SOX2 maintains the quiescent progenitor cell state of postnatal retinal Müller glia

Development (Cambridge)

Volumn 140, Issue 7, 2013, Pages 1445-1456

  Surzenko, Natalia ^a,b,c   Crowl, Tessa ^a,b   Bachleda, Amelia ^a,b   Langer, Lee ^a,b   Pevny, Larysa ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

M ller glia; Quiescence; Retina; SOX2

Indexed keywords

TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIVISION; CELL MUTANT; CELL TYPE; CONTROLLED STUDY; GENETIC ANALYSIS; GLIA CELL; MOUSE; MUELLER CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RETINA DEGENERATION; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGENESIS; NEUROGLIA; RETINA; SOXB1 TRANSCRIPTION FACTORS; STEM CELLS;

EID: 84875062171     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.071878     Document Type: Article

References (64)

1. Austin, C. P., Feldman, D. E., Ida, J. A., Jr and Cepko, C. L. (1995). Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637-3650.
2. Bao, Z. Z. and Cepko, C. L. (1997). The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci. 17, 1425-1434.
3. Bringmann, A., Pannicke, T., Grosche, J., Francke, M., Wiedemann, P., Skatchkov, S. N., Osborne, N. N. and Reichenbach, A. (2006). Müller cells in the healthy and diseased retina. Prog. Retin. Eye Res. 25, 397-424.
4. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6, 1162-1168.
5. Chenn, A. and Walsh, C. A. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
6. Close, J. L., Liu, J., Gumuscu, B. and Reh, T. A. (2006). Epidermal growth factor receptor expression regulates proliferation in the postnatal rat retina. Glia 54, 94-104.
7. Del Debbio, C. B., Balasubramanian, S., Parameswaran, S., Chaudhuri, A., Qiu, F. and Ahmad, I. (2010). Notch and Wnt signaling mediated rod photoreceptor regeneration by Müller cells in adult mammalian retina. PLoS ONE 5, e12425.
8. Donovan, S. L. and Dyer, M. A. (2007). Preparation and square wave electroporation of retinal explant cultures. Nat. Protoc. 1, 2710-2718.
9. Dubois-Dauphin, M., Poitry-Yamate, C., de Bilbao, F., Julliard, A. K., Jourdan, F. and Donati, G. (1999). Early postnatal Müller cell death leads to retinal but not optic nerve degeneration in NSE-Hu-Bcl-2 transgenic mice. Neuroscience 95, 9-21.
10. Dyer, M. A. and Cepko, C. L. (2000). Control of Müller glial cell proliferation and activation following retinal injury. Nat. Neurosci. 3, 873-880.
11. Ehm, O., Göritz, C., Covic, M., Schäffner, I., Schwarz, T. J., Karaca, E., Kempkes, B., Kremmer, E., Pfrieger, F. W., Espinosa, L. et al. (2010). RBPJkappa-dependent signaling is essential for long-term maintenance of neural stem cells in the adult hippocampus. J. Neurosci. 30, 13794-13807.
12. Ellis, P., Fagan, B. M., Magness, S. T., Hutton, S., Taranova, O., Hayashi, S., McMahon, A., Rao, M. and Pevny, L. (2004). SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26, 148-165.
13. Elshatory, Y., Everhart, D., Deng, M., Xie, X., Barlow, R. B. and Gan, L. (2007). Islet-1 controls the differentiation of retinal bipolar and cholinergic amacrine cells. J. Neurosci. 27, 12707-12720.
14. Favaro, R., Valotta, M., Ferri, A. L., Latorre, E., Mariani, J., Giachino, C., Lancini, C., Tosetti, V., Ottolenghi, S., Taylor, V. et al. (2009). Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat. Neurosci. 12, 1248-1256.
15. Ferri, A. L., Cavallaro, M., Braida, D., Di Cristofano, A., Canta, A., Vezzani, A., Ottolenghi, S., Pandolfi, P. P., Sala, M., DeBiasi, S. et al. (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131, 3805-3819.
16. Fischer, A. J. and Reh, T. A. (2001). Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4, 247-252.
17. Furukawa, T., Mukherjee, S., Bao, Z. Z., Morrow, E. M. and Cepko, C. L. (2000). rax, Hes1, and notch1 promote the formation of Müller glia by postnatal retinal progenitor cells. Neuron 26, 383-394.
18. Gomes, F. L., Zhang, G., Carbonell, F., Correa, J. A., Harris, W. A., Simons, B. D. and Cayouette, M. (2011). Reconstruction of rat retinal progenitor cell lineages in vitro reveals a surprising degree of stochasticity in cell fate decisions. Development 138, 227-235.
19. Graham, V., Khudyakov, J., Ellis, P. and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765.
20. Hatakeyama, J. and Kageyama, R. (2002). Retrovirus-mediated gene transfer to retinal explants. Methods 28, 387-395.
21. Hayashi, S. and McMahon, A. P. (2002). Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244, 305-318.
22. Henrique, D., Hirsinger, E., Adam, J., Le Roux, I., Pourquié, O., Ish-Horowicz, D. and Lewis, J. (1997). Maintenance of neuroepithelial progenitor cells by Delta-Notch signalling in the embryonic chick retina. Curr. Biol. 7, 661-670.
23. Hitchcock, P., Ochocinska, M., Sieh, A. and Otteson, D. (2004). Persistent and injury-induced neurogenesis in the vertebrate retina. Prog. Retin. Eye Res. 23, 183-194.
24. Hojo, M., Ohtsuka, T., Hashimoto, N., Gradwohl, G., Guillemot, F. and Kageyama, R. (2000). Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127, 2515-2522.
25. Holmberg, J., Hansson, E., Malewicz, M., Sandberg, M., Perlmann, T., Lendahl, U. and Muhr, J. (2008). SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation. Development 135, 1843-1851.
26. Horsford, D. J., Nguyen, M. T., Sellar, G. C., Kothary, R., Arnheiter, H. and McInnes, R. R. (2005). Chx10 repression of Mitf is required for the maintenance of mammalian neuroretinal identity. Development 132, 177-187.
27. Jadhav, A. P., Cho, S. H. and Cepko, C. L. (2006a). 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.
28. Jadhav, A. P., Mason, H. A. and Cepko, C. L. (2006b). Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133, 913-923.
29. Jadhav, A. P., Roesch, K. and Cepko, C. L. (2009). Development and neurogenic potential of Müller glial cells in the vertebrate retina. Prog. Retin. Eye Res. 28, 249-262.
30. Joly, S., Pernet, V., Samardzija, M. and Grimm, C. (2011). Pax6-positive Müller glia cells express cell cycle markers but do not proliferate after photoreceptor injury in the mouse retina. Glia 59, 1033-1046.
31. Karl, M. O., Hayes, S., Nelson, B. R., Tan, K., Buckingham, B. and Reh, T. A. (2008). Stimulation of neural regeneration in the mouse retina. Proc. Natl. Acad. Sci. USA 105, 19508-19513.
32. Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T. and Matsuzaki, F. (2008). Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101.
33. Kriegstein, A. and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184.
34. Lardelli, M. and Lendahl, U. (1993). Motch A and motch B - two mouse Notch homologues coexpressed in a wide variety of tissues. Exp. Cell Res. 204, 364-372.
35. Livesey, F. J. and Cepko, C. L. (2001). Vertebrate neural cell-fate determination:lessons from the retina. Nat. Rev. Neurosci. 2, 109-118.
36. Marquardt, T. (2003). Transcriptional control of neuronal diversification in the retina. Prog. Retin. Eye Res. 22, 567-577.
37. Marquardt, T. and Gruss, P. (2002). Generating neuronal diversity in the retina:one for nearly all. Trends Neurosci. 25, 32-38.
38. Matsuda, T. and Cepko, C. L. (2004). Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA 101, 16-22.
39. Matsuda, T. and Cepko, C. L. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA 104, 1027-1032.
40. Matsushima, D., Heavner, W. and Pevny, L. H. (2011). Combinatorial regulation of optic cup progenitor cell fate by SOX2 and PAX6. Development 138, 443-454.
41. Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. and Gaiano, N. (2007). Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351-355.
42. Nelson, B. R., Ueki, Y., Reardon, S., Karl, M. O., Georgi, S., Hartman, B. H., Lamba, D. A. and Reh, T. A. (2011). Genome-wide analysis of Müller glial differentiation reveals a requirement for Notch signaling in postmitotic cells to maintain the glial fate. PLoS ONE 6, e22817.
43. Ohsawa, R. and Kageyama, R. (2008). Regulation of retinal cell fate specification by multiple transcription factors. Brain Res. 1192, 90-98.
44. Ooto, S., Akagi, T., Kageyama, R., Akita, J., Mandai, M., Honda, Y. and Takahashi, M. (2004). Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc. Natl. Acad. Sci. USA 101, 13654-13659.
45. Pevny, L. H. and Lovell-Badge, R. (1997). Sox genes find their feet. Curr. Opin. Genet. Dev. 7, 338-344.
46. Pevny, L. H. and Nicolis, S. K. (2010). Sox2 roles in neural stem cells. Int. J. Biochem. Cell Biol. 42, 421-424.
47. Rich, K. A., Figueroa, S. L., Zhan, Y. and Blanks, J. C. (1995). Effects of Müller cell disruption on mouse photoreceptor cell development. Exp. Eye Res. 61, 235-248.
48. Roesch, K., Jadhav, A. P., Trimarchi, J. M., Stadler, M. B., Roska, B., Sun, B. B. and Cepko, C. L. (2008). The transcriptome of retinal Müller glial cells. J. Comp. Neurol. 509, 225-238.
49. Sang, L. and Coller, H. A. (2009). Fear of commitment: Hes1 protects quiescent fibroblasts from irreversible cellular fates. Cell Cycle 8, 2161-2167.
50. Sang, L., Coller, H. A. and Roberts, J. M. (2008). Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science 321, 1095-1100.
51. Shimojo, H., Ohtsuka, T. and Kageyama, R. (2011). Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front. Neurosci. 5, 78.
52. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
53. Takatsuka, K., Hatakeyama, J., Bessho, Y. and Kageyama, R. (2004). Roles of the bHLH gene Hes1 in retinal morphogenesis. Brain Res. 1004, 148-155.
54. Taranova, O. V., Magness, S. T., Fagan, B. M., Wu, Y., Surzenko, N., Hutton, S. R. and Pevny, L. H. (2006). SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20, 1187-1202.
55. Tomita, K., Ishibashi, M., Nakahara, K., Ang, S. L., Nakanishi, S., Guillemot, F. and Kageyama, R. (1996). Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16, 723-734.
56. Turner, D. L. and Cepko, C. L. (1987). A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131-136.
57. Ueki, Y., Karl, M. O., Sudar, S., Pollak, J., Taylor, R. J., Loeffler, K., Wilken, M. S., Reardon, S. and Reh, T. A. (2012). P53 is required for the developmental restriction in Müller glial proliferation in mouse retina. Glia 60, 1579-1589.
58. van Rossum, A. G., Aartsen, W. M., Meuleman, J., Klooster, J., Malysheva, A., Versteeg, I., Arsanto, J. P., Le Bivic, A. and Wijnholds, J. (2006). Pals1/Mpp5 is required for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum. Mol. Genet. 15, 2659-2672.
59. Wegner, M. and Stolt, C. C. (2005). From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 28, 583-588.
60. Willbold, E., Berger, J., Reinicke, M. and Wolburg, H. (1997). On the role of Müller glia cells in histogenesis: only retinal spheroids, but not tectal, telencephalic and cerebellar spheroids develop histotypical patterns. J. Hirnforsch. 38, 383-396.
61. Yang, X., Klein, R., Tian, X., Cheng, H. T., Kopan, R. and Shen, J. (2004). Notch activation induces apoptosis in neural progenitor cells through a p53- dependent pathway. Dev. Biol. 269, 81-94.
62. Yaron, O., Farhy, C., Marquardt, T., Applebury, M. and Ashery-Padan, R. (2006). Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133, 1367-1378.
63. Young, R. W. (1985a). Cell differentiation in the retina of the mouse. Anat. Rec.212, 199-205.
64. Young, R. W. (1985b). Cell proliferation during postnatal development of the retina in the mouse. Brain Res. 353, 229-239.