The group E Sox genes Sox8 and Sox9 are regulated by Notch signaling and are required for Müller glial cell development in mouse retina

Experimental Eye Research

Volumn 89, Issue 4, 2009, Pages 549-558

  Muto, Akihiko ^a   Iida, Atsumi ^a   Satoh, Shinya ^a   Watanabe, Sumiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

development; mouse; M ller glial cell; notch; retina; Sox8; Sox9; specification

Indexed keywords

GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR HES 5; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; MUELLER CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA; RETINA DEVELOPMENT; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION; VERTEBRATE;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; DIPEPTIDES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; MICE; MICE, INBRED ICR; NEUROGLIA; PLASMIDS; RECEPTORS, NOTCH; RETINA; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; SOXE TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 69749106313     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2009.05.006     Document Type: Article

References (57)

1. Akazawa C., Sasai Y., Nakanishi S., and Kageyama R. Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J. Biol. Chem. 267 (1992) 21879-21885
2. Bagheri-Fam S., Barrionuevo F., Dohrmann U., Gunther T., Schule R., Kemler R., Mallo M., Kanzler B., and Scherer G. Long-range upstream and downstream enhancers control distinct subsets of the complex spatiotemporal Sox9 expression pattern. Dev. Biol. 291 (2006) 382-397
3. Bernardos R.L., Lentz S.I., Wolfe M.S., and Raymond P.A. Notch-Delta signaling is required for spatial patterning and Müller glia differentiation in the zebrafish retina. Dev. Biol. 278 (2005) 381-395
4. Bi W., Deng J.M., Zhang Z., Behringer R.R., and de Crombrugghe B. Sox9 is required for cartilage formation. Nat. Genet. 22 (1999) 85-89
5. Britsch S., Goerich D.E., Riethmacher D., Peirano R.I., Rossner M., Nave K.A., Birchmeier C., and Wegner M. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 15 (2001) 66-78
6. Das A.V., Mallya K.B., Zhao X., Ahmad F., Bhattacharya S., Thoreson W.B., Hegde G.V., and Ahmad I. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev. Biol. 299 (2006) 283-302
7. Deneen B., Ho R., Lukaszewicz A., Hochstim C.J., Gronostajski R.M., and Anderson D.J. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52 (2006) 953-968
8. Dyer M.A., and Cepko C.L. Control of Müller glial cell proliferation and activation following retinal injury. Nat. Neurosci. 3 (2000) 873-880
9. Finzsch M., Stolt C.C., Lommes P., and Wegner M. Sox9 and Sox10 influence survival and migration of oligodendrocyte precursors in the spinal cord by regulating PDGF receptor alpha expression. Development 135 (2008) 637-646
10. Foster J.W., Dominguez-Steglich M.A., Guioli S., Kowk G., Weller P.A., Stevanovic M., Weissenbach J., Mansour S., Young I.D., Goodfellow P.N., Brook J.D., and Schafer A.J. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372 (1994) 525-530
11. Franze K., Grosche J., Skatchkov S.N., Schinkinger S., Foja C., Schild D., Uckermann O., Travis K., Reichenbach A., and Guck J. Müller cells are living optical fibers in the vertebrate retina. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 8287-8292
12. Furukawa T., Mukherjee S., Bao Z.Z., Morrow E.M., and Cepko C.L. Rax, Hes1, and notch1 promote the formation of Müller glia by postnatal retinal progenitor cells. Neuron 26 (2000) 383-394
13. Garcia M., and Vecino E. Role of Müller glia in neuroprotection and regeneration in the retina. Histol. Histopathol. 18 (2003) 1205-1218
14. Goureau O., Rhee K.D., and Yang X.J. Ciliary neurotrophic factor promotes Müller glia differentiation from the postnatal retinal progenitor pool. Dev. Neurosci. 26 (2004) 359-370
15. Hardingham T.E., Oldershaw R.A., and Tew S.R. Cartilage, SOX9 and Notch signals in chondrogenesis. J. Anat. 209 (2006) 469-480
16. Hatakeyama J., and Kageyama R. Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15 (2004) 83-89
17. Hojo M., Ohtsuka T., Hashimoto N., Gradwohl G., Guillemot F., and Kageyama R. Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127 (2000) 2515-2522
18. Inoue T., Hojo M., Bessho Y., Tano Y., Lee J.E., and Kageyama R. Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129 (2002) 831-842
19. Jadhav A.P., Cho S.H., and Cepko C.L. Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 18998-19003
20. Jadhav A.P., Mason H.A., and Cepko C.L. Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133 (2006) 913-923
21. James J., Das A.V., Rahnenfuhrer J., and Ahmad I. Cellular and molecular characterization of early and late retinal stem cells/progenitors: differential regulation of proliferation and context dependent role of Notch signaling. J. Neurobiol. 61 (2004) 359-376
22. Kamachi Y., Uchikawa M., and Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16 (2000) 182-187
23. Kellerer S., Schreiner S., Stolt C.C., Scholz S., Bosl M.R., and Wegner M. Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 133 (2006) 2875-2886
24. Kiefer J.C. Back to basics: Sox genes. Dev. Dyn. 236 (2007) 2356-2366
25. Kobayashi N., Kimura S., Ito T., Yahagi N., Ichinose M., Omata M., and Iba H. The Brm gene suppressed at the post-transcriptional level in various human cell lines is inducible by transient HDAC inhibitor treatment, which exhibits antioncogenic potential. Oncogene 24 (2005) 5471-5481
26. Kuhlbrodt K., Herbarth B., Sock E., Enderich J., Hermans-Borgmeyer I., and Wegner M. Cooperative function of POU proteins and SOX proteins in glial cells. J. Biol. Chem. 273 (1998) 16050-16057
27. Kuhlbrodt K., Herbarth B., Sock E., Hermans-Borgmeyer I., and Wegner M. Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18 (1998) 237-250
28. Le T.T., Wroblewski E., Patel S., Riesenberg A.N., and Brown N.L. Math5 is required for both early retinal neuron differentiation and cell cycle progression. Dev. Biol. 295 (2006) 764-778
29. Lillien L. Changes in retinal cell fate induced by overexpression of EGF receptor. Nature 377 (1995) 158-162
30. Lillien L., and Wancio D. Changes in epidermal growth factor receptor expression and competence to generate glia regulate timing and choice of differentiation in the retina. Mol. Cell. Neurosci. 10 (1998) 296-308
31. Liu A., Li J., Marin-Husstege M., Kageyama R., Fan Y., Gelinas C., and Casaccia-Bonnefil P. A molecular insight of Hes5-dependent inhibition of myelin gene expression: old partners and new players. EMBO J. 25 (2006) 4833-4842
32. Livesey F.J., and Cepko C.L. Vertebrate neural cell-fate determination: lessons from the retina. Nat. Rev. Neurosci. 2 (2001) 109-118
33. Malki S., Bertab P., Poulata F., and Boizet-Bonhoure B. Cytoplasmic retention of the sex-determining factor SOX9 via the microtubule network. Exp. Cell Res. 309 (2005) 468-475
34. Morita S., Kojima T., and Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7 (2000) 1063-1066
35. Morrow E.M., Furukawa T., Lee J.E., and Cepko C.L. NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126 (1999) 23-36
36. Muto A., Aoki Y., and Watanabe S. Mouse Rab11-FIP4 regulates proliferation and differentiation of retinal progenitors in a Rab11-independent manner. Dev. Dyn. 236 (2007) 214-225
37. Ohtsuka T., Ishibashi M., Gradwohl G., Nakanishi S., Guillemot F., and Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18 (1999) 2196-2207
38. Ong C.-T., Cheng H.-T., Chang L.-W., Ohtsuka T., Kageyama R., Stormo G.D., and Kopan R. Target selectivity of vertebrate notch proteins. Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J. Biol. Chem. 281 (2006) 5106-5119
39. Ooto S., Akagi T., Kageyama R., Akita J., Mandai M., Honda Y., and Takahashi M. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13654-13659
40. Pevny L., and Placzek M. SOX genes and neural progenitor identity. Curr. Opin. Neurobiol. 15 (2005) 7-13
41. Rich K.A., Figueroa S.L., Zhan Y., and Blanks J.C. Effects of Müller cell disruption on mouse photoreceptor cell development. Exp. Eye Res. 61 (1995) 235-248
42. Schepers G.E., Bullejos M., Hosking B.M., and Koopman P. Cloning and characterisation of the Sry-related transcription factor gene Sox8. Nucleic Acids Res. 28 (2000) 1473-1480
43. Seymour P.A., Freude K.K., Tran M.N., Mayes E.E., Jensen J., Kist R., Scherer G., and Sander M. SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 1865-1870
44. Sock E., Schmidt K., Hermanns-Borgmeyer I., Bosl M.R., and Wegner M. Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8. Mol. Cell. Biol. 21 (2001) 6951-6959
45. Stolt C.C., Lommes P., Friedrich R.P., and Wegner M. Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 131 (2004) 2349-2358
46. Stolt C.C., Lommes P., Sock E., Chaboissier M.C., Schedl A., and Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 17 (2003) 1677-1689
47. Stolt C.C., Rehberg S., Ader M., Lommes P., Riethmacher D., Schachner M., Bartsch U., and Wegner M. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 16 (2002) 165-170
48. Stolt C.C., Schmitt S., Lommes P., Sock E., and Wegner M. Impact of transcription factor Sox8 on oligodendrocyte specification in the mouse embryonic spinal cord. Dev. Biol. 281 (2005) 309-317
49. Takatsuka K., Hatakeyama J., Bessho Y., and Kageyama R. Roles of the bHLH gene Hes1 in retinal morphogenesis. Brain Res. 1004 (2004) 148-155
50. Tanaka S., Kamachi Y., Tanouchi A., Hamada H., Jing N., and Kondoh H. Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol. Cell. Biol. 24 (2004) 8834-8846
51. Tomita K., Ishibashi M., Nakahara K., Ang S.L., Nakanishi S., Guillemot F., and Kageyama R. Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16 (1996) 723-734
52. Turner D.L., and Cepko C.L. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328 (1987) 131-136
53. Uchikawa M., Kamachi Y., and Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech. Dev. 84 (1999) 103-120
54. Vidal V.P., Chaboissier M.C., de Rooij D.G., and Schedl A. Sox9 induces testis development in XX transgenic mice. Nat. Genet. 28 (2001) 216-217
55. Wilson M., and Koopman P. Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr. Opin. Genet. Dev. 12 (2002) 441-446
56. Xue L.P., Lu J., Cao Q., Kaur C., and Ling E.A. Nestin expression in Müller glial cells in postnatal rat retina and its upregulation following optic nerve transection. Neuroscience 143 (2006) 117-127
57. Yaron O., Farhy C., Marquardt T., Applebury M., and Ashery-Padan R. Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133 (2006) 1367-1378