Variability in contrast agent uptake by different but similar stem cell types

International Journal of Nanomedicine

Volumn 8, Issue , 2013, Pages 4577-4591

  Ketkar Atre, Ashwini ^a   Struys, Tom ^a,b   Soenen, Stefaan J ^c   Lambrichts, Ivo ^b   Verfaillie, Catherine M ^d   De Cuyper, Marcel ^d   Himmelreich, Uwe ^a  

^a DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^b HASSELT UNIVERSITY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Cell labeling; Iron oxide; Magnetic resonance imaging; Mesenchymal stem cells; MR contrast agents; Multipotent adult progenitor cells; Nanoparticles; Transmission electron microscopy

Indexed keywords

C 200; IRON; MAGNETOLIPOSOME; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL FATE; CELL LABELING; CELL METABOLISM; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DRUG UPTAKE; DYE DILUTION CURVE; ENDOCYTOSIS; INTERNALIZATION; MESENCHYMAL STEM CELL; MULTIPOTENT ADULT PROGENITOR CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; STEM CELL;

CELL LABELING; IRON OXIDE; MAGNETIC RESONANCE IMAGING; MESENCHYMAL STEM CELLS; MR CONTRAST AGENTS; MULTIPOTENT ADULT PROGENITOR CELLS; NANOPARTICLES; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CELL PROLIFERATION; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETITE NANOPARTICLES; MICE; RATS; STAINING AND LABELING; STEM CELLS;

EID: 84888586265     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S51588     Document Type: Article

References (54)

1. Guo QS, Zhu MY, Wang L, etal. Combined transfection of the three transcriptional factors, PDX-1, NeuroD1, and MafA, causes differentiation of bone marrow mesenchymal stem cells into insulin-producing cells. Exp Diabetes Res. 2012;2012:672013.
2. Jacobs SA, Pinxteren J, Roobrouck VD, etal. Human multipotent adult progenitor cells are non-immunogenic and exert potent immunomodulatory effects on alloreactive T cell responses. Cell Transplant. Epub October 1, 2012.
3. Mora-Lee S, Sirerol-Piquer MS, Gutiérrez-Pérez M, etal. Therapeutic effects of hMAPC and hMSC transplantation after stroke in mice. PLoS One. 2012;7(8):e43683.
4. Scheibe F, Ladhoff J, Huck J, etal. Immune effects of mesenchymal stromal cells in experimental stroke. J Cereb Blood Flow Metab. 2012;32(8):1578-1588.
5. Walker PA, Bedi SS, Shah SK, etal. Intravenous multipotent adult progenitor cell therapy after traumatic brain injury: modulation of the resident microglia population. J Neuroinflammation. 2012;9:228.
6. Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol. 2004;36(4): 568-584.
7. Pittenger MF, Mackay AM, Beck SC, etal. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143-147.
8. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105(1):93-98.
9. Jiang XX, Zhang Y, Liu B, etal. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005;105(10):4120-4126.
10. Wang M, Yang Y, Yang D, etal. The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology. 2009;126(2):220-232.
11. Jiang Y, Jahagirdar BN, Reinhardt RL, etal. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002;418(6893):41-49.
12. Sohni A, Verfaillie CM. Multipotent adult progenitor cells. Best Pract Res Clin Haematol. 2011;24(1):3-11.
13. Binas B, Verfaillie CM. Concise review: bone marrow meets blastocyst: lessons from an unlikely encounter. Stem Cells. 2012;31(4):620-626.
14. Lo Nigro A, Geraerts M, Notelaers T, etal. MAPC culture conditions support the derivation of cells with nascent hypoblast features from bone marrow and blastocysts. J Mol Cell Biol. 2012;4(6):423-426.
15. Cromer Berman SM, Walczak P, Bulte JW. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2011;3(4):343-355.
16. Himmelreich U, Hoehn M. Stem cell labeling for magnetic resonance imaging. Minim Invasive Ther Allied Technol. 2008;17(2):132-142.
17. Bulte JW, Arbab AS, Douglas T, Frank JA. Preparation of magnetically labeled cells for cell tracking by magnetic resonance imaging. Methods Enzymol. 2004;386:275-299.
18. Hoehn M, Küstermann E, Blunk J, etal. Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci U S A. 2002;99(25):16267-16272.
19. Hoshino K, Ly HQ, Frangioni JV, Hajjar RJ. In vivo tracking in cardiac stem cell-based therapy. Prog Cardiovasc Dis. 2007;49(6):414-420.
20. Zhang SJ, Wu JC. Comparison of imaging techniques for tracking cardiac stem cell therapy. J Nucl Med. 2007;48(12):1916-1919.
21. Adonai N, Nguyen KN, Walsh J, etal. Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography. Proc Natl Acad Sci U S A. 2002;99(5):3030-3035.
22. Connor DM, Benveniste H, Dilmanian FA, Kritzer MF, Miller LM, Zhong Z. Computed tomography of amyloid plaques in a mouse model of Alzheimer's disease using diffraction enhanced imaging. Neuroimage. 2009;46(4):908-914.
23. Chaudhari AJ, Darvas F, Bading JR, etal. Hyperspectral and multispectral bioluminescence optical tomography for small animal imaging. Phys Med Biol. 2005;50(23):5421-5441.
24. Himmelreich U, Dresselaers T. Cell labeling and tracking for experimental models using magnetic resonance imaging. Methods. 2009;48(2):112-124.
25. Neoh KG, Kang ET. Surface modification of magnetic nanoparticles for stem cell labeling. Soft Matter. 2012;8(7):2057-2069.
26. Küstermann E, Himmelreich U, Kandal K, etal. Efficient stem cell labeling for MRI studies. Contrast Media Mol Imaging. 2008;3(1):27-37.
27. Thorek DL, Tsourkas A. Size, charge and concentration dependent uptake of iron oxide particles by non-phagocytic cells. Biomaterials. 2008;29(26):3583-3590.
28. Breyer A, Estharabadi N, Oki M, etal. Multipotent adult progenitor cell isolation and culture procedures. Exp Hematol. 2006;34(11): 1596-1601.
29. Subramanian K, Geraerts M, Pauwelyn KA, etal. Isolation procedure and characterization of multipotent adult progenitor cells from rat bone marrow. Methods Mol Biol. 2010;636:55-78.
30. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood. 2004;103(5):1662-1668.
31. De Cuyper M, Joniau M. Magnetoliposomes. Formation and structural characterization. Eur Biophys J. 1988;15(5):311-319.
32. Soenen SJ, Vercauteren D, Braeckmans K, Noppe W, De Smedt S, De Cuyper M. Stable long-term intracellular labelling with fluorescently tagged cationic magnetoliposomes. Chembiochem. 2009;10(2): 257-267.
33. Crabbe A, Vandeputte C, Dresselaers T, etal. Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant. 2010;19(8): 919-936.
34. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63.
35. Struys T, Ketkar-Atre A, Gervois P, etal. Magnetic resonance imaging of human dental pulp stem cells in vitro and in vivo. Cell Transplant. Epub October 8, 2013.
36. Hodenius MA, Niendorf T, Krombach GA, etal. Synthesis, physicochemical characterization and MR relaxometry of aqueous ferrofluids. J Nanosci Nanotechnol. 2008;8(5):2399-2409.
37. Jung CW, Jacobs P. Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging. 1995;13(5):661-674.
38. Daldrup-Link HE, Meier R, Rudelius M, etal. In vivo tracking of genetically engineered, anti-HER2/neu directed natural killer cells to HER2/neu positive mammary tumors with magnetic resonance imaging. Eur Radiol. 2005;15(1):4-13.
39. Soenen SJ, Nuytten N, De Meyer SF, De Smedt SC, De Cuyper M. High intracellular iron oxide nanoparticle concentrations affect cellular cytoskeleton and focal adhesion kinase-mediated signaling. Small. 2010;6(7):832-842.
40. 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. 2004;17(7):513-517.
41. Pisanic TR 2nd, Blackwell JD, Shubayev VI, Fiñones RR, Jin S. Nanotoxicity of iron oxide nanoparticle internalization in growing neurons. Biomaterials. 2007;28(16):2572-2581.
42. Schäfer R, Kehlbach R, Wiskirchen J, etal. Transferrin receptor upregulation: in vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology. 2007;244(2):514-523.
43. 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(5):581-592.
44. Schäfer R, Kehlbach R, Müller M, etal. Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy. 2009;11(1):68-78.
45. 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(4):431-441.
46. Stroh A, Zimmer C, Gutzeit C, etal. Iron oxide particles for molecular magnetic resonance imaging cause transient oxidative stress in rat macrophages. Free Radic Biol Med. 2004;36(8):976-984.
47. Ulloa-Montoya F, Kidder BL, Pauwelyn KA, etal. Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol. 2007;8(8):R163.
48. Soenen SJ, Himmelreich U, Nuytten N, Pisanic TR 2nd, Ferrari A, De Cuyper M. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small. 2010;6(19):2136-2145.
49. Soenen SJ, Himmelreich U, Nuytten N, De Cuyper M. Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials. 2011;32(1):195-205.
50. Cohen B, Dafni H, Meir G, Harmelin A, Neeman M. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6glioma tumors. Neoplasia. 2005;7(2):109-117.
51. Soenen SJ, De Smedt SC, Braeckmans K. Limitations and caveats of magnetic cell labeling using transfection agent complexed iron oxide nanoparticles. Contrast Media Mol Imaging. 2012;7(2):140-152.
52. Rocker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol. 2009;4(9):577-580.
53. Soenen SJ, De Cuyper M. Assessing cytotoxicity of (iron oxide-based) nanoparticles: an overview of different methods exemplified with cationic magnetoliposomes. Contrast Media Mol Imaging. 2009;4(5):207-219.
54. Fayol D, Luciani N, Lartigue L, Gazeau F, Wilhelm C. Managing magnetic nanoparticle aggregation and cellular uptake: a precondition for efficient stem-cell differentiation and MRI tracking. Adv Healthc Mater. 2013;2(2):313-325.