In vitro expanded stem cells from the developing retina fail to generate photoreceptors but differentiate into myelinating oligodendrocytes

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Czekaj, Magdalena ^a   Haas, Jochen ^a   Gebhardt, Marlen ^b   Müller Reichert, Thomas ^d   Humphries, Peter ^c   Farrar, Jane ^c   Bartsch, Udo ^b   Ader, Marius ^a  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; MYELIN; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CHX10; TRANSCRIPTION FACTOR RAX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL ASSAY; CELL CULTURE; CELL ISOLATION; CELL LINEAGE; CELL RENEWAL; CHX10 GENE; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GLIA CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYELINATION; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PHOTORECEPTOR; PROTEIN EXPRESSION; RAX GENE; RETINA STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL EXPANSION; STEM CELL TRANSPLANTATION;

ANIMALS; ASTROCYTES; AXONS; CELL DIFFERENTIATION; DOWN-REGULATION; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; MICE; MICE, INBRED C57BL; MYELIN SHEATH; ORGAN SPECIFICITY; PHOTORECEPTOR CELLS, VERTEBRATE; RECEPTORS, NOTCH; RETINA; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS;

MAMMALIA;

EID: 84864328427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041798     Document Type: Article

References (90)

1. Delyfer MN, Leveillard T, Mohand-Said S, Hicks D, Picaud S, et al. (2004) Inherited retinal degenerations: therapeutic prospects. Biology of the cell/under the auspices of the European Cell Biology Organization 96: 261-269.
2. Berson EL, Rosner B, Sandberg MA, Weigel-DiFranco C, Moser A, et al. (2004) Clinical trial of docosahexaenoic acid in patients with retinitis pigmentosa receiving vitamin A treatment. Archives of ophthalmology 122: 1297-1305.
3. Maeda T, Cideciyan AV, Maeda A, Golczak M, Aleman TS, et al. (2009) Loss of cone photoreceptors caused by chromophore depletion is partially prevented by the artificial chromophore pro-drug, 9-cis-retinyl acetate. Human molecular genetics 18: 2277-2287.
4. Zrenner E, Bartz-Schmidt KU, Benav H, Besch D, Bruckmann A, et al. (2011) Subretinal electronic chips allow blind patients to read letters and combine them to words. Proceedings Biological sciences/The Royal Society 278: 1489-1497.
5. Millington-Ward S, Chadderton N, O'Reilly M, Palfi A, Goldmann T, et al. (2011) Suppression and Replacement Gene Therapy for Autosomal Dominant Disease in a Murine Model of Dominant Retinitis Pigmentosa. Molecular Therapy 19: 642-649.
6. Farrar GJ, Palfi A, O'Reilly M, (2010) Gene therapeutic approaches for dominant retinopathies. Current gene therapy 10: 381-388.
7. Michalakis S, Muhlfriedel R, Tanimoto N, Krishnamoorthy V, Koch S, et al. (2010) Restoration of Cone Vision in the CNGA3(-/-) Mouse Model of Congenital Complete Lack of Cone Photoreceptor Function. Human Gene Therapy 21: 1181-1181.
8. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, et al. (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444: 203-207.
9. Bartsch U, Oriyakhel W, Kenna PF, Linke S, Richard G, et al. (2008) Retinal cells integrate into the outer nuclear layer and differentiate into mature photoreceptors after subretinal transplantation into adult mice. Experimental eye research 86: 691-700.
10. Lakowski J, Baron M, Bainbridge J, Barber AC, Pearson RA, et al. (2010) Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Human molecular genetics 19: 4545-4559.
11. Eberle D, Schubert S, Postel K, Corbeil D, Ader M, (2011) Increased integration of transplanted CD73-positive photoreceptor precursors into adult mouse retina. Investigative Ophthalmology & Visual Science 52: 6462-6471.
12. Pearson RA, Barber AC, Rizzi M, Hippert C, Xue T, et al. (2012) Restoration of vision after transplantation of photoreceptors. Nature 485: 99-103.
13. Reynolds BA, Weiss S, (1992) Generation of Neurons and Astrocytes from Isolated Cells of the Adult Mammalian Central-Nervous-System. Science 255: 1707-1710.
14. Reynolds BA, Tetzlaff W, Weiss S, (1992) A Multipotent Egf-Responsive Striatal Embryonic Progenitor-Cell Produces Neurons and Astrocytes. Journal of Neuroscience 12: 4565-4574.
15. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, et al. (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS biology 3: 1594-1606.
16. Gabay L, Lowell S, Rubin LL, Anderson DJ, (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40: 485-499.
17. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Gotz M, (2004) Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Molecular and cellular neurosciences 25: 664-678.
18. Pollard SM, Wallbank R, Tomlinson S, Grotewold L, Smith A, (2008) Fibroblast growth factor induces a neural stem cell phenotype in foetal forebrain progenitors and during embryonic stem cell differentiation. Molecular and cellular neurosciences 38: 393-403.
19. Conti L, Cattaneo E, (2010) Neural stem cell systems: physiological players or in vitro entities? Nature reviews Neuroscience 11: 176-187.
20. Coles BL, Angenieux B, Inoue T, Del Rio-Tsonis K, Spence JR, et al. (2004) Facile isolation and the characterization of human retinal stem cells. Proceedings of the National Academy of Sciences of the United States of America 101: 15772-15777.
21. Klassen HJ, Ng TF, Kurimoto Y, Kirov I, Shatos M, et al. (2004) Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Investigative Ophthalmology & Visual Science 45: 4167-4173.
22. Merhi-Soussi F, Angenieux B, Canola K, Kostic C, Tekaya M, et al. (2006) High yield of cells committed to the photoreceptor fate from expanded mouse retinal stem cells. Stem cells 24: 2060-2070.
23. Canola K, Arsenijevic Y, (2007) Generation of cells committed towards the photoreceptor fate for retinal transplantation. Neuroreport 18: 851-855.
24. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, et al. (2000) Retinal stem cells in the adult mammalian eye. Science 287: 2032-2036.
25. Cicero SA, Johnson D, Reyntjens S, Frase S, Connell S, et al. (2009) Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 106: 6685-6690.
26. Gualdoni S, Baron M, Lakowski J, Decembrini S, Smith AJ, et al. (2010) Adult ciliary epithelial cells, previously identified as retinal stem cells with potential for retinal repair, fail to differentiate into new rod photoreceptors. Stem cells 28: 1048-1059.
27. Marquardt T, (2003) Transcriptional control of neuronal diversification in the retina. Progress in Retinal and Eye Research 22: 567-577.
28. Hatakeyama J, Kageyama R, (2004) Retinal cell fate determination and bHLH factors. Seminars in cell & developmental biology 15: 83-89.
29. Ffrench-Constant C, Miller RH, Burne JF, Raff MC, (1988) Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. Journal of neurocytology 17: 13-25.
30. Bartsch U, Faissner A, Trotter J, Dorries U, Bartsch S, et al. (1994) Tenascin Demarcates the Boundary between the Myelinated and Nonmyelinated Part of Retinal Ganglion-Cell Axone in the Developing and Adult-Mouse. Journal of Neuroscience 14: 4756-4768.
31. Pollard SM, Conti L, Sun YR, Goffredo D, Smith A, (2006) Adherent neural stem (NS) cells from fetal and adult forebrain. Cerebral cortex 16: I112-I120.
32. Jalava NS, Lopez-Picon FR, Kukko-Lukjanov TK, Holopainen IE, (2007) Changes in microtubule-associated protein-2 (MAP2) expression during development and after status epilepticus in the immature rat hippocampus. International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience 25: 121-131.
33. Hafidi A, Fellous A, Ferhat L, Romand MR, Romand R, (1992) Developmental differentiation of MAP2 expression in the central versus the peripheral and efferent projections of the inner ear. The Journal of comparative neurology 323: 423-431.
34. Torres-Fernandez O, Yepes GE, Gomez JE, Pimienta HJ, (2005) Calbindin distribution in cortical and subcortical brain structures of normal and rabies-infected mice. The International journal of neuroscience 115: 1375-1382.
35. Anelli R, Heckman CJ, (2005) The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord. Journal of neurocytology 34: 369-385.
36. Munkle MC, Waldvogel HJ, Faull RL, (2000) The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus. Journal of chemical neuroanatomy 19: 155-173.
37. Weyer A, Schilling K, (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. Journal of neuroscience research 73: 400-409.
38. Wu P, Tarasenko YI, Gu Y, Huang LY, Coggeshall RE, et al. (2002) Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nature neuroscience 5: 1271-1278.
39. Yoon K, Gaiano N, (2005) Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nature neuroscience 8: 709-715.
40. Louvi A, Artavanis-Tsakonas S, (2006) Notch signalling in vertebrate neural development. Nature reviews Neuroscience 7: 93-102.
41. Nelson BR, Hartman BH, Georgi SA, Lan MS, Reh TA, (2007) Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Developmental biology 304: 479-498.
42. Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, et al. (2010) Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem cells 28: 955-964.
43. Glaser T, Pollard SM, Smith A, Brustle O, (2007) Tripotential differentiation of adherently expandable neural stem (NS) cells. PloS one 2: e298.
44. Zhou Q, Anderson DJ, (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109: 61-73.
45. Shibasaki K, Takebayashi H, Ikenaka K, Feng L, Gan L, (2007) Expression of the basic helix-loop-factor Olig2 in the developing retina: Olig2 as a new marker for retinal progenitors and late-born cells. Gene expression patterns: GEP 7: 57-65.
46. Cai J, Zhu Q, Zheng K, Li H, Qi Y, et al. (2010) Co-localization of Nkx6.2 and Nkx2.2 homeodomain proteins in differentiated myelinating oligodendrocytes. Glia 58: 458-468.
47. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, et al. (2002) Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes & development 16: 165-170.
48. Ader M, Meng J, Schachner M, Bartsch U, (2000) Formation of myelin after transplantation of neural precursor cells into the retina of young postnatal mice. Glia 30: 301-310.
49. Pressmar S, Ader M, Richard G, Schachner M, Bartsch U, (2001) The fate of heterotopically grafted neural precursor cells in the normal and dystrophic adult mouse retina. Investigative Ophthalmology & Visual Science 42: 3311-3319.
50. Lindvall O, Kokaia Z, Martinez-Serrano A, (2004) Stem cell therapy for human neurodegenerative disorders-how to make it work. Nature medicine 10.
51. Lindvall O, Kokaia Z, (2010) Stem cells in human neurodegenerative disorders-time for clinical translation? The Journal of clinical investigation 120: 29-40.
52. Lodi D, Iannitti T, Palmieri B, (2011) Stem cells in clinical practice: applications and warnings. Journal of experimental & clinical cancer research: CR 30: 9.
53. Klassen H, Sakaguchi DS, Young MJ, (2004) Stem cells and retinal repair. Progress in Retinal and Eye Research 23: 149-181.
54. Turner DL, Snyder EY, Cepko CL, (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4: 833-845.
55. Livesey R, Cepko C, (2001) Neurobiology. Developing order. Nature 413: 471, 473.
56. Lamba DA, Karl MO, Ware CB, Reh TA, (2006) Efficient generation of retinal progenitor cells from human embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 103: 12769-12774.
57. Lamba DA, Gust J, Reh TA, (2009) Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell stem cell 4: 73-79.
58. Lamba DA, McUsic A, Hirata RK, Wang PR, Russell D, et al. (2010) Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PloS one 5: e8763.
59. Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, et al. (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472: 51-56.
60. Meyer S, Nolte J, Opitz L, Salinas-Riester G, Engel W, (2010) Pluripotent embryonic stem cells and multipotent adult germline stem cells reveal similar transcriptomes including pluripotency-related genes. Molecular human reproduction 16: 846-855.
61. Takahashi M, Osakada F, Ikeda H, Mandai M, Wataya T, et al. (2008) Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nature Biotechnology 26: 215-224.
62. Takahashi M, Palmer TD, Takahashi J, Gage FH, (1998) Widespread integration and survival of adult-derived neural progenitor cells in the developing optic retina. Molecular and cellular neurosciences 12: 340-348.
63. Nishida A, Takahashi M, Tanihara H, Nakano I, Takahashi JB, et al. (2000) Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Investigative Ophthalmology & Visual Science 41: 4268-4274.
64. Klassen H, Kiilgaard JF, Zahir T, Ziaeian B, Kirov I, et al. (2007) Progenitor cells from the porcine neural retina express photoreceptor markers after transplantation to the subretinal space of allorecipients. Stem cells 25: 1222-1230.
65. Canola K, Angenieux B, Tekaya M, Quiambao A, Naash MI, et al. (2007) Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Investigative Ophthalmology & Visual Science 48: 446-454.
66. Mansergh FC, Vawda R, Millington-Ward S, Kenna PF, Haas J, et al. (2010) Loss of photoreceptor potential from retinal progenitor cell cultures, despite improvements in survival. Experimental eye research 91: 500-512.
67. Soderpalm AK, Fox DA, Karlsson JO, van Veen T, (2000) Retinoic acid produces rod photoreceptor selective apoptosis in developing mammalian retina. Investigative Ophthalmology & Visual Science 41: 937-947.
68. Qiu G, Seiler MJ, Mui C, Arai S, Aramant RB, et al. (2005) Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Experimental eye research 80: 515-525.
69. Gamm DM, Wright LS, Capowski EE, Shearer RL, Meyer JS, et al. (2008) Regulation of prenatal human retinal neurosphere growth and cell fate potential by retinal pigment epithelium and Mash1. Stem cells 26: 3182-3193.
70. Crawford TQ, Roelink H, (2007) The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling. Developmental dynamics: an official publication of the American Association of Anatomists 236: 886-892.
71. Taranova OV, Magness ST, Fagan BM, Wu Y, Surzenko N, et al. (2006) SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes & development 20: 1187-1202.
72. Matsushima D, Heavner W, Pevny LH, (2011) Combinatorial regulation of optic cup progenitor cell fate by SOX2 and PAX6. Development 138: 443-454.
73. Burmeister M, Novak J, Liang MY, Basu S, Ploder L, et al. (1996) Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nature genetics 12: 376-384.
74. Liu IS, Chen JD, Ploder L, Vidgen D, van der Kooy D, et al. (1994) Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13: 377-393.
75. Bernier G, Tetreault N, Champagne MP, (2009) The LIM homeobox transcription factor Lhx2 is required to specify the retina field and synergistically cooperates with Pax6 for Six6 trans-activation. Developmental biology 327: 541-550.
76. Schmitt S, Aftab U, Jiang C, Redenti S, Klassen H, et al. (2009) Molecular characterization of human retinal progenitor cells. Investigative Ophthalmology & Visual Science 50: 5901-5908.
77. Perry VH, Lund RD, (1990) Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons. Journal of neurocytology 19: 265-272.
78. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, et al. (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304: 1338-1340.
79. Alvarez-Buylla A, Lim DA, (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41: 683-686.
80. Ciccolini F, Svendsen CN, (1998) Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: Identification of neural precursors responding to both EGF and FGF-2. Journal of Neuroscience 18: 7869-7880.
81. Kessaris N, Jamen F, Rubin LL, Richardson WD, (2004) Cooperation between sonic hedgehog and fibroblast growth factor/MAPK signalling pathways in neocortical precursors. Development 131: 1289-1298.
82. Abematsu M, Kagawa T, Fukuda S, Inoue T, Takebayashi H, et al. (2006) Basic fibroblast growth factor endows dorsal telencephalic neural progenitors with the ability to differentiate into oligodendrocytes but not gamma-aminobutyric acidergic neurons. Journal of neuroscience research 83: 731-743.
83. Chandran S, Kato H, Gerreli D, Compston A, Svendsen CN, et al. (2003) FGF-dependent generation of oligodendrocytes by a hedgehog-independent pathway. Development 130: 6599-6609.
84. Trimarchi JM, Stadler MB, Cepko CL, (2008) Individual retinal progenitor cells display extensive heterogeneity of gene expression. PloS one 3: e1588.
85. FitzGibbon T, Nestorovski Z, (1997) Morphological consequences of myelination in the human retina. Experimental eye research 65: 809-819.
86. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y, (1997) 'Green mice' as a source of ubiquitous green cells. FEBS letters 407: 313-319.
87. Chan F, Bradley A, Wensel TG, Wilson JH, (2004) Knock-in human rhodopsin-GFP fusions as mouse models for human disease and targets for gene therapy. Proceedings of the National Academy of Sciences of the United States of America 101: 9109-9114.
88. Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, et al. (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nature genetics 15: 216-219.
89. Li T, Snyder WK, Olsson JE, Dryja TP, (1996) Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments. Proceedings of the National Academy of Sciences of the United States of America 93: 14176-14181.
90. Vasileva A, Tiedau D, Firooznia A, Muller-Reichert T, Jessberger R, (2009) Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Current biology: CB 19: 630-639.