Multipotent stem cells isolated from the adult mouse retina are capable of producing functional photoreceptor cells

Cell Research

Volumn 23, Issue 6, 2013, Pages 788-802

  Li, Tianqing ^a   Lewallen, Michelle ^a   Chen, Shuyi ^a   Yu, Wei ^a   Zhang, Nian ^a   Xie, Ting ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Photoreceptor cells; Retinal stem cells

Indexed keywords

EYE PROTEIN; HOMEODOMAIN PROTEIN; NESTIN; PAIRED BOX TRANSCRIPTION FACTOR; REPRESSOR PROTEIN; SOX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX;

ANIMAL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; METABOLISM; MOUSE; MULTIPOTENT STEM CELL; PHOTORECEPTOR CELL; RETINA; RETINA DEGENERATION; TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EYE PROTEINS; HOMEODOMAIN PROTEINS; MICE; MULTIPOTENT STEM CELLS; NESTIN; PAIRED BOX TRANSCRIPTION FACTORS; PHOTORECEPTOR CELLS, VERTEBRATE; REPRESSOR PROTEINS; RETINA; RETINAL DEGENERATION; SOXB1 TRANSCRIPTION FACTORS;

MUS;

EID: 84878678210     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2013.48     Document Type: Article

References (53)

1. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature 2006; 444:203-207.
2. Pearson RA, Barber AC, Rizzi M, et al. Restoration of vision after transplantation of photoreceptors. Nature 2012; 485:99- 103.
3. Ikeda H, Osakada F, Watanabe K, et al. Generation of Rx+/ Pax6+ neural retinal precursors from embryonic stem cells. Proc Natl Acad Sci USA 2005; 102:11331-11336.
4. 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; 103:12769-12774.
5. 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.
6. Eiraku M, Takata N, Ishibashi H, et al. Self-organizing opticcup morphogenesis in three-dimensional culture. Nature 2011; 472:51-56.
7. Nakano T, Ando S, Takata N, et al. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012; 10:771-785.
8. 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; 4:73-79.
9. 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.
10. Tucker BA, Park IH, Qi SD, et al. Transplantation of adult mouse iPS cell-derived photoreceptor precursors restores retinal structure and function in degenerative mice. PloS One 2011; 6:e18992.
11. West EL, Gonzalez-Cordero A, Hippert C, et al. Defining the integration capacity of embryonic stem cell-derived photoreceptor precursors. Stem Cells 2012; 30:1424-1435.
12. Tropepe V, Coles BL, Chiasson BJ, et al. Retinal stem cells in the adult mammalian eye. Science 2000; 287:2032-2036.
13. Ahmad I, Tang L, Pham H. Identification of neural progenitors in the adult mammalian eye. Biochem Biophys Res Commun 2000; 270:517-521.
14. Coles BL, Angenieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA 2004; 101:15772-15777.
15. MacNeil A, Pearson RA, MacLaren RE, Smith AJ, Sowden JC, Ali RR. Comparative analysis of progenitor cells isolated from the iris, pars plana, and ciliary body of the adult porcine eye. Stem Cells 2007; 25:2430-2438.
16. 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; 106:6685-6690.
17. Gualdoni S, Baron M, Lakowski J, et al. Adult ciliary epithelial cells, previously identified as retinal stem cells with potential for retinal repair, fail to differentiate into new rod photoreceptors. Stem Cells 2010; 28:1048-1059.
18. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009; 32:149-184.
19. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. Latestage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 2007; 27:7028- 7040.
20. Yurco P, Cameron DA. Responses of Müller glia to retinal injury in adult zebrafish. Vision Res 2005; 45:991-1002.
21. Ooto S, Akagi T, Kageyama R, et al. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA 2004; 101:13654-13659.
22. Dyer MA, Cepko CL. Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci 2000; 3:873-880.
23. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci USA 2008; 105:19508-19513.
24. Das AV, Mallya KB, Zhao X, et al. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 2006; 299:283-302.
25. Chacko DM, Rogers JA, Turner JE, Ahmad I. Survival and differentiation of cultured retinal progenitors transplanted in the subretinal space of the rat. Biochem Biophys Res Commun 2000; 268:842-846.
26. Yang P, Seiler MJ, Aramant RB, Whittemore SR. In vitro isolation and expansion of human retinal progenitor cells. Exp Neurol 2002; 177:326-331.
27. Klassen H, Kiilgaard JF, Warfvinge K, et al. Photoreceptor differentiation following transplantation of allogeneic retinal progenitor cells to the dystrophic rhodopsin pro347leu transgenic pig. Stem Cells Int 2012; 2012:939801.
28. 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; 45:4167-4173.
29. Taranova OV, Magness ST, Fagan BM, et al. SOX2 is a dosedependent regulator of retinal neural progenitor competence. Genes Dev 2006; 20:1187-1202.
30. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cells 2001; 105:43-55.
31. Nunes MC, Roy NS, Keyoung HM, et al. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 2003; 9:439-447.
32. Chow RL, Lang RA. Early eye development in vertebrates. Annu Rev Cell Dev Biol 2001; 17:255-296.
33. Merkle FT, Tramontin AD, García- Verdugo JM, Alvarez- Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004; 101:17528-17532.
34. Stanke J, Moose HE, El-Hodiri HM, Fischer AJ. Comparative study of Pax2 expression in glial cells in the retina and optic nerve of birds and mammals. J Comp Neurol 2010; 518:2316- 2333.
35. Bao Z-Z, Cepko CL. The expression and function of notch pathway genes in the developing rat eye. J Neurosci 1997; 17:1425-1434.
36. Hyatt GA, Schmitt EA, Fadool JM, Dowling JE. Retinoic acid alters photoreceptor development in vivo. Proc Natl Acad Sci USA 1996; 93:13298-13303.
37. Levine EM, Fuhrmann S, Reh TA. Soluble factors and the development of rod photoreceptors. Cell Mol Life Sci 2000; 57:224-234.
38. 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; 4:73-79.
39. Akhmedov NB, Piriev NI, Chang B, et al. A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc Natl Acad Sci USA 2000; 97:5551-5556.
40. Haider NB, Naggert J, Nishina PM. Excess cone cell proliferation due to lack of a functional NR2E3 causes retinal dysplasia and degeneration in rd7/rd7 mice. Hum Mol Genet 2001; 10:1619-1626.
41. Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the [beta] subunit of rod cGMP-phosphodiesterase. Nature 1990; 347:677-680.
42. Farber DB, Park S, Yamashita C. Cyclic GMP-phosphodiesterase of rd retina: biosynthesis and content. Exp Eye Res 1988; 46:363-374.
43. Ajioka I, Martins RA, Bayazitov IT, et al. Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 2007; 131:378-390.
44. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 1997; 187:36-42.
45. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449:1003-1007.
46. Roesch K, Jadhav AP, Trimarchi JM, et al. The transcriptome of retinal Müller glial cells. J Comp Neurol 2008; 509:225- 238.
47. Xie T, Li L. Stem cells and their niche: an inseparable relationship. Development 2007; 134:2001-2006.
48. Altshuler D, Lo Turco JJ, Rush J, Cepko C. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 1993; 119:1317-1328.
49. Jadhav AP, Cho SH, Cepko CL. Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc Natl Acad Sci USA 2006; 103:18998-19003.
50. Jadhav AP, Mason HA, Cepko CL. Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 2006; 133:913-923.
51. Akhmedov NB, Piriev NI, Chang B, et al. A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc Natl Acad Sci USA 2000; 97:5551-5556.
52. Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 1990; 347:677-680.
53. Li T, Zheng J, Xie Y, et al. Transplantable neural progenitor populations derived from rhesus monkey embryonic stem cells. Stem Cells 2005; 23:1295-1303.