Transplantation of human bone marrow mesenchymal stem cells as a thin subretinal layer ameliorates retinal degeneration in a rat model of retinal dystrophy

Experimental Eye Research

Volumn 118, Issue , 2014, Pages 135-144

  Tzameret, Adi ^a   Sher, Ifat ^a   Belkin, Michael ^a   Treves, Avraham J ^b   Meir, Amilia ^b   Nagler, Arnon ^b   Levkovitch Verbin, Hani ^a   Barshack, Iris ^a   Rosner, Mordechai ^a   Rotenstreich, Ygal ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

Author keywords

Age related macular degeneration; Electroretinogram; Mesenchymal stem cells; Retinitis pigmentosa; Royal College of Surgeon rats; Subretinal transplantation

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B WAVE; CELL SUSPENSION; CONTROLLED STUDY; DARK ADAPTATION; ELECTRORETINOGRAM; FUNCTIONAL STATUS; HISTOPATHOLOGY; HUMAN; HUMAN BONE MARROW MESENCHYMAL STEM CELL TRANSPLANTATION; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MIDDLE AGED; NONHUMAN; NORMAL HUMAN; PERINATAL PERIOD; PHOTORECEPTOR; PHOTOSTIMULATION; PRIORITY JOURNAL; RAT; RETINA DEGENERATION; RETINA DYSTROPHY; RISK ASSESSMENT; THERAPY EFFECT; TREATMENT OUTCOME;

EID: 84891155619     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.10.023     Document Type: Article

References (43)

1. Arnhold S., Heiduschka P., Klein H., Absenger Y., Basnaoglu S., Kreppel F., Henke-Fahle S., Kochanek S., Bartz-Schmidt K.U., Addicks K., Schraermeyer U. Adenovirally transduced bone marrow stromal cells differentiate into pigment epithelial cells and induce rescue effects in RCS rats. Investig. Ophthalmol. Vis. Sci. 2006, 47:4121-4129.
2. Bourne M.C., Campbell D.A., Tansley K. Hereditary degeneration of the rat retina. Br. J. Ophthalmol. 1938, 22:613-623.
3. Caplan A.I. Why are MSCs therapeuticα New data: new insight. J.Pathol. 2009, 217:318-324.
4. Caplan A.I., Dennis J.E. Mesenchymal stem cells as trophic mediators. J.Cell. Biochem. 2006, 98:1076-1084.
5. Castanheira P., Torquetti L., Nehemy M.B., Goes A.M. Retinal incorporation and differentiation of mesenchymal stem cells intravitreally injected in the injured retina of rats. Arq. Bras. Oftalmol. 2008, 71:644-650.
6. Chen D., Zhao M., Mundy G.R. Bone morphogenetic proteins. Growth Factors 2004, 22:233-241.
7. D'Cruz P.M., Yasumura D., Weir J., Matthes M.T., Abderrahim H., LaVail M.M., Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 2000, 9:645-651.
8. Edwards R.B., Szamier R.B. Defective phagocytosis of isolated rod outer segments by RCS rat retinal pigment epithelium in culture. Science 1977, 197:1001-1003.
9. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279:1528-1530.
10. Foster C.S., Wetzig R. Immune reactions in the eye. Surv. Immunol. Res. 1982, 1:93-108.
11. Gamm D.M., Wang S., Lu B., Girman S., Holmes T., Bischoff N., Shearer R.L., Sauve Y., Capowski E., Svendsen C.N., Lund R.D. Protection of visual functions by human neural progenitors in a rat model of retinal disease. PLoS One 2007, 2:e338.
12. Hartong D.T., Berson E.L., Dryja T.P. Retinitis pigmentosa. Lancet 2006, 368:1795-1809.
13. Idelson M., Alper R., Obolensky A., Ben-Shushan E., Hemo I., Yachimovich-Cohen N., Khaner H., Smith Y., Wiser O., Gropp M., Cohen M.A., Even-Ram S., Berman-Zaken Y., Matzrafi L., Rechavi G., Banin E., Reubinoff B. Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell. Stem Cell. 2009, 5:396-408.
14. 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. Investig. Ophthalmol. Vis. Sci. 2010, 51:2051-2059.
15. Kicic A., Shen W.Y., Wilson A.S., Constable I.J., Robertson T., Rakoczy P.E. Differentiation of marrow stromal cells into photoreceptors in the rat eye. J.Neurosci. 2003, 23:7742-7749.
16. Kofuji P., Ceelen P., Zahs K.R., Surbeck L.W., Lester H.A., Newman E.A. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J.Neurosci. 2000, 20:5733-5740.
17. Kopen G.C., Prockop D.J., Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10711-10716.
18. Levkovitch-Verbin H. Animal models of optic nerve diseases. Eye (Lond) 2004, 18:1066-1074.
19. Li N., Li X.R., Yuan J.Q. Effects of bone-marrow mesenchymal stem cells transplanted into vitreous cavity of rat injured by ischemia/reperfusion. Graefe's Arch. Clin. Exp. Ophthalmol. 2009, 247:503-514.
20. Lo B., Parham L. Ethical issues in stem cell research. Endocr. Rev. 2009, 30:204-213.
21. Lu B., Malcuit C., Wang S., Girman S., Francis P., Lemieux L., Lanza R., Lund R. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 2009, 27:2126-2135.
22. 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. 2010, 91:449-455.
23. Lund R.D., Wang S., Klimanskaya I., Holmes T., Ramos-Kelsey R., Lu B., Girman S., Bischoff N., Sauve Y., Lanza R. Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats. Cloning Stem Cells 2006, 8:189-199.
24. Miller J.W., Le Couter J., Strauss E.C., Ferrara N. Vascular endothelial growth factor a in intraocular vascular disease. Ophthalmology 2013, 120:106-114.
25. Nowak J.Z. Age-related macular degeneration (AMD): pathogenesis and therapy. Pharmacol. Rep. 2006, 58:353-363.
26. Oh J.Y., Kim M.K., Shin M.S., Lee H.J., Ko J.H., Wee W.R., Lee J.H. The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 2008, 26:1047-1055.
27. Otani A., Dorrell M.I., Kinder K., Moreno S.K., Nusinowitz S., Banin E., Heckenlively J., Friedlander M. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J.Clin. Investig. 2004, 114:765-774.
28. Park H.Y., Kim J.H., Sun Kim H., Park C.K. Stem cell-based delivery of brain-derived neurotrophic factor gene in the rat retina. Brain Res. 2012, 1469:10-23.
29. Park K.I., Himes B.T., Stieg P.E., Tessler A., Fischer I., Snyder E.Y. Neural stem cells may be uniquely suited for combined gene therapy and cell replacement: evidence from engraftment of neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp. Neurol. 2006, 199:179-190.
30. Penn R.D., Hagins W.A. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 1969, 223:201-204.
31. Phinney D.G., Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 2007, 25:2896-2902.
32. Prockop D.J. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin. Pharmacol. Ther. 2007, 82:241-243.
33. Rodriguez F.D., Vecino E. Stem cell plasticity, neuroprotection and regeneration in human eye diseases. Curr. Stem Cell. Res. Ther. 2011, 6:73-81.
34. Schwartz S.D., Hubschman J.P., Heilwell G., Franco-Cardenas V., Pan C.K., Ostrick R.M., Mickunas E., Gay R., Klimanskaya I., Lanza R. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012, 379:713-720.
35. Tomita M., Adachi Y., Yamada H., Takahashi K., Kiuchi K., Oyaizu H., Ikebukuro K., Kaneda H., Matsumura M., Ikehara S. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells 2002, 20:279-283.
36. Vandervelde S., van Luyn M.J., Tio R.A., Harmsen M.C. Signaling factors in stem cell-mediated repair of infarcted myocardium. J.Mol. Cell. Cardiol. 2005, 39:363-376.
37. Wang S., Girman S., Lu B., Bischoff N., Holmes T., Shearer R., Wright L.S., Svendsen C.N., Gamm D.M., Lund R.D. Long-term vision rescue by human neural progenitors in a rat model of photoreceptor degeneration. Investig. Ophthalmol. Vis. Sci. 2008, 49:3201-3206.
38. 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 2010, 5:e9200.
39. West E.L., Pearson R.A., MacLaren R.E., Sowden J.C., Ali R.R. Cell transplantation strategies for retinal repair. Prog. Brain Res. 2009, 175:3-21.
40. Wurziger K., Lichtenberger T., Hanitzsch R. On-bipolar cells and depolarising third-order neurons as the origin of the ERG-b-wave in the RCS rat. Vis. Res. 2001, 41:1091-1101.
41. Young B., Eggenberger E., Kaufman D. Current electrophysiology in ophthalmology: a review. Curr. Opin. Ophthalmol. 2012, 23:497-505.
42. Yu S., Tanabe T., Dezawa M., Ishikawa H., Yoshimura N. Effects of bone marrow stromal cell injection in an experimental glaucoma model. Biochem. Biophys. Res. Commun. 2006, 344:1071-1079.
43. Zhang Y., Wang W. Effects of bone marrow mesenchymal stem cell transplantation on light-damaged retina. Investig. Ophthalmol. Vis. Sci. 2010, 51:3742-3748.