Cell-based therapy for retina degeneration: The promise of a cure

Vision Research

Volumn 47, Issue 22, 2007, Pages 2815-2824

  Gaillard, Frédéric ^a   Sauvé, Yves ^b  

^a UNIVERSITÉ DE POITIERS   (France)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cell based therapy; Photoreceptors; Retina; Retinal dystrophy; Stem cells; Visual function

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; SOMATOMEDIN C;

BLINDNESS; CELL DIFFERENTIATION; CELL SURVIVAL; CELL THERAPY; DIABETIC RETINOPATHY; ELECTRORETINOGRAM; ELECTROSTIMULATION; EMBRYONIC STEM CELL; GENE THERAPY; HUMAN; NONHUMAN; PARACRINE SIGNALING; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RAT; RETINA DEGENERATION; RETINA MACULA AGE RELATED DEGENERATION; RETINITIS PIGMENTOSA; REVIEW; SCHWANN CELL; ANIMAL; CYTOLOGY; DISEASE MODEL; PHOTORECEPTOR CELL; PROCEDURES; RETINAL DEGENERATION; STEM CELL TRANSPLANTATION; TRANSPLANTATION; TREATMENT OUTCOME;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; PHOTORECEPTOR CELLS, VERTEBRATE; PIGMENT EPITHELIUM OF EYE; RATS; RETINAL DEGENERATION; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME;

EID: 34548733046     PISSN: 00426989     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.visres.2007.06.018     Document Type: Review

References (81)

1. Algvere P.V., Berglin L., Gouras P., Sheng Y., and Kopp E.D. Transplantation of RPE in age-related macular degeneration: Observations in disciform lesions and dry RPE atrophy. Graefes Archives of Clinical and Experimental Ophthalmology 235 (1997) 149-158
2. Arnhold S., Klein H., Semkova I., Addicks K., and Schraermeyer U. Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space. Investigative Ophthalmology and Visual Sciences 45 (2004) 4251-4255
3. Aymerich M.S., Alberdi E.M., Martinez A.S., and Becerra P. Evidence for pigment epithelium-Derived factor receptors in the neural retina. Investigative Ophthalmology and Visual Sciences 42 (2001) 3287-3293
4. Banin E., Obolensky A., Idelson M., Hemo I., Reinhardtz E., Pikarsky E., et al. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells. Stem cells 24 (2006) 246-257
5. Barnstable C.J., and Tombran-Tink J. Neuroprotective and antiangiogenic actions of PEDF in the eye: Molecular targets and therapeutic potential. Progress in Retina and Eye Research 23 (2004) 561-577
6. Berger A.S., Tezel T.H., Del Priore L.V., and Kaplan H.J. Photoreceptor transplantation in retinitis pigmentosa: Short-term follow-up. Ophthalmology 110 (2003) 383-391
7. Bok D., Yasumura D., Matthes M.T., Ruiz A., Duncan J.L., Chappelow A.V., et al. Effects of adeno-associated virus-vectored ciliary neurotrophic factor on retinal structure and function in mice with a P216L rds/peripherin mutation. Experimental Eye Research 74 (2002) 719-735
8. Campochiaro P.A., Hacket S.F., and Conway B.P. Retinoic acid promotes density-dependent growth arrest in human retinal pigment epithelial cells. Investigative Ophthalmology and Visual Sciences 32 (1991) 65-72
9. Campochiaro P.A., Nguyen Q.D., Shah S.M., Klein M.L., Holz E., Frank R.N., et al. Adenoviral vector-delivered pigment epithelium-derived factor for neovascular age-related macular degeneration: Results of a phase I clinical trial. Human Gene Therapy 17 (2006) 167-176
10. Canola K., Angenieux B., Tekaya M., Quiambao A., Naash M.I., Munier F.L., et al. Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Investigative Ophthalmology and Visual Science 48 (2007) 446-454
11. Carter-Dawson L.D., and LaVail M.M. Rods and cones in the mouse retina II. Autoradiographic analysis of cell generation using tritiated thymidine. Journal of Comparative Neurology 188 (1979) 263-272
12. Cashman S.M., Binkley E.A., and Kumar-Singh R. Towards mutation-independent silencing of genes involved in retinal degeneration by RNA interference. Gene Therapy 12 (2005) 1223-1228
13. Cayouette M., Smith S.B., Becerra S.P., and Gravel C. Pigment epithelium-derived factor delays the death of photoreceptors in mouse models of inherited retinal degenerations. Neurobiology of Disease 6 (1999) 523-532
14. Chacko D.M., Rogers J.A., Turner J.E., and Ahmad I. Survival and differentiation of cultured retinal progenitors transplanted in the subretinal space of the rat. Biochemical and Biophysical Research Communications 268 (2000) 842-846
15. Coffey P.J., Girman S., Wang S.M., Hetherington L., Keegan D.J., Adamson P., et al. Long-term preservation of cortically dependent visual function in RCS rats by transplantation. Nature Neuroscience 5 (2002) 53-56
16. Conti S.M., and Kertes P.J. Surgical management of age-related macular degeneration. Canadian Journal Ophthalmology 40 (2005) 341-351
17. Daniele L.L., Lillo C., Lyubarsky A.L., Nikonov S.S., Philip N., Mears A.J., et al. Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Investigative Ophthalmology and Visual Sciences 46 (2005) 2156-2167
18. D'Cruz P.M., Yasumura D., Weir J., Matthes M.T., Abderrahim H., LaVail M.M., et al. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Human Molecular Genetics 9 (2000) 645-651
19. Del Cerro M., Humayun M.S., Sadda S.R., Cao J., Hayashi N., Green W.R., et al. Histologic correlation of human neural retinal transplantation. Investigative Ophthalmology and Visual Sciences 41 (2000) 3142-3148
20. Del Priore L.V., Hornbeck R., Kaplan H.J., Jones Z., Silverman M.S., Mosinger-Ogilvie J., et al. Debridment of the pig retinal pigment epithelium in vivo. Archives of Ophthalmology 113 (1993) 939-944
21. Dong X., Pulido J.S., Qu T., and Sugaya K. Differentiation of human neural stem cells into retinal cells. NeuroReport 14 (2003) 143-146
22. Dunn K.C., Aotaki-Keen A.E., Putkey F.R., and Hjelmeland L.M. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Experimental Eye Research 62 (1996) 155-169
23. Fisher S.K., Lewis G.P., Linberg K.A., and Verardo M.R. Cellular remodeling in mammalian retina: Results from studies of experimental retinal detachment. Progress in Retina and Eye Research 24 (2005) 395-431
24. Fu Y., Zhong H., Wang M.H., Luo D.G., Liao H.W., Maeda H., et al. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proceedings of the National Academy of Science of the United States of America 102 (2005) 10339-10344
25. Gal A., Li Y., Thompson D.A., Weir J., Orth U., Jacobson S.G., et al. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nature Genetics 26 (2000) 270-271
26. Gamm D.M., Wang S., Lu B., Girman S., Holmes T., Bischoff N., et al. Protection of photoreceptors and visual function by human neural progenitors. PLoS ONE 2 (2007) e388
27. Girman S.V., Wang S., and Lund R.D. Cortical visual functions can be preserved by subretinal RPE cell grafting in RCS rats. Vision Research 43 (2003) 1817-1827
28. Girman S.V., Wang S., and Lund R.D. Time course of deterioration of rod and cone function in RCS rat and the effects of subretinal cell grafting: A light- and dark-adaptation study. Vision Research 45 (2005) 343-354
29. Gouras P., Du J., Gelanze M., Lopez R., Kwun R., Kjeldbye H., et al. Survival and synapse formation of transplanted rat rods. Journal of Neural Transplantation and Plasticity 2 (1991) 91-100
30. Gouras P., Du J., Kjeldbye H., Kwun R., Lopez R., and Zack D.J. Transplanted photoreceptors identified in dystrophic mouse retina by a transgenic reporter gene. Investigative Ophthalmology and Visual Sciences 32 (1991) 3167-3174
31. Gouras P., Du J., Kjeldbye H., Yamamoto S., and Zack D.J. Long-term photoreceptor transplants in dystrophic and normal mouse retina. Investigative Ophthalmology and Visual Sciences 35 (1994) 3145-3153
32. Gouras P., and Tanabe T. Survival and integration of neural retinal transplants in rd mice. Graefes Archives of Clinical and Experimental Ophthalmology 241 (2003) 403-409
33. Green E.S., Rendahl K.G., Zhou S., Ladner M., Coyne M., Srivastava R., et al. Two animal models of retinal degeneration are rescued by recombinant adeno-associated virus-mediated production of FGF-5 and FGF-18. Molecular Therapy 3 (2001) 507-515
34. Guo Y., Saloupis P., Shaw S.J., and Rickman D.W. Engraftment of adult neural progenitor cells transplanted to rat retina injured by transient ischemia. Investigative Ophthalmology and Visual Sciences 44 (2003) 3194-3201
35. Hara A., Niwa M., Kunisada T., Yoshimura N., Katayama M., Kozawa O., et al. Embryonic stem cells are capable of generating a neuronal network in the adult mouse retina. Brain Research 999 (2004) 216-221
36. Harris J.R., Brown G.A., Jorgensen M., Kaushal S., Ellis E.A., Grant M.B., et al. Bone marrow-derived cells home to and regenerate retinal pigment epithelium after injury. Investigative Ophthalmology and Visual Sciences 47 (2006) 2108-2113
37. Huang Q., Xu P., Xia X., Hu H.H., Wang F., and Li H.M. Subretinal transplantation of human fetal lung fibroblasts expressed ciliary neurotrophic factor gene prevent photoreceptor degeneration in RCS rats. Zhonghua Yan Ke Za Zhi 42 (2006) 127-130 Paper in Chinese language.
38. Imai D., Yoneya S., Gehlbach P.L., Wei L.L., and Mori K. Intraocular gene transfer of pigment epithelium-derived factor rescues photoreceptors from light-induced cell death. Journal of Cellular Physiology 202 (2005) 570-578
39. Jones B.W., and Marc R.E. Retinal remodeling during retinal degeneration. Experimental Eye Research 81 (2005) 123-137
40. Joussen A.M., and Joeres S. Benefits and limitations in vitreoretinal surgery for proliferative diabetic retinopathy and macular edema. In: Lang G.E. (Ed). Diabetic retinopathy developmental ophthalmology (2007), Basel, Karger 69-87
41. Kanuga N., Winton H.L., Beauchene L., Koman A., Zerbib A., Halford S., et al. Characterization of genetically modified human retinal pigment epithelial cells developed for in vitro and transplantation studies. Investigative Ophthalmology and Visual Sciences 43 (2002) 546-555
42. Keegan D.J., Kenna P., Humphries M.M., Humphries P., Flitcroft D.I., Coffey P.J., et al. Transplantation of syngeneic Schwann cells to the retina of the rhodopsin knockout (rho(-/-)) mouse. Investigative Ophthalmology and Visual Sciences 44 (2003) 3526-3532
43. Klassen H.J., Ng T.F., Kurimoto Y., Kirov I., Shatos M., Coffey P., et al. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Investigative Ophthalmology and Visual Sciences 45 (2004) 4167-4173
44. Klimanskaya I., Hipp J., Rezai K.A., West M., Atala M., and Lanza R. Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics. Cloning and Stem Cells 6 (2004) 217-245
45. Kwan A.S.L., Wang S., and Lund R.D. Photoreceptor layer reconstruction in a rodent model of retinal degeneration. Experimental Neurology 159 (1999) 21-33
46. Lamba D.A., Karl M.O., Ware C.B., and Reh T.A. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proceedings of the National Academy of Science of the United States of America 103 (2006) 12769-12774
47. Lavail M.M., Li L., Turner J.E., and Yasumura D. Retinal pigment epithelial cell transplantation in RCS rats: Normal metabolism in rescued photoreceptors. Experimental Eye Research 55 (1992) 555-562
48. Lawrence J.M., Keegan D.J., Muir E.M., Coffey P.J., Rogers J.H., Wilby M.J., et al. Transplantation of Schwann cell line clones secreting GDNF or BDNF into the retinas of dystrophic Royal College of Surgeons rats. Investigative Ophthalmology and Visual Sciences 45 (2004) 267-274
49. Layer P.G., Rothermel A., and Willbold E. From stem cells towards neural layers: A lesson from re-aggregated embryonic retinal cells. Neuroreport 12 (2001) A39-A46
50. Leveillard T., Mohand-Said S., Lorentz O., Hicks D., Fintz A.C., Clerin E., et al. Identification and characterization of rod-derived cone viability factor. Nature Genetics 36 (2004) 755-759
51. Liang F.Q., Aleman T.S., Dejneka N.S., Dudus L., Fisher K.J., Maguire A.M., et al. Long-term protection of retinal structure but not function using RAAV.CNTF in animal models of retinitis pigmentosa. Molecular Therapy 4 (2001) 461-472
52. Limb G.A., Daniels J.T., Cambrey A.D., Secker G.A., Shortt A.J., Lawrence J.M., et al. Current prospects for adult stem cell-based therapies in ocular repair and regeneration. Current Eye Research 31 (2006) 381-390
53. Lund R.D., Kwan A.S., Keegan D.J., Sauvé Y., Coffey P.J., and Lawrence J.M. Cell transplantation as a treatment for retinal disease. Progress in Retina and Eye Research 20 (2001) 415-449
54. Lund R.D., Wang S., Klimanskaya I., Holmes T., Ramos-Kelsey R., Lu B., et al. Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats. Cloning and Stem Cells 8 (2006) 189-199
55. Lund R.D., Wang S., Lu B., Girman S., Holmes T., Sauvé Y., et al. Cells isolated from umbilical cord tissue rescue photoreceptors and visual functions in a rodent model of retinal disease. Stem Cells 25 (2007) 602-611
56. MacLaren R.E., Pearson R.A., MacNeil A., Douglas R.H., Salt T.E., Akimoto M., et al. Retinal repair by transplantation of photoreceptor precursors. Nature 444 (2006) 203-207
57. McGill T.J., Lund R.D., Douglas R.M., Wang S., Lu B., Silver B.D., et al. Syngeneic Schwann cell transplantation preserves vision in RCS rat without immunosuppression. Investigative Ophthalmology and Visual Sciences 48 (2007) 1906-1912
58. McGill T.J., Lund R.D., Douglas R.M., Wang S., Lu B., and Prusky G.T. Preservation of vision following cell-based therapies in a model of retinal degenerative disease. Vision Research 44 (2004) 2559-2566
59. McHenry C.L., Liu Y., Feng W., Nair A.R., Feathers K.L., Ding X., et al. MERTK arginine-844-cysteine in a patient with severe rod-cone dystrophy: Loss of mutant protein function in transfected cells. Investigative Ophthalmology and Visual Sciences 45 (2004) 1456-1463
60. Mears A.J., Kondo M., Swain P.K., Takada Y., Bush R.A., Saunders T.L., et al. Nrl is required for rod photoreceptor development. Nat. Genet. 29 2001 (2001) 447-452
61. Meyer J.S., Katz M.L., Maruniak J.A., and Kirk M.D. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 24 (2006) 274-283
62. Mohand-Said S., Hicks D., Dreyfus H., and Sahel J.A. Selective transplantation of rods delays cone loss in a retinitis pigmentosa model. Archives of Ophthalmology 118 (2000) 807-811
63. Nishida A., Takahashi M., Tanihara H., Nakano I., Takahashi J.B., Mizoguchi A., et al. Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Investigative Ophthalmology and Visual Sciences 41 (2000) 4268-4274
64. O'Brien K.M., Schulte D., and Hendrickson A.E. Expression of photoreceptor-associated molecules during human fetal eye development. Molecular Vision 9 (2003) 401-409
65. Oh E.C., Khan N., Novelli F., Khanna H., Strettoi E., and Swaroop A. Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 1679-1684
66. Pressmar S., Ader M., Richard G., Schachner M., and Bartsch U. The fate of heterotopically grafted neural precursor cells in the normal and dystrophic adult mouse retina. Investigative Ophthalmology and Visual Sciences 42 (2001) 3311-3319
67. Sakaguchi D.S., Van Hoffelen S.J., and Young M.J. Differentiation and morphological integration of neural progenitor cells transplanted into the developing mammalian eye. Annals of the New York Academy of Sciences 995 (2003) 127-139
68. Sauvé Y., Girman S.V., Wang S., Keegan D.J., and Lund R.D. Preservation of visual responsiveness in the superior colliculus of RCS rats after retinal pigment epithelium cell transplantation. Neuroscience 114 (2002) 389-401
69. Sauvé Y., Pinilla I., and Lund R.D. Partial preservation of rod and cone ERG function following subretinal injection of ARPE-19 cells in RCS rats. Vision Research 46 (2006) 1459-1472
70. Seiler M.J., and Aramant R.B. Transplantation of neuroblastic progenitor cells as a sheet preserves and restores retinal function. Seminars in Ophthalmology 20 (2005) 31-42
71. Sharma R.K., Bergstrom A., Zucker C.L., Adolph A.R., and Ehinger B. Survival of long-term retinal cell transplants. Acta Ophthalmologica Scandinavia 78 (2000) 396-402
72. Sieving P.A., Caruso R.C., Tao W., Coleman H.R., Thompson D.J., Fullmer K.R., et al. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: Phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proceedings of the National Academy of Sciences of the United Sates of America 103 (2006) 3896-3901
73. Suzuki T., Mandai M., Akimoto M., Yoshimura N., and Takahashi M. The simultaneous treatment of MMP-2 stimulants in retinal transplantation enhances grafted cell migration into the host retina. Stem Cells 24 (2006) 2406-2411
74. Tao W., Wen R., Goddard M.B., Sherman S.D., O'Rourke P.J., Stabila P.F., et al. Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa. Investigative Ophthalmology and Visual Sciences 43 (2002) 3292-3298
75. Valentino A., Kaplan H.J., Del Priore L.V., Fang J., Berger A., and Silverman M.S. Retinal pigment epithelium repopulation and photoreceptor repair after submacular surgery. Archives of Ophthalmology 113 (1995) 932-938
76. Wang S., Lu B., Wood P., and Lund R.D. Grafting ARPE-19 and Schwann cells to the subretinal space in RCS rats. Investigative Opthalmology and Visual Sciences 46 (2005) 2552-2560
77. Yanai D., Weiland J.D., Mahadevappa M., Greenberg R.J., Fine I., and Humayun M.S. Visual performance using a retinal prosthesis in three subjects with retinitis pigmentosa. American Journal of Ophthalmology 143 (2007) 820-827
78. Yang P., Seiler M.J., Aramant R.B., and Whittemore S.R. Differential lineage restriction of rat retinal progenitor cells in vitro and in vivo. Journal of Neuroscience Research 69 (2002) 466-476
79. Young M.J., Ray J., Whiteley S.J.O., Klassen H., and Gage F.H. Neuronal differentiation and morphological integration of hippocampal progenitor cells transplanted to the retina of immature and mature dystrophic rats. Molecular and Cellular Neuroscience 16 (2000) 197-205
80. Zacks D.N., Han Y., Zeng Y., and Swaroop A. Activation of signaling pathways and stress-response genes in an experimental model of retinal detachment. Investigative Ophthalmology and Visual Sciences 47 (2006) 1691-1695
81. Zhang Y., Arner K., Ehinger B., and Perez M.T. Limitation of anatomical integration between subretinal transplants and the host retina. Investigative Ophthalmology and Visual Sciences 44 (2003) 324-331