Novel bimodal iron oxide particles for efficient tracking of human neural stem cells in vivo

Nanomedicine

Volumn 10, Issue 16, 2015, Pages 2499-2512

  Aswendt, Markus ^a   Henn, Nadine ^a   Michalk, Stefanie ^a   Schneider, Gabriele ^a   Steiner, Mark Steven ^b   Bissa, Ursula ^b   Dose, Christian ^b   Hoehn, Mathias ^a,c,d  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b MILTENYI BIOTEC GMBH   (Germany)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d PERCUROS B V   (Netherlands)

Author keywords

bioluminescence imaging; cell tracking; iron oxide nanoparticle; MRI; neural stem cells

Indexed keywords

FERATRACK DIRECT VIO594 DYE; FERATRACK DIRECT VIO680 DYE; FERATRACK DIRECT VIO790 DYE; FIREFLY LUCIFERASE; FLUORESCENT DYE; IRON; SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG; FERRIC ION; FERRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CELL LABELING; CELL MIGRATION; CELL PROLIFERATION; CELL TRACKING; CELL VIABILITY; CONTROLLED STUDY; ENGRAFTMENT; FLUORESCENCE IMAGING; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MEASUREMENT; MICROSCOPY; MOLECULAR IMAGING; MOUSE; MR RELAXOMETRY; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SPECTROPHOTOMETRY; CHEMISTRY; CYTOLOGY;

FERRIC COMPOUNDS; HUMANS; NEURAL STEM CELLS;

EID: 84940536512     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.15.94     Document Type: Article

References (44)

1. Lindvall O, Kokaia Z. Stem cells in human neurodegenerative disorders - Time for clinical translation? J. Clin. Invest. 120(1), 29-40 (2010
2. Hoehn M, Wiedermann D, Justicia C., et al. Cell tracking using magnetic resonance imaging. J. Physiol. 584(Pt 1), 25-30 (2007
3. Bulte JW, Duncan ID, Frank JA. In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J. Cereb. Blood Flow. 22(8), 899-907 (2002
4. Weinstein JS, Varallyay CG, Dosa E., et al. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J. Cereb. Blood Flow. 30(1), 15-35 (2010
5. Stroh A, Faber C, Neuberger T., et al. In vivo detection limits of magnetically labeled embryonic stem cells in the rat brain using high-field (17.6 T) magnetic resonance imaging. NeuroImage. 24(3), 635-645 (2005
6. Himmelreich U, Hoehn M. Stem cell labeling for magnetic resonance imaging. Minim. Invasive Ther. Allied Technol. 17(2), 132-142 (2008
7. Kustermann E, Himmelreich U, Kandal K., et al. Efficient stem cell labeling for MRI studies. Contrast Media Mol. Imaging. 3(1), 27-37 (2008
8. Ketkar-Atre A, Struys T, Soenen SJ., et al. Variability in contrast agent uptake by different but similar stem cell types. Int. J. Nanomedicine. 8, 4577-4591 (2013
9. Soenen SJ, Himmelreich U, Nuytten N, De Cuyper M. Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials. 32(1), 195-205 (2011
10. 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. 6(7), 832-842 (2010
11. Ros PR, Freeny PC, Harms SE., et al. Hepatic MR imaging with ferumoxides: a multicenter clinical trial of the safety and efficacy in the detection of focal hepatic lesions. Radiology. 196(2), 481-488 (1995
12. Varallyay P, Nesbit G, Muldoon LL., et al. Comparison of two superparamagnetic viral-sized iron oxide particles ferumoxides and ferumoxtran-10 with a gadolinium chelate in imaging intracranial tumors. Am. J. Neuroradiol. 23(4), 510-519 (2002
13. Karussis D, Karageorgiou C, Vaknin-Dembinsky A., et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 67(10), 1187-1194 (2010
14. Cromer Berman SM, Walczak P, Bulte JW. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip. Rev. 3(4), 343-355 (2011
15. Neri M, Maderna C, Cavazzin C., et al. Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: relevance for in vivo cell tracking. Stem Cells. 26(2), 505-516 (2008
16. Panizzo RA, Gadian DG, Sowden JC, Wells JA, Lythgoe MF, Ferretti P. Monitoring ferumoxide-labelled neural progenitor cells and lesion evolution by magnetic resonance imaging in a model of cell transplantation in cerebral ischaemia. F1000 Res. 2, 252 (2013
17. Chang DJ, Moon H, Lee YH., et al. In vivo tracking of human neural stem cells following transplantation into a rodent model of ischemic stroke. Int. J. Stem Cells. 5(1), 79-83 (2012
18. Shen WB, Plachez C, Chan A., et al. Human neural progenitor cells retain viability, phenotype, proliferation, and lineage differentiation when labeled with a novel iron oxide nanoparticle, Molday ION Rhodamine B. Int. J. Nanomedicine. 8, 4593-4600 (2013
19. Hinds KA, Hill JM, Shapiro EM., et al. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood. 102(3), 867-872 (2003
20. Khurana A, Nejadnik H, Chapelin F., et al. Ferumoxytol: a new, clinically applicable label for stem-cell tracking in arthritic joints with MRI. Nanomedicine (Lond.) 8(12), 1969-1983 (2013
21. Thu MS, Bryant LH, Coppola T., et al. Self-Assembling nanocomplexes by combining ferumoxytol, heparin and protamine for cell tracking by magnetic resonance imaging. Nat. Med. 18(3), 463-467 (2012
22. Gutova M, Frank JA, D'apuzzo M., et al. Magnetic resonance imaging tracking of ferumoxytol-labeled human neural stem cells: studies leading to clinical use. Stem Cells Transl. Med. 2(10), 766-775 (2013
23. Miltenyi S, Muller W, Weichel W, Radbruch A. High gradient magnetic cell separation with MACS. Cytometry. 11(2), 231-238 (1990
24. Mouaziz H, Veyret R, Theretz A, Ginot F, Elaissari A. Aminodextran containing magnetite nanoparticles for molecular biology applications: preparation and evaluation. J. Biomed. Nanotechnol. 5(2), 172-181 (2009
25. 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. 7(2), 140-152 (2012
26. Aswendt M, Adamczak J, Couillard-Despres S, Hoehn M. Boosting bioluminescence neuroimaging: an optimized protocol for brain studies. PLoS ONE. 8(2), e55662 (2013
27. Tennstaedt A, Aswendt M, Adamczak J., et al. Human neural stem cell intracerebral grafts show spontaneous early neuronal differentiation after several weeks. Biomaterials. 44, 143-154 (2015
28. Berman SC, Galpoththawela C, Gilad AA, Bulte JW, Walczak P. Long-Term MR cell tracking of neural stem cells grafted in immunocompetent versus immunodeficient mice reveals distinct differences in contrast between live and dead cells. Magn. Resn. Med. 65(2), 564-574 (2011
29. Hoehn M, Kustermann E, Blunk J., et al. 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. USA. 99(25), 16267-16272 (2002
30. Lepore AC, Walczak P, Rao MS, Fischer I, Bulte JW. MR imaging of lineage-restricted neural precursors following transplantation into the adult spinal cord. Exper. Neurol. 201(1), 49-59 (2006
31. Chen CC, Ku MC, D MJ, Lai JS, Hueng DY, Chang C. Simple SPION incubation as an efficient intracellular labeling method for tracking neural progenitor cells using MRI. PLoS ONE. 8(2), e56125 (2013
32. Kallur T, Farr TD, Bohm-Sturm P, Kokaia Z, Hoehn M. Spatio-Temporal dynamics, differentiation and viability of human neural stem cells after implantation into neonatal rat brain. Eur. J. Neuroscience. 34(3), 382-393 (2011
33. De Temmerman ML, Soenen SJ, Symens N., et al. Magnetic layer-by-layer coated particles for efficient MRI of dendritic cells and mesenchymal stem cells. Nanomedicine (Lond.) 9(9), 1363-1376 (2014
34. Mcfadden C, Mallett CL, Foster PJ. Labeling of multiple cell lines using a new iron oxide agent for cell tracking by MRI. Contrast Media Mol. Imaging. 6(6), 514-522 (2011
35. Schwarz S, Wong JE, Bornemann J., et al. Polyelectrolyte coating of iron oxide nanoparticles for MRI-based cell tracking. Nanomedicine. 8(5), 682-691 (2012
36. Cromer Berman SM, Kshitiz, , Wang CJ., et al. Cell motility of neural stem cells is reduced after SPIO-labeling, which is mitigated after exocytosis. Magn. Resn. Med. 69(1), 255-262 (2013
37. Eamegdool SS, Weible MW 2nd, Pham BT, Hawkett BS, Grieve SM, Chan-Ling T. Ultrasmall superparamagnetic iron oxide nanoparticle prelabelling of human neural precursor cells. Biomaterials. 35(21), 5549-5564 (2014
38. Novotna B, Jendelova P, Kapcalova M., et al. Oxidative damage to biological macromolecules in human bone marrow mesenchymal stromal cells labeled with various types of iron oxide nanoparticles. Toxicol. Lett. 210(1), 53-63 (2012
39. Cianciaruso C, Pagani A, Martelli C., et al. Cellular magnetic resonance with iron oxide nanoparticles: long-Term persistence of SPIO signal in the CNS after transplanted cell death. Nanomedicine (Lond.) 9(10), 1457-1474 (2014
40. Magnitsky S, Walton RM, Wolfe JH, Poptani H. Magnetic resonance imaging as a tool for monitoring stem cell migration. Neurodegen. Dis. 4(4), 314-321 (2007
41. Bergwerf I, Tambuyzer B, De Vocht N., et al. Recognition of cellular implants by the brain's innate immune system. Immunol. Cell Biol. 89(4), 511-516 (2011
42. Tennstaedt A, Aswendt M, Adamczak J, Hoehn M. Noninvasive multimodal imaging of stem cell transplants in the brain using bioluminescence imaging and magnetic resonance imaging. Methods Mol. Biol. 1052, 153-166 (2013
43. Daadi MM, Li Z, Arac A., et al. Molecular and magnetic resonance imaging of human embryonic stem cellderived neural stem cell grafts in ischemic rat brain. Mol. Ther. 17(7), 1282-1291 (2009
44. Amemori T, Romanyuk N, Jendelova P., et al. Human conditionally immortalized neural stem cells improve locomotor function after spinal cord injury in the rat. Stem Cell Res. Ther. 4(3), 68 (2013