2005;105: 1815-22. (Pubitemid 40223708)
5. Granero-Molto F, Weis JA, Miga MI, Landis B, Myers TJ, O'Rear L et al. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells. 2009;27: 1887-98.
6. LeBlanc K., Ringden O. Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr Opin Immunol. 2006;18:586-91. (Pubitemid 44311450)
7. Satija NK, Singh VK, Verma YK, Gupta P, Sharma S, Afrin F et al. Mesenchymal Stem Cell-based Therapy: A New Paradigm in Regenerative Medicine. J Cell Mol Med. 2009;13:4385-402.
8. Song L, Baksh D, Tuan RS. Mesenchymal stem cell-based cartilage tissue engineering: cells, scaffold and biology. Cytotherapy. 2004;6:596-601. (Pubitemid 40028921)
9. Dominici M, Le Blanc K., Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al. Minimal criteria for defi ning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-17. (Pubitemid 44269669)
10. 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. (Pubitemid 351366863)
11. 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. (Pubitemid 44464736)
12. 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.
13. Prather WR, Toren A, Meiron M, Ofi r 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.
14. 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.
15. 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. (Pubitemid 350265499)
16. 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. Offi c J Eur Union. 2001;L311:67-128.
17. 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. Offi c J Eur Union. 2009;52:3-12.
18. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H et al. 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. (Pubitemid 37467591)
19. 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. (Pubitemid 37280845)
20. Arbab AS, Yocum GT, Kalish H, Jordan EK, Anderson SA, Khakoo AY et al. Effi cient magnetic cell labeling with protaminesulfate complexed to ferumoxides for cellular MRI. Blood. 2004;104:1217-23. (Pubitemid 39038047)
21. B abic M, Horak D, Trchova M, Jendelova P, Glogarova K, Lesny P et al. Poly(L-lysine)-modifi ed iron oxide nanoparticles for stem cell labeling. Bioconjug Chem. 2008;19:740-50. (Pubitemid 351431406)
22. Bulte JW, Douglas T, Witwer B, Zhang SC, Strable E, Lewis BK et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol. 2001;19:1141-7. (Pubitemid 33115700)
23. Bulte JW, Douglas T, Witwer B, Zhang SC, Lewis BK, van GP et al. 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. (Pubitemid 34857712)
24. Lorenz MR, Holzapfel V, Musyanovych A, Nothelfer K, Walther P, Frank H et al. Uptake of functionalized, fl uorescent- labeled polymeric particles in different cell lines and stem cells. Biomaterials. 2006;27:2820-8. (Pubitemid 43165751)
25. Lorenz MR, Kohnle MV, Dass M, Walther P, Hocherl A, Ziener U et al. Synthesis of fl uorescent polyisoprene nanoparticles and their uptake into various cells. Macromol Biosci. 2008;8:711-27.
26. Mailander V, Lorenz MR, Holzapfel V, Musyanovych A, Fuchs K, Wiesneth M et al. Carboxylated superparamagnetic iron oxide particles label cells intracellularly without transfection agents. Mol Imaging Biol. 2008;10:138-46.
27. Uchida M, Terashima M, Cunningham CH, Suzuki Y, Willits DA, Willis AF et al. A human ferritin iron oxide nanocomposite magnetic resonance contrast agent. Magn Reson Med. 2008;60:1073-81.
28. W ilhelm C, Gazeau F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials. 2008;29:3161-74.
29. 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.
30. Wang HH, Wang YX, Leung KC, Au DW, Xuan S, Chak CP et al. Durable mesenchymal stem cell labelling by using polyhedral superparamagnetic iron oxide nanoparticles. Chemistry. 2009;15:12417-25.
31. Schafer R, Kehlbach R, Wiskirchen J, Bantleon R, Pintaske J, Brehm BR et al. Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology. 2007;244:514-23. (Pubitemid 47080884)
32. Schafer R, Ayturan M, Bantleon R, Kehlbach R, Siegel G, Pintaske J et al. 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 infl uences their in vivo distribution. Cell Transplant. 2008;17:923-41.
33. Schafer R, Kehlbach R, Muller M, Bantleon R, Kluba T, Ayturan M et al. 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.
34. 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.
35. Landfester K. Miniemulsion polymerization and the structure of polymer and hybrid nanoparticles. Angew Chem Int Ed Engl. 2009;48:4488-507.
36. 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.
37. Blackwood KA, McKean R, Canton I, Freeman CO, Franklin KL, Cole D et al. Development of biodegradable electrospunscaffolds for dermal replacement. Biomaterials. 2008;29: 3091-104.
38. Simamora P, Chern W. Poly-L-lactic acid: an overview. J Drugs Dermatol. 2006;5:436-40.
39. 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.
40. Rojewski M, Fekete N, Fürst D, Bourin P, Lotfi R, Mailander V et al. GMP-grade large scale expansion of bone marrowderived human mesenchymal stem/stroma cells (MSC): Comparison of effi cacy of different expansion systems and role of cytokines/chemokines. Blood. 2010;116:152.
41. Rüster B, Gottig S, Ludwig RJ, Bistrian R, Muller S, Seifried E et al. Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood. 2006;108:3938-44. (Pubitemid 44864580)
42. Maby-El HH, Ame-Thomas P, Pangault C, Tribut O, DeVos J, Jean R et al. Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine- 2,3 dioxygenase. Cancer Res. 2009;69:3228-37.
43. Kuhlpeter R, Dahnke H, Matuszewski L, Persigehl T, von WA, Allkemper T et al. R2 and R2? mapping for sensing cellbound superparamagnetic nanoparticles: in vitro and murine in vivo testing. Radiology. 2007;245:449-57. (Pubitemid 47612526)
44. 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.
45. 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.
46. 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. (Pubitemid 47237499)
47. Dausend J, Musyanovych A, Dass M, Walther P, Schrezenmeier H, Landfester K et al. Uptake mechanism of oppositely charged fl uorescent nanoparticles in HeLa cells. Macromol Biosci. 2008;8:1135-43.
48. 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. (Pubitemid 43776561)
49. Bulte JW, Zhang S, van GP, Herynek V, Jordan EK, Duncan ID et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci USA. 1999;96:15256-61. (Pubitemid 30019799)
50. 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. (Pubitemid 34831596)
51. de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol. 2005;23:1407-13. (Pubitemid 41679393)
52. 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. (Pubitemid 47267643)
53. Schafer R, Kehlbach R, Wiskirchen J, Bantleon R, Pintaske J, Brehm BR et al. Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology. 2007;244:514-23. (Pubitemid 47080884)
54. Wang J, Chen G, Pantopoulos K. Inhibition of transferring receptor 1 transcription by a cell density response element. Biochem J. 2005;392:383-8. (Pubitemid 41796527)
55. Boult J, Roberts K, Brookes MJ, Hughes S, Bury JP, Cross SS et al. Overexpression of cellular iron import proteins is associated with malignant progression of esophageal adenocarcinoma. Clin Cancer Res. 2008;14:379-87. (Pubitemid 351226104)
56. 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.
57. Terszowski G, Waskow C, Conradt P, Lenze D, Koenigsmann J, Carstanjen D et al. Prospective isolation and global gene expression analysis of the erythrocyte colony-forming unit (CFU-E). Blood. 2005;105:1937-45. (Pubitemid 40731775)
58. Terunuma A, Kapoor V, Yee C, Telford WG, Udey MC, Vogel JC. Stem cell activity of human side population and alpha6 integrin-bright keratinocytes defi ned by a quantitative in vivo assay. Stem Cells. 2007;25:664-9. (Pubitemid 46354225)
59. Beckmann J, Scheitza S, Wernet P, Fischer JC, Giebel B. Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identifi cation of asymmetrically segregating proteins. Blood. 2007;109: 5494-501. (Pubitemid 46890575)
60. 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. (Pubitemid 44382446)
61. Bayer Schering Pharma. Summary of Product Characteristics Resovist. 2007. www.fachinfo.de/data/fi /jsearch?praep. (visited on 2-8-2008).
62. Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG et al. Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke. 2008;39:1569-74.