Biology and therapeutic potential of adult retinal stem cells

Canadian Journal of Ophthalmology

Volumn 45, Issue 4, 2010, Pages 342-351

  Ballios, Brian G ^a   Van Kooy, Derek Der ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adult stem cells; Regenerative medicine; Retinal degeneration

Indexed keywords

BIOLOGICAL MARKER; TRANSCRIPTION FACTOR OTX2;

ADULT STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELLULAR DISTRIBUTION; CYTOLOGY; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HUMAN; NONHUMAN; PHOTORECEPTOR; PROTEIN EXPRESSION; RETINA CELL; RETINA DEGENERATION; REVIEW; STEM CELL TRANSPLANTATION; SUBRETINAL STEM CELL TRANSPLANTATION; VISUAL IMPAIRMENT; ANIMAL; REGENERATIVE MEDICINE; RETINA; RETINAL DEGENERATION; TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; HUMANS; REGENERATIVE MEDICINE; RETINA; RETINAL DEGENERATION; STEM CELL TRANSPLANTATION;

EID: 77955437273     PISSN: 00084182     EISSN: 17153360     Source Type: Journal    
DOI: 10.3129/i10-070     Document Type: Review

References (93)

1. Cruess A, Zlateva G, Xu X, Rochon S. Burden of illness of neovascular age-related macular degeneration in Canada. Can J Ophthalmol 2007;42:836-43.
2. Klein BEK. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol 2007;14:179-83.
3. Shintani K, Shechtman DL, Gurwood AS. Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry 2009;80:384-401.
4. Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA 2003; 290:2057-60. (Pubitemid 37430590)
5. Lee P, Wang CC, Adamis AP. Ocular neovascularization: an epidemiologic review. Surv Ophthalmol 1998;43:245-69.
6. Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 2006;355:1419-31.
7. Menon G, Walters G. New paradigms in the treatment of wet AMD: the impact of anti-VEGF therapy. Eye 2009; 23(Suppl 1):1-7.
8. Comer GM, Ciulla TA. Current and future pharmacological intervention for diabetic retinopathy. Expert Opin Emerg Drugs 2005;10:441-55.
9. Algvere PV, Gouras P, Kopp ED. Long-term outcome of RPE allografts in non-immunosuppressed patients with AMD. Eur J Ophthalmol 1999;9:217-30.
10. Algvere PV, Berglin L, Gouras P, Sheng Y. Human fetal RPE transplants in age related macular degeneration (ARMD). Invest Ophthalmol Vis Sci 1996;37:S96. (Pubitemid 126821940)
11. Das TP, Del Cerro M, Lazar ES, et al. Transplantation of neural retina in patients with retinitis pigmentosa. Invest Ophthalmol Vis Sci 1996;37:S96. (Pubitemid 126821938)
12. Berson EL, Jakobiec FA. Neural retinal cell transplantation: ideal versus reality. Ophthalmology 1999;106:445-6.
13. Klassen H, Sakaguchi DS, Young MJ. Stem cells and retinal repair. Prog Retin Eye Res 2004;23:149-81.
14. Enzmann V, Yolcu E, Kaplan HJ, Ildstad ST. Stem cells as tools in regenerative therapy for retinal degeneration. Arch Ophthalmol 2009;127:563-71.
15. Daley GQ, Scadden DT. Prospects for stem cell-based therapy. Cell 2008;132:544-8.
16. Amariglio N, Hirshberg A, Scheithauer BW, et al. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 2009;6:e1000029.
17. Sharp J, Keirstead HS. Therapeutic applications of oligodendrocyte precursors derived from human embryonic stem cells. Curr Opin Biotechnol 2007;18:434-40. (Pubitemid 350116594)
18. Keirstead HS, Nistor G, Bernal G, et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 2005;25:4694-705. (Pubitemid 40664118)
19. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-76. (Pubitemid 44233629)
20. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007; 448:313-7. (Pubitemid 47080336)
21. Aoi T, Yae K, Nakagawa M, et al. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 2008;321:699-702.
22. Giorgetti A, Montserrat N, Rodriguez-Piza I, Azqueta C, Veiga A, Belmonte JC. Generation of induced pluripotent stem cells from human cord blood cells with only two factors: Oct4 and Sox2. Nat Protoc 2010;5:811-20.
23. Kim JB, Greber B, Arauzo-Bravo MJ, et al. Direct reprogramming of human neural stem cells by OCT4. Nature 2009;461:649-3.
24. Zhou H, Wu S, Joo JY, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009;4:381-4.
25. Woltjen K, Michael IP, Mohseni P, et al. PiggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 2009;458:766-70.
26. Belmonte JCI, Ellis J, Hochedlinger K, Yamanaka S. Induced pluripotent stem cells and reprogramming: seeing the science through the hype. Nat Rev Genet 2009;10:878-83.
27. Clarke L, van der Kooy D. A safer stem cell: inducing pluripotency. Nat Med 2009;15:1001-2.
28. Lamba DA, Gust J, Reh TA. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 2009;4:73-9.
29. Lamba DA, Karl MO, Ware CB, Reh TA. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci USA 2006;103:12769-74.
30. Banin E, Obolensky A, Idelson M, et al. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells. Stem Cells 2006;24:246-57. (Pubitemid 44464792)
31. Osakada F, Ikeda H,Mandai M, et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat Biotechnol 2008;26:215-24. (Pubitemid 351225958)
32. Lamba DA, McUsic A, Hirata RK, Wang PR, Russell D, Reh TA. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS ONE 2010;5:e8763.
33. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008;132:598-611.
34. Scadden DT. The stem-cell niche as an entity of action. Nature 2006;441:1075-9.
35. Turner DL, Cepko CL. A common progenitor for neurons and glia persists in rat retina late in development. Nature 1987;328:131-6.
36. Holt CE, Bertsch TW, Ellis HM, Harris WA. Cellular determination in the xenopus retina is independent of lineage and birth date. Neuron 1988;1:15-26.
37. Wetts R, Fraser SE. Multipotent precursors can give rise to all major cell types of the frog retina. Science 1988;239:1142-5. (Pubitemid 18084323)
38. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 1996;93:589-95. (Pubitemid 26041133)
39. Adler R, Hatlee M. Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 1989;243:391-3. (Pubitemid 19047516)
40. Reh TA, Kijavin IJ. Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J Neurosci 1989;9:4179-89.
41. Belliveau MJ, Cepko CL. Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 1999;126:555-66.
42. Watanabe T, Raff MC. Diffusible rod-promoting signals in the developing rat retina. Development 1992;114:899-906.
43. Warfvinge K, Kiilgaard JF, Lavik EB, et al. Retinal progenitor cell xenografts to the pig retina: morphologic integration and cytochemical differentiation. Arch Ophthalmol 2005;123:1385-93. (Pubitemid 41429739)
44. Young MJ. Stem cells in the mammalian eye: a tool for retinal repair. APMIS 2005;113:845-57.
45. Otteson DC, Hitchcock PF. Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 2003;43:927-36.
46. Thummel R, Kassen SC, Enright JM, Nelson CM, Montgomery JE, Hyde DR. Characterization of Muller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp Eye Res 2008;87:433-44.
47. Park CM, Hollenberg MJ. Growth factor-induced retinal regeneration in vivo. Int Rev Cytol 1993;146:49-74.
48. Park CM, Hollenberg MJ. Basic fibroblast growth factor induces retinal regeneration in vivo. Dev Biol 1989;134:201-5.
49. Guillemot F, Cepko CL. Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an in vitro assay of early retinal development. Development 1992;114:743-54.
50. Opas M, Dziak E. bFGF-induced transdifferentiation of RPE to neuronal progenitors is regulated by the mechanical properties of the substratum. Dev Biol 1994;161:440-54. (Pubitemid 24077413)
51. Fischer AJ, Reh TA. Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 2000;220:197-210.
52. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-10.
53. Lois C, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 1993;90:2074-7. (Pubitemid 23070000)
54. Morshead CM, Reynolds BA, Craig CG, et al.Neural stemcells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994;13:1071-82.
55. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996;16:2649-58.
56. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996;16:2027-33. (Pubitemid 26144015)
57. Suhonen JO, Peterson DA, Ray J, Gage FH. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 1996;383:624-27. (Pubitemid 26347584)
58. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 1996;19:387-93.
59. McKay R. Stem cells in the central nervous system. Science 1997;276:66-71. (Pubitemid 27161244)
60. Tropepe V, Coles BLK, Chiasson BJ, et al. Retinal stem cells in the adult mammalian eye. Science 2000;287:2032-6. (Pubitemid 30158683)
61. Coles BLK, Angenieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA 2004;101:15772-7. (Pubitemid 39473563)
62. Young RW. Cell differentiation in the retina of the mouse. Anat Rec 1985;212:199-205.
63. Xu S, Sunderland ME, Coles BLK, et al. The proliferation and expansion of retinal stem cells require functional Pax6. Dev Biol 2007;304:713-21. (Pubitemid 46527572)
64. Ahmad I, Tang L, Pham H. Identification of neural progenitors in the adult mammalian eye. Biochem Biophys Res Commun 2000;270:517-21. (Pubitemid 30446867)
65. Asami M, Sun G, Yamaguchi M, Kosaka M. Multipotent cells from mammalian iris pigment epithelium. Dev Biol 2007; 304:433-46. (Pubitemid 46399698)
66. Reneker LW, Silversides DW, Xu L, Overbeek PA. Formation of corneal endothelium is essential for anterior segment development - a transgenic mouse model of anterior segment dysgenesis. Development 2000;127:533-42. (Pubitemid 30093401)
67. Cicero SA, Johnson D, Reyntjens S, et al. Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci USA 2009;106:6685-90.
68. Inoue T, Coles BL, Dorval K, et al. Maximizing functional photoreceptor differentiation from adult human retinal stem cells. Stem Cells 2009;28:489-500.
69. Canola K, Arsenijevic Y. Generation of cells committed towards the photoreceptor fate for retinal transplantation. NeuroReport 2007;18:851-5. (Pubitemid 46791512)
70. Angenieux B, Schorderet DF, Arsenijevic Y. Epidermal growth factor is a neuronal differentiation factor for retinal stem cells in vitro. Stem Cells 2006;24:696-706. (Pubitemid 44464774)
71. Merhi-Soussi F, Angenieux B, Canola K, et al. High yield of cells committed to the photoreceptor fate from expanded mouse retinal stem cells. Stem Cells 2006;24:2060-70.
72. Canola K, Angenieux B, Tekaya M, et al. Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Invest Ophthalmol Vis Sci 2007;48:446-54.
73. Djojosubroto MW, Arsenijevic Y. Retinal stem cells: promising candidates for retina transplantation. Cell Tissue Res 2008;331:347-57.
74. Ballios BG, Cooke MJ, van der Kooy D, Shoichet MS. A hydrogel-based stem cell delivery system to treat retinal degenerative diseases. Biomaterials 2010;31:2555-64.
75. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature 2006; 444:203-7.
76. Calvert PD, Krasnoperova NV, Lyubarsky AL, et al. Phototransduction in transgenicmice after targeted deletion of the rod transducin α-subunit. Proc Natl Acad Sci USA 2000;97:13913-8.
77. Tremblay F, Abdel-Majid RM, Neumann PE. Electroretinographic oscillatory potentials are reduced in adenylyl cyclase type I deficient mice. Vision Res 2002;42:1715-25.
78. Prusky GT, Alam NM, Beekman S, Douglas RM. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 2004;45:4611-6.
79. Kinouchi R, Takeda M, Yang L, et al. Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat Neurosci 2003;6:863-8.
80. Klassen HJ, Ng TF, Kurimoto Y, et al. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest Ophthalmol Vis Sci 2004;45:4167-73.
81. Redenti S, Neeley WL, Rompani S, et al. Engineering retinal progenitor cell and scrollable poly(glycerol-sebacate) composites for expansion and subretinal transplantation. Biomaterials 2009;30:3405-14.
82. Neeley WL, Redenti S, Klassen H, et al. A microfabricated scaffold for retinal progenitor cell grafting. Biomaterials 2008; 29:418-26.
83. Tao S, Young C, Redenti S, et al. Survival, migration and differentiation of retinal progenitor cells transplanted on micro-machined poly(methyl methacrylate) scaffolds to the subretinal space. Lab Chip 2007;7:695-701.
84. Tomita M, Lavik E, Klassen H, Zahir T, Langer R, Young MJ. Biodegradable polymer composite grafts promote the survival and differentiation of retinal progenitor cells. Stem Cells 2005; 23:1579-88.
85. Hogg RE, Chakravarthy U. Visual function and dysfunction in early and late age-related maculopathy. Prog Retin Eye Res 2006;25:249-76.
86. Arden GB, Sidman RL, Arap W, Schlingemann RO. Spare the rod and spoil the eye. Br J Ophthalmol 2005;89:764-9.
87. Rakoczy PE, Yu MJT, Nusinowitz S, Chang B, Heckenlively JR. Mouse models of age-related macular degeneration. Exp Eye Res 2006;82:741-52.
88. Ding X, Patel M, Chan C-C. Molecular pathology of age-related macular degeneration. Prog Retin Eye Res 2009;28:1-18.
89. Nishida A, Furukawa A, Koike C, et al. Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 2003;6:1255-63.
90. Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL. Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet 1999;23:466-70.
91. Burmeister M, Novak J, Liang M-Y, et al. Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat Genet 1996;12:376-84.
92. Livne-Bar I, Pacal M, Cheung MC, et al. Chx10 is required to block photoreceptor differentiation but is dispensable for progenitor proliferation in the postnatal retina. Proc Natl Acad Sci USA 2006;103:4988-93.
93. Dorval KM, Bobechko BP, Ahmad KF, Bremner R. Transcriptional activity of the paired-like homeodomain proteins CHX10 and VSX1. J Biol Chem 2005;280:10100-8.