Focused Magnetic Stem Cell Targeting to the Retina Using Superparamagnetic Iron Oxide Nanoparticles

Cell Transplantation

Volumn 21, Issue 6, 2012, Pages 1137-1148

  Yanai, Anat ^a   Häfeli, Urs O ^a   Metcalfe, Andrew L ^a   Soema, Peter ^a   Addo, Lois ^a   Gregory Evans, Cheryl Y ^a   Po, Kelvin ^a   Shan, Xianghong ^a   Moritz, Orson L ^a   Gregory Evans, Kevin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Magnetic targeting; Retina; Superparamagnetic iron oxide nanoparticles (SPIONs)

Indexed keywords

GOLD; INTERLEUKIN 10; NEODYMIUM; SCATTER FACTOR; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; INJECTION; MAGNETISM; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; ORBIT; PRIORITY JOURNAL; RAT; RETINA; RETINA MACULA AGE RELATED DEGENERATION;

ANIMALS; CELL SURVIVAL; FERRIC COMPOUNDS; HEPATOCYTE GROWTH FACTOR; INTERLEUKIN-10; MAGNETITE NANOPARTICLES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICROSCOPY, CONFOCAL; RATS; RATS, TRANSGENIC; RETINAL DEGENERATION;

RATTUS; RODENTIA;

EID: 84865527543     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X627435     Document Type: Article

References (47)

1. Arbab, A. S.; Jordan, E. K.; Wilson, L. B.; Yocum, G. T.; Lewis, B. K.; Frank, J. A. In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum. Gene Ther. 15:351-360; 2004.
2. Arnhold, S.; Klein, H.; Semkova, I.; Addicks, K.; Schraermeyer, U. Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space. Invest. Ophthalmol. Vis. Sci. 45:4251-4255; 2004.
3. Baker, P. S.; Brown, G. C. Stem-cell therapy in retinal disease. Curr. Opin. Ophthalmol. 20:175-181; 2009.
4. Balakumaran, A.; Pawelczyk, E.; Ren, J.; Sworder, B.; Chaudhry, M.; Sabatino, M.; Stroncek, D.; Frank, J. A.; Robey, P. G. Superparamagnetic iron oxide nanoparticles labeling of bone marrow stromal (mesenchymal) cells does not affect their "stemness". PLoS One 5:e11462; 2010.
5. Berson, E. L.; Rosner, B.; Weigel-DiFranco, C.; Dryja, T. P.; Sandberg, M. A. Disease progression in patients with dominant retinitis pigmentosa and rhodopsin mutations. Invest. Ophthalmol. Vis. Sci. 43:3027-3036; 2002.
6. Castanheira, P.; Torquetti, L. T.; Magalhãs, D. R.; Nehemy, M. B.; Goes, A. M. DAPI diffusion after intravitreal injection of mesenchymal stem cells in the injured retina of rats. Cell Transplant. 18:423-431; 2009.
7. Chen, H.; Kaminski, M. D.; Pytel, P.; Macdonald, L.; Rosengart, A. J. Capture of magnetic carriers within large arteries using external magnetic fields. J. Drug Target. 16: 262-268; 2008.
8. Chen, J.; Makino, C. L.; Peachey, N. S.; Baylor, D. A.; Simon, M. I. Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267:374-377; 1995.
9. Coletti, D.; Teodori, L.; Albertini, M. C. Static magnetic fields enhance skeletal muscle differentiation in vitro by improving myoblast alignment. Cytometry A. 71:846- 856; 2007.
10. Congdon, N.; O'Colmain, B.; Klaver, C. C.; Klein, R.; Munoz, B.; Friedman, D. S.; Kempen, J.; Taylor, H. R.; Mitchell, P. Eye diseases prevalence research group. Causes and prevalence of visual impairment among adults in the United States. Arch. Ophthalmol. 122:477-485; 2004.
11. Gregory-Evans, K.; Chang, F.; Hodges, M. D.; Gregory-Evans, C. Y. Ex vivo gene therapy using intravitreal injection of GDNF-secreting mouse embryonic stem cells in a rat model of retinal degeneration. Mol. Vis. 15:962-973; 2009.
12. Grierson, I.; Rahi, A. H. Structural basis of contraction in vitreal fibrous membranes. Br. J. Ophthalmol. 65:737-749; 1981.
13. Guerin, K.; Gregory-Evans, C. Y.; Hodges, M. D.; Moosajee, M.; Mackay, D. S.; Gregory-Evans, K.; Flannery, J. G. Systemic aminoglycoside treatment in rodent models of retinitis pigmentosa. Exp. Eye Res. 87:197-207; 2008.
14. Hafeli, U. O.; Pauer, G. J. In vitro and in vivo toxicity of magnetic nanoparticles. J. Magn. Magn. Mater. 194: 76-82; 1999.
15. Halbach, K. Design of permanent multipole magnets with oriented rare earth cobalt material. Nucl. Instrum. Methods 169:1-10; 1980.
16. Hamasaki, T.; Tanaka, N.; Kamei, N. Magnetically labeled neural progenitor cells, which are localized by magnetic force, promote axon growth in organotypic cocultures. Spine 32:2300-2305; 2007.
17. Hayden, M. E.; Häfeli, U. O. Magnetic bandages for targeted delivery of therapeutic agents. J. Phys. Cond. Matter 18:S2877-s2891; 2006.
18. Joe, A. W.; Gregory-Evans, K. Mesenchymal stem cells and potential applications in treating ocular disease. Curr. Eye Res. 35:941-952; 2010.
19. Johnson, T. V.; Bull, N. D.; Hunt, D. P.; Marina, N.; Tomarev, S. I.; Martin, K. R. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 51: 2051-2059; 2010.
20. Kulbatski, I. Stem/precursor cell-based CNS therapy: The importance of circumventing immune suppression by transplanting autologous cells. Stem Cell. Rev. 6:405-410; 2010.
21. Kyrtatos, P. G.; Lehtolainen, P.; Junemann-Ramirez, M.; Garcia-Prieto, A.; Price, A. N.; Martin, J. F.; Gadian, D. G.; Pankhurst, Q. A.; Lythgoe, M. F. Magnetic tagging increases delivery of circulating progenitors in vascular injury. JACC Cardiovasc. Interv. 2:794-802; 2009.
22. Loebinger, M. R.; Kyrtatos, P. G.; Turmaine, M.; Price, A. N.; Pankhurst, Q.; Lythgoe, M. F.; Janes, S. M. Magnetic resonance imaging of mesenchymal stem cells homing to pulmonary metastases using biocompatible magnetic nanoparticles. Cancer Res. 69:8862-8867; 2009.
23. Lu, B.; Wang, S.; Girman, S.; McGill, T.; Ragaglia, V.; Lund, R. Human adult bone marrow-derived somatic cells rescue vision in a rodent model of retinal degeneration. Exp. Eye Res. 91:449-455; 2010.
24. Marchetti, V.; Krohne, T. U.; Friedlander, D. F.; Friedlander, M. Stemming vision loss with stem cells. J. Clin. Invest. 120:3012-3021; 2010.
25. Marchi, N.; Teng, Q.; Nguyen, M. T.; Franic, L.; Desai, N. K.; Masaryk, T.; Rasmussen, P.; Trasciatti, S.; Janigro, D. Multimodal investigations of trans-endothelial cell trafficking under condition of disrupted blood-brain barrier integrity. BMC Neurosci. 11:34; 2010.
26. Monzen, S.; Takahashi, K.; Toki, T. Exposure to a MRI-type high-strength static magnetic field stimulates megakaryocytic/erythroid hematopoiesis in CD34(+) cells from human placental and umbilical cord blood. Bioelectromagnetics 30:280-285; 2009.
27. Myers, T. J.; Granero-Molto, F.; Longobardi, L.; Li, T.; Yan, Y.; Spagnoli, A. Mesenchymal stem cells at the intersection of cell and gene therapy. Expert Opin. Biol. Ther. 10:1663-1679; 2010.
28. Nagai, N.; Kawao, N.; Okada, K.; Okumoto, K.; Teramura, T.; Ueshima, S.; Umemura, K.; Matsuo, O. Systemic transplantation of embryonic stem cells accelerates brain lesion decrease and angiogenesis. Neuroreport 21:575-579; 2010.
29. Nishida, K.; Tanaka, N.; Nakanishi, K.; Kamei, N.; Hamasaki, T.; Yanada, S.; Mochizuki, Y.; Ochi, M. Magnetic targeting of bone marrow stromal cells into spinal cord: Through cerebrospinal fluid. Neuroreport 17:1269-1272; 2006.
30. Parekkadan, B.; Milwid, J. M. Mesenchymal stem cells as therapeutics. Ann. Rev. Biomed. Eng. 12:87-117; 2010.
31. Pearson, R. A.; Barber, A. C.; West, E. L.; MacLaren, R. E.; Duran, Y.; Bainbridge, J. W.; Sowden, J. C.; Ali, R. R. Targeted disruption of outer limiting membrane junctional proteins (Crb1 and ZO-1) increases integration of transplanted photoreceptor precursors into the adult wild-type and degenerating retina. Cell Transplant. 19: 487-503; 2010.
32. Pislaru, S. V.; Harbuzariu, A.; Gulati, R.; Witt, T.; Sandhu, N. P.; Simari, R. D.; Sandhu, G. S. Magnetically targeted endothelial cell localization in stented vessels. J. Am. Coll. Cardiol. 48:1839-1845; 2006.
33. Polyak, B.; Fishbein, I.; Chorny, M.; Alferiev, I.; Williams, D.; Yellen, B.; Friedman, G.; Levy, R. J. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc. Natl. Acad. Sci. USA 105:698-703; 2008.
34. Riegler, J.; Wells, J. A.; Kyrtatos, P. G.; Price, A. N.; Pankhurst, Q. A.; Lythgoe, M. F. Targeted magnetic delivery and tracking of cells using a magnetic resonance imaging system. Biomaterials 31:5366-5371; 2010.
35. Schäfer, R.; Ayturan, M.; Bantleon, R. 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. 17:923-941; 2008.
36. Schäfer, R.; Bantleon, R.; Kehlbach, R.; Siegel, G.; Wiskirchen, J.; Wolburg, H.; Kluba, T.; Eibofner, F.; Northoff, H.; Claussen, C. D.; Schlemmer, H. P. Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol. 11:22; 2010.
37. Schäfer, R.; Kehlbach, R.; Muller, M. Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 11:68-78; 2009.
38. Schäfer, R.; Kehlbach, R.; Wiskirchen, J. Transferrin receptor upregulation: In vitro labeling of rat mesenchymal stem cells with superparamagnetic iron oxide. Radiology 244:514-523; 2007.
39. Solomon, S. D.; Dong, L. M.; Haller, J. A.; Gilson, M. M.; Bressler, N. M.; SST research group and the SST adverse event review committee. Risk factors for rhegmatogenous retinal detachment in the submacular surgery trials: SST report No. 22. Retina 29:819-824; 2009.
40. Steinberg, R. H.; Flannery, J. G.; Naash, M.; LaVail, M. M. Transgenic rat models of inherited retinal degeneration caused by mutant opsin genes. Invest. Ophthalmol. Vis. Sci. 37(Suppl.):698; 1996.
41. Tang, C.; Russell, P. J.; Martiniello-Wilks, R.; Rasko, J. E.; Khatri, A. Concise review: Nanoparticles and cellular carriers-allies in cancer imaging and cellular gene therapy? Stem Cells 28:1686-1702; 2010.
42. Tiefenauer, L. X. Magnetic nanoparticles as contrast agents for medical diagnosis. In: Vo-Dinh, T., ed. Nanotechnology in biology and medicine: Methods, devices, and applications. Boca Raton, FL: CRC Press; 2007:1-20.
43. Wang, H. C.; Brown, J.; Alayon, H.; Stuck, B. E. Transplantation of quantum dot-labelled bone marrow-derived stem cells into the vitreous of mice with laser-induced retinal injury: Survival, integration and differentiation. Vision Res. 50:665-673; 2010.
44. Wang, S.; Lu, B.; Girman, S.; Duan, J.; McFarland, T.; Zhang, Q. S.; Grompe, M.; Adamus, G.; Appukuttan, B.; Lund, R. Non-invasive stem cell therapy in a rat model for retinal degeneration and vascular pathology. PLoS One 5: e9200; 2010.
45. Wilhelm, C.; Bal, L.; Smirnov, P.; Galy-Fauroux, I.; Clment, O.; Gazeau, F.; Emmerich, J. Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28:3797-3806; 2007.
46. Yagi, H.; Soto-Gutierrez, A.; Parekkadan, B.; Kitagawa, Y.; Tompkins, R. G.; Kobayashi, N.; Yarmush, M. L. Mesenchymal stem cells: Mechanisms of immunomodulation and homing. Cell Transplant. 19:667-679; 2010.
47. Zhang, Y.; Wang, W. Effects of bone marrow mesenchymal stem cell transplantation on light-damaged retina. Invest. Ophthalmol. Vis. Sci. 51:3742-3748; 2010.