Retinal stem cells: Promising candidates for retina transplantation

Cell and Tissue Research

Volumn 331, Issue 1, 2008, Pages 347-357

  Djojosubroto, Meta W ^a   Arsenijevic, Yvan ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Differentiation; Progenitor; Radial glia; Retina; Stem cells; Transplantation

Indexed keywords

CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CYTOLOGY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RETINA CELL; RETINA TRANSPLANTATION; REVIEW; RODENT; STEM CELL; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; HUMANS; RETINA; STEM CELL NICHE; STEM CELLS;

ANIMALIA; RODENTIA;

EID: 37249025199     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-007-0501-8     Document Type: Review

References (113)

1. Abdouh M, Bernier G (2006) In vivo reactivation of a quiescent cell population located in the ocular ciliary body of adult mammals. Exp Eye Res 83:153-164
2. Agathocleous M, Locker M, Harris WA, Perron M (2007) A general role of hedgehog in the regulation of proliferation. Cell Cycle 6:156-159
3. Ahmad I, Tang L, Pham H (2000) Identification of neural progenitors in the adult mammalian eye. Biochem Biophys Res Commun 270:517-521
4. Akagi T, Haruta M, Akita J, Nishida A, Honda Y, Takahashi M (2003) Different characteristics of rat retinal progenitor cells from different culture periods. Neurosci Lett 341:213-216
5. Altshuler D, Cepko C (1992) A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. Development 114:947-957
6. Altshuler D, Lo Turco JJ, Rush J, Cepko C (1993) Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119:1317-1328
7. Anchan RM, Reh TA, Angello J, Balliet A, Walker M (1991) EGF and TGF-alpha stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6:923-936
8. Angenieux B, Schorderet DF, Arsenijevic Y (2006) Epidermal growth factor is a neuronal differentiation factor for retinal stem cells in vitro. Stem Cells 24:696-706
9. Arai S, Thomas BB, Seiler MJ, Aramant RB, Qiu G, Mui C, Juan E de, Sadda SR (2004) Restoration of visual responses following transplantation of intact retinal sheets in rd mice. Exp Eye Res 79:331-341
10. Arnhold S, Klein H, Semkova I, Addicks K, Schraermeyer U (2004) 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
11. Banin E, Obolensky A, Idelson M, Hemo I, Reinhardtz E, Pikarsky E, Ben Hur T, Reubinoff B (2006) Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells. Stem Cells 24:246-257
12. Belecky-Adams T, Tomarev S, Li HS, Ploder L, McInnes RR, Sundin O, Adler R (1997) Pax-6, Prox 1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest Ophthalmol Vis Sci 38:1293-1303
13. Belliveau MJ, Cepko CL (1999) Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 126:555-566
14. Canola K, Arsenijevic Y (2007) Generation of cells committed towards the photoreceptor fate for retinal transplantation. Neuroreport 18:851-855
15. Canola K, Angenieux B, Tekaya M, Quiambao A, Naash MI, Munier FL, Schorderet DF, Arsenijevic Y (2007) 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 48:446-454
16. Castelo-Branco G, Wagner J, Rodriguez FJ, Kele J, Sousa K, Rawal N, Pasolli HA, Fuchs E, Kitajewski J, Arenas E (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci USA 100:12747-12752
17. Cayouette M, Poggi L, Harris WA (2006) Lineage in the vertebrate retina. Trends Neurosci 29:563-570
18. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589-595
19. Coles BL, Angenieux B, Inoue T, Rio-Tsonis K, Spence JR, McInnes RR, Arsenijevic Y, Kooy D van der (2004) Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA 101:15772-15777
20. Coles BL, Horsford DJ, McInnes RR, Kooy D van der (2006) Loss of retinal progenitor cells leads to an increase in the retinal stem cell population in vivo. Eur J Neurosci 23:75-82
21. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283
22. Das AV, James J, Rahnenfuhrer J, Thoreson WB, Bhattacharya S, Zhao X, Ahmad I (2005) Retinal properties and potential of the adult mammalian ciliary epithelium stem cells. Vision Res 45:1653-1666
23. Das AV, Mallya KB, Zhao X, Ahmad F, Bhattacharya S, Thoreson WB, Hegde GV, Ahmad I (2006a) Neural stem cell properties of Muller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299:283-302
24. Das AV, Zhao X, James J, Kim M, Cowan KH, Ahmad I (2006b) Neural stem cells in the adult ciliary epithelium express GFAP and are regulated by Wnt signaling. Biochem Biophys Res Commun 339:708-716
25. Dorsky RI, Rapaport DH, Harris WA (1995) Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14:487-496
26. Dyer MA, Cepko CL (2001) p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J Neurosci 21:4259-4271
27. Elliott J, Cayouette M, Gravel C (2006) The CNTF/LIF signaling pathway regulates developmental programmed cell death and differentiation of rod precursor cells in the mouse retina in vivo. Dev Biol 300:583-598
28. Ezzeddine ZD, Yang X, DeChiara T, Yancopoulos G, Cepko CL (1997) Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina. Development 124:1055-1067
29. Fernald RD (1990) Teleost vision: seeing while growing. J Exp Zool Suppl 5:167-180
30. Fischer AJ, Reh TA (2000) Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 220:197-210
31. Fischer AJ, Reh TA (2003) Growth factors induce neurogenesis in the ciliary body. Dev Biol 259:225-240
32. Fischer AJ, McGuire CR, Dierks BD, Reh TA (2002) Insulin and fibroblast growth factor 2 activate a neurogenic program in Muller glia of the chicken retina. J Neurosci 22:9387-9398
33. Fuhrmann S, Kirsch M, Hofmann HD (1995) Ciliary neurotrophic factor promotes chick photoreceptor development in vitro. Development 121:2695-2706
34. Fuhrmann S, Heller S, Rohrer H, Hofmann HD (1998) A transient role for ciliary neurotrophic factor in chick photoreceptor development. J Neurobiol 37:672-683
35. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL (2000) rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394
36. Gaasterland DE, Pederson JE, MacLellan HM, Reddy VN (1979) Rhesus monkey aqueous humor composition and a primate ocular perfusate. Invest Ophthalmol Vis Sci 18:1139-1150
37. Ghosh F, Arner K, Ehinger B (1998) Transplant of full-thickness embryonic rabbit retina using pars plana vitrectomy. Retina 18:136-142
38. Gotz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21:1031-1044
39. Gregg C, Weiss S (2003) Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells. J Neurosci 23:11587-11601
40. Guo Y, Saloupis P, Shaw SJ, Rickman DW (2003) Engraftment of adult neural progenitor cells transplanted to rat retina injured by transient ischemia. Invest Ophthalmol Vis Sci 44:3194-3201
41. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde YA, Gotz M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308-315
42. Hicks D, Courtois Y (1992) Fibroblast growth factor stimulates photoreceptor differentiation in vitro. J Neurosci 12:2022-2033
43. Hunter DD, Murphy MD, Olsson CV, Brunken WJ (1992) S-laminin expression in adult and developing retinae: a potential cue for photoreceptor morphogenesis. Neuron 8:399-413
44. Jadhav AP, Cho SH, Cepko CL (2006) Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc Natl Acad Sci USA 103:18998-19003
45. James J, Das AV, Bhattacharya S, Chacko DM, Zhao X, Ahmad I (2003) In vitro generation of early-born neurons from late retinal progenitors. J Neurosci 23:8193-8203
46. Kelley MW, Turner JK, Reh TA (1994) Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120:2091-2102
47. Kelley MW, Turner JK, Reh TA (1995) Regulation of proliferation and photoreceptor differentiation in fetal human retinal cell cultures. Invest Ophthalmol Vis Sci 36:1280-1289
48. Kelley MW, Williams RC, Turner JK, Creech-Kraft JM, Reh TA (1999) Retinoic acid promotes rod photoreceptor differentiation in rat retina in vivo. Neuroreport 10:2389-2394
49. Khanna H, Akimoto M, Siffroi-Fernandez S, Friedman JS, Hicks D, Swaroop A (2006) Retinoic acid regulates the expression of photoreceptor transcription factor NRL. J Biol Chem 281:27327-27334
50. Kirsch M, Schulz-Key S, Wiese A, Fuhrmann S, Hofmann H (1998) Ciliary neurotrophic factor blocks rod photoreceptor differentiation from postmitotic precursor cells in vitro. Cell Tissue Res 291:207-216
51. Klassen HJ, Ng TF, Kurimoto Y, Kirov I, Shatos M, Coffey P, Young MJ (2004) Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest Ophthalmol Vis Sci 45:4167-4173
52. Klassen H, Kiilgaard JF, Zahir T, Ziaeian B, Kirov I, Scherfig E, Warfvinge K, Young MJ (2007) Progenitor cells from the porcine neural retina express photoreceptor markers after transplantation to the subretinal space of allorecipients. Stem Cells 25:1222-1230
53. Kubo F, Takeichi M, Nakagawa S (2003) Wnt2b controls retinal cell differentiation at the ciliary marginal zone. Development 130:587-598
54. Kubota A, Nishida K, Nakashima K, Tano Y (2006) Conversion of mammalian Muller glial cells into a neuronal lineage by in vitro aggregate-culture. Biochem Biophys Res Commun 351:514-520
55. Lamba DA, Karl MO, Ware CB, Reh TA (2006) Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci USA 103:12769-12774
56. Lavik EB, Klassen H, Warfvinge K, Langer R, Young MJ (2005) Fabrication of degradable polymer scaffolds to direct the integration and differentiation of retinal progenitors. Biomaterials 26:3187-3196
57. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595
58. Lillien L, Cepko C (1992) Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF alpha. Development 115:253-266
59. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444:203-207
60. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P (2001) Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105:43-55
61. Mayer EJ, Hughes EH, Carter DA, Dick AD (2003) Nestin positive cells in adult human retina and in epiretinal membranes. Br J Ophthalmol 87:1154-1158
62. Merhi-Soussi F, Angenieux B, Canola K, Kostic C, Tekaya M, Hornfeld D, Arsenijevic Y (2006) High yield of cells committed to the photoreceptor fate from expanded mouse retinal stem cells. Stem Cells 24:2060-2070
63. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425:962-967
64. Moshiri A, Reh TA (2004) Persistent progenitors at the retinal margin of ptc+/- mice. J Neurosci 24:229-237
65. Nelson BR, Gumuscu B, Hartman BH, Reh TA (2006) Notch activity is downregulated just prior to retinal ganglion cell differentiation. Dev Neurosci 28:128-141
66. Nelson BR, Hartman BH, Georgi SA, Lan MS, Reh TA (2007) Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Dev Biol 304:479-498
67. Neophytou C, Vernallis AB, Smith A, Raff MC (1997) Muller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development. Development 124:2345-2354
68. Nishida A, Takahashi M, Tanihara H, Nakano I, Takahashi JB, Mizoguchi A, Ide C, Honda Y (2000) Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Invest Ophthalmol Vis Sci 41:4268-4274
69. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA 101:13654-13659
70. Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M (2007) Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 27:4210-4219
71. Otani A, Dorrell MI, Kinder K, Moreno SK, Nusinowitz S, Banin E, Heckenlively J, Friedlander M (2004) Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J Clin Invest 114:765-774
72. Otteson DC, Hitchcock PF (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43:927-936
73. Perron M, Harris WA (2000) Retinal stem cells in vertebrates. Bioessays 22:685-688
74. Perron M, Kanekar S, Vetter ML, Harris WA (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev Biol 199:185-200
75. Qiu G, Seiler MJ, Arai S, Aramant RB, Sadda SR (2004) Alternative culture conditions for isolation and expansion of retinal progenitor cells. Curr Eye Res 28:327-336
76. Qiu G, Seiler MJ, Mui C, Arai S, Aramant RB, Juan E de Jr, Sadda S (2005) Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Exp Eye Res 80:515-525
77. Radtke ND, Aramant RB, Seiler MJ, Petry HM, Pidwell D (2004) Vision change after sheet transplant of fetal retina with retinal pigment epithelium to a patient with retinitis pigmentosa. Arch Ophthalmol 122:1159-1165
78. Rapaport DH, Patheal SL, Harris WA (2001) Cellular competence plays a role in photoreceptor differentiation in the developing Xenopus retina. J Neurobiol 49:129-141
79. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474:304-324
80. Reh TA, Kljavin IJ (1989) Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J Neurosci 9:4179-4189
81. Riobo NA, Manning DR (2007) Pathways of signal transduction employed by vertebrate Hedgehogs. Biochem J 403:369-379
82. Roger J, Brajeul V, Thomasseau S, Hienola A, Sahel JA, Guillonneau X, Goureau O (2006) Involvement of pleiotrophin in CNTF-mediated differentiation of the late retinal progenitor cells. Dev Biol 298:527-539
83. Rubio D, Garcia-Castro J, Martin MC, de la FR, Cigudosa JC, Lloyd AC, Bernad A (2005) Spontaneous human adult stem cell transformation. Cancer Res 65:3035-3039
84. Sagdullaev BT, Aramant RB, Seiler MJ, Woch G, McCall MA (2003) Retinal transplantation-induced recovery of retinotectal visual function in a rodent model of retinitis pigmentosa. Invest Ophthalmol Vis Sci 44:1686-1695
85. Sarmento LM, Huang H, Limon A, Gordon W, Fernandes J, Tavares MJ, Miele L, Cardoso AA, Classon M, Carlesso N (2005) Notch1 modulates timing of G1-S progression by inducing SKP2 transcription and p27 Kip1 degradation. J Exp Med 202:157-168
86. Saxena MT, Schroeter EH, Mumm JS, Kopan R (2001) Murine notch homologs (N1-4) undergo presenilin-dependent proteolysis. J Biol Chem 276:40268-40273
87. Schraermeyer U, Thumann G, Luther T, Kociok N, Armhold S, Kruttwig K, Andressen C, Addicks K, Bartz-Schmidt KU (2001) Subretinally transplanted embryonic stem cells rescue photoreceptor cells from degeneration in the RCS rats. Cell Transplant 10:673-680
88. Schulz-Key S, Hofmann HD, Beisenherz-Huss C, Barbisch C, Kirsch M (2002) Ciliary neurotrophic factor as a transient negative regulator of rod development in rat retina. Invest Ophthalmol Vis Sci 43:3099-3108
89. Shiras A, Chettiar S, Shepal V, Rajendran G, Prasad R, Shastry P (2007) Spontaneous transformation of human adult non-tumorigenic stem cells to cancer stem cells is driven by genomic instability in a human model of glioblastoma. Stem Cells (in press)
90. Silva AO, Ercole CE, McLoon SC (2003) Regulation of ganglion cell production by Notch signaling during retinal development. J Neurobiol 54:511-524
91. Silverman MS, Hughes SE (1989) Transplantation of photoreceptors to light-damaged retina. Invest Ophthalmol Vis Sci 30:1684-1690
92. Spence JR, Aycinena JC, Rio-Tsonis K (2007) Fibroblast growth factor-hedgehog interdependence during retina regeneration. Dev Dyn 236:1161-1174
93. Taranova OV, Magness ST, Fagan BM, Wu Y, Surzenko N, Hutton SR, Pevny LH (2006) SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev 20:1187-1202
94. Tomita M, Adachi Y, Yamada H, Takahashi K, Kiuchi K, Oyaizu H, Ikebukuro K, Kaneda H, Matsumura M, Ikehara S (2002) Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells 20:279-283
95. Tomita M, Lavik E, Klassen H, Zahir T, Langer R, Young MJ (2005) Biodegradable polymer composite grafts promote the survival and differentiation of retinal progenitor cells. Stem Cells 23:1579-1588
96. Tomita M, Mori T, Maruyama K, Zahir T, Ward M, Umezawa A, Young MJ (2006) A comparison of neural differentiation and retinal transplantation with bone marrow-derived cells and retinal progenitor cells. Stem Cells 24:2270-2278
97. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, McInnes RR, Kooy D van der (2000) Retinal stem cells in the adult mammalian eye. Science 287:2032-2036
98. Turner DL, Snyder EY, Cepko CL (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4:833-845
99. Watanabe T, Raff MC (1990) Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 4:461-467
100. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142-1145
101. Wetts R, Serbedzija GN, Fraser SE (1989) Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev Biol 136:254-263
102. Wojciechowski AB, Englund U, Lundberg C, Warfvinge K (2004) Survival and long distance migration of brain-derived precursor cells transplanted to adult rat retina. Stem Cells 22:27-38
103. Wu P, Tarasenko YI, Gu Y, Huang LY, Coggeshall RE, Yu Y (2002) Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nat Neurosci 5:1271-1278
104. Xu S, Sunderland ME, Coles BL, Kam A, Holowacz T, Ashery-Padan R, Marquardt T, McInnes RR, Kooy D van der (2007) The proliferation and expansion of retinal stem cells require functional Pax6. Dev Biol 304:713-721
105. Yang J, Klassen H, Pries M, Wang W, Nissen MH (2006) Aqueous humor enhances the proliferation of rat retinal precursor cells in culture, and this effect is partially reproduced by ascorbic acid. Stem Cells 24:2766-2775
106. Yang P, Seiler MJ, Aramant RB, Whittemore SR (2002) In vitro isolation and expansion of human retinal progenitor cells. Exp Neurol 177:326-331
107. Yang XJ (2004) Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin Cell Dev Biol 15:91-103
108. Yaron O, Farhy C, Marquardt T, Applebury M, Ashery-Padan R (2006) Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133:1367-1378
109. Young MJ, Ray J, Whiteley SJ, Klassen H, Gage FH (2000) Neuronal differentiation and morphological integration of hippocampal progenitor cells transplanted to the retina of immature and mature dystrophic rats. Mol Cell Neurosci 16:197-205
110. Young RW (1985) Cell differentiation in the retina of the mouse. Anat Rec 212:199-205
111. Zahir T, Klassen H, Young MJ (2005) Effects of ciliary neurotrophic factor on differentiation of late retinal progenitor cells. Stem Cells 23:424-432
112. Zahir T, Klassen H, Tomita M, Young MJ (2006) Sorbitol causes preferential selection of Muller glial precursors from late retinal progenitor cells in vitro. Mol Vis 12:1606-1614
113. Zencak D, Lingbeek M, Kostic C, Tekaya M, Tanger E, Hornfeld D, Jaquet M, Munier FL, Schorderet DF, Lohuizen M van, Arsenijevic Y (2005) Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation. J Neurosci 25:5774-5783