Generation of retinal ganglion-like cells from reprogrammed mouse fibroblasts

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 11, 2010, Pages 5970-5978

  Chen, Mengfei ^a,b   Chen, Qin ^a   Sun, Xuerong ^a   Shen, Wenjuan ^c   Liu, Bingqian ^a   Zhong, Xiufeng ^a,d   Leng, Yunxia ^a   Li, Chunmei ^a   Zhang, Weizhong ^a   Chai, Fang ^a   Huang, Bing ^a   Gao, Qianying ^a   Xiang, Andy Peng ^b   Zhuo, Yehong ^a   Ge, Jian ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICKKOPF 1 PROTEIN; KRUPPEL LIKE FACTOR 4; NESTIN; NEUROGENIN 3; NOGGIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR ISLET 1; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR POU4F2; TRANSCRIPTION FACTOR RX1; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR THY1.2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE CONTROL; GENE OVEREXPRESSION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CELLS, CULTURED; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, INBRED BALB C; RETINAL GANGLION CELLS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 79551666633     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4504     Document Type: Article

References (70)

1. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature. 2006;444: 203-207.
2. Spaide RF. The potential of pluripotent cells in vitreoretinal diseases. Retina. 2008;28:1031-1034.
3. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154-156.
4. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634-7638.
5. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282: 1145-1147.
6. Vugler A, Lawrence J, Walsh J, et al. Embryonic stem cells and retinal repair. Mech Dev. 2007;124:807-829.
7. Meyer JS, Katz ML, Maruniak JA, Kirk MD. Embryonic stem cellderived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells. 2006;24: 274-283.
8. Ikeda H, Osakada F, Watanabe K, et al. Generation of Rx+/Pax6+ neural retinal precursors from embryonic stem cells. Proc Natl Acad Sci U S A. 2005;102:11331-11336.
9. Lamba DA, Karl MO, Ware CB, Reh TA. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci U S A. 2006;103:12769-12774.
10. 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;26:215-224.
11. Jagatha B, Divya MS, Sanalkumar R, et al. In vitro differentiation of retinal ganglion-like cells from embryonic stem cell derived neural progenitors. Biochem Biophys Res Commun. 2009;380:230-235.
12. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663-676.
13. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell.2007;131:861-872.
14. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318: 1917-1920.
15. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature. 2008;451:141-146.
16. Lowry WE, Richter L, Yachechko R, et al. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci U S A. 2008;105:2883-2888.
17. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell. 2007;1: 39-49.
18. Park IH, Arora N, Huo H, et al. Disease-specific induced pluripotent stem cells. Cell. 2008;134:877-886.
19. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol.2009;27:275-280.
20. Karumbayaram S, Novitch BG, Patterson M, et al. Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells. 2009;27:806-811.
21. Wernig M, Zhao JP, Pruszak J, et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A. 2008;105:5856-5861.
22. Hanna J, Wernig M, Markoulaki S, et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science. 2007;318:1920-1923.
23. Tateishi K, He J, Taranova O, Liang G, D'Alessio AC, Zhang Y. Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J Biol Chem. 2008;283:31601-31607.
24. Mauritz C, Schwanke K, Reppel M, et al. Generation of functional murine cardiac myocytes from induced pluripotent stem cells. Circulation. 2008;118:507-517.
25. Narazaki G, Uosaki H, Teranishi M, et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation. 2008;118:498-506.
26. Hirami Y, Osakada F, Takahashi K, et al. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci Lett. 2009;458:126-131.
27. Osakada F, Jin ZB, Hirami Y, et al. In vitro differentiation of retinal cells from human pluripotent stem cells by small-molecule induction. J Cell Sci. 2009;122:3169-3179.
28. Zuber ME, Gestri G, Viczian AS, Barsacchi G, Harris WA. Specification of the vertebrate eye by a network of eye field transcription factors. Development. 2003;130:5155-5167.
29. Mu X, Klein WH. A gene regulatory hierarchy for retinal ganglion cell specification and differentiation. Semin Cell Dev Biol. 2004; 15:115-123.
30. Mu X, Fu X, Sun H, Beremand PD, Thomas TL, Klein WH. A gene network downstream of transcription factor Math5 regulates retinal progenitor cell competence and ganglion cell fate. Dev Biol.2005;280:467-481.
31. Huangfu D, Osafune K, Maehr R, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol. 2008;26:1269-1275.
32. Ferri AL, Cavallaro M, Braida D, et al. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development. 2004;131:3805-3819.
33. Ellis P, Fagan BM, Magness ST, et al. Sox2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci. 2004;26:148-165.
34. Fantes J, Ragge NK, Lynch SA, et al. Mutations in Sox2 cause anophthalmia. Nat Genet. 2003;33:461-463.
35. Kamachi Y, Uchikawa M, Collignon J, Lovell-Badge R, Kondoh H. Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development. 1998;125:2521-2532.
36. Hever AM, Williamson KA, van Heyningen V. Developmental malformations of the eye: the role of Pax6, Sox2 and Otx2. Clin Genet.2006;69:459-470.
37. Taranova OV, Magness ST, Fagan BM, et al. Sox2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 2006;20:1187-1202.
38. Ma W, Yan RT, Li X, Wang SZ. Reprogramming retinal pigment epithelium to differentiate toward retinal neurons with Sox2. Stem Cells. 2009;27:1376-1387.
39. Lin YP, Ouchi Y, Satoh S, Watanabe S. Sox2 plays a role in the induction of amacrine and Muller glial cells in mouse retinal progenitor cells. Invest Ophthalmol Vis Sci. 2009;50:68-74.
40. Danno H, Michiue T, Hitachi K, Yukita A, Ishiura S, Asashima M. Molecular links among the causative genes for ocular malformation: Otx2 and Sox2 coregulate Rax expression. Proc Natl Acad Sci U S A.2008;105:5408-5413.
41. Takahashi K, Okita K, Nakagawa M, Yamanaka S. Induction of pluripotent stem cells from fibroblast cultures. Nat Protocols.2007;2:3081-3089.
42. Meissner A, Wernig M, Jaenisch R. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol. 2007;25:1177-1181.
43. Chen M, Sun X, Jiang R, et al. Role of MEF feeder cells in direct reprogramming of mousetail-tip fibroblasts. Cell Biol Int. 2009;33: 1268-1273.
44. Guo Y, Saloupis P, Shaw SJ, Rickman DW. Engraftment of adult neural progenitor cells transplanted to rat retina injured by transient ischemia. Invest Ophthalmol Vis Sci. 2003;44:3194-3201.
45. Kondo T, Johnson SA, Yoder MC, Romand R, Hashino E. Sonic hedgehog and retinoic acid synergistically promote sensory fate specification from bone marrow-derived pluripotent stem cells. Proc Natl Acad Sci U S A. 2005;102:4789-4794.
46. Tomita M, Mori T, Maruyama K, et al. A comparison of neural differentiation and retinal transplantation with bone marrow-derived cells and retinal progenitor cells. Stem Cells. 2006;24:2270-2278.
47. Brambrink T, Foreman R, Welstead GG, et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell. 2008;2:151-159.
48. Ying QL, Nichols J, Chambers I, Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell. 2003;115:281-292.
49. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med. 2004;10:55-63.
50. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell. 2001;105:43-55.
51. Riesenberg AN, Le TT, Willardsen MI, Blackburn DC, Vetter ML, Brown NL. Pax6 regulation of Math5 during mouse retinal neurogenesis. Genesis. 2009;47:175-187.
52. Nelson BR, Gumuscu B, Hartman BH, Reh TA. Notch activity is downregulated just prior to retinal ganglion cell differentiation. Dev Neurosci. 2006;28:128-141.
53. Matter-Sadzinski L, Puzianowska-Kuznicka M, Hernandez J, Ballivet M, Matter JM. A bHLH transcriptional network regulating the specification of retinal ganglion cells. Development. 2005;132:3907-3921.
54. Soldner F, Hockemeyer D, Beard C, et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell. 2009;136:964-977.
55. Graham V, Khudyakov J, Ellis P, Pevny L. Sox2 functions to maintain neural progenitor identity. Neuron. 2003;39:749-765.
56. Silver SJ, Rebay I. Signaling circuitries in development: insights from the retinal determination gene network. Development. 2005; 132:3-13.
57. Lad EM, Cheshier SH, Kalani MY. Wnt signaling in retinal development and disease. Stem Cells Dev. 2009;18:7-16.
58. Smith JR, Vallier L, Lupo G, Alexander M, Harris WA, Pedersen RA. Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm. Dev Biol.2008;313:107-117.
59. Gerrard L, Rodgers L, Cui W. Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells. 2005;23:1234-1241.
60. Pera MF, Andrade J, Houssami S, et al. Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J Cell Sci. 2004;117:1269-1280.
61. Meyer-Franke A, Kaplan MR, Pfrieger FW, Barres BA. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron.1995;15:805-819.
62. Brown NL, Patel S, Brzezinski J, Glaser T. Math5 is required for retinal ganglion cell and optic nerve formation. Development.2001;128:2497-2508.
63. Wang SW, Kim BS, Ding K, et al. Requirement for Math5 in the development of retinal ganglion cells. Genes Dev. 2001;15:24-29.
64. Liu W, Mo Z, Xiang M. The Ath5 proneural genes function upstream of Brn3 POU domain transcription factor genes to promote retinal ganglion cell development. Proc Natl Acad Sci U S A.2001;98:1649-1654.
65. Yang Z, Ding K, Pan L, Deng M, Gan L. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol.2003;264:240-254.
66. Hatakeyama J, Kageyama R. Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol. 2004;15:83-89.
67. Silva AO, Ercole CE, McLoon SC. Regulation of ganglion cell production by Notch signaling during retinal development. J Neurobiol.2003;54:511-524.
68. Gan L, Wang SW, Huang Z, Klein WH. POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev Biol. 1999;210:469-480.
69. Yao J, Sun X, Wang Y, Xu G, Qian J. Math5 promotes retinal ganglion cell expression patterns in retinal progenitor cells. Mol Vis. 2007;13:1066-1072.
70. Kinouchi R, Takeda M, Yang L, et al. Robust neural integration from retinal transplants in mice deficient in GFAP and vimentin. Nat Neurosci. 2003;6:863-868.