Pleiotropic Effects of Sox2 During the Development of the Zebrafish Epithalamus

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Feb 6

PMID 24498133

Citations 4

Authors

Sofia Pavlou

Katy Astell

Ioannis Kasioulis

Milica Gakovic

Richard Baldock

Veronica Van Heyningen

Pedro Coutinho

Affiliations

Soon will be listed here.

Abstract

The zebrafish epithalamus is part of the diencephalon and encompasses three major components: the pineal, the parapineal and the habenular nuclei. Using sox2 knockdown, we show here that this key transcriptional regulator has pleiotropic effects during the development of these structures. Sox2 negatively regulates pineal neurogenesis. Also, Sox2 is identified as the unknown factor responsible for pineal photoreceptor prepatterning and performs this function independently of the BMP signaling. The correct levels of sox2 are critical for the functionally important asymmetrical positioning of the parapineal organ and for the migration of parapineal cells as a coherent structure. Deviations from this strict control result in defects associated with abnormal habenular laterality, which we have documented and quantified in sox2 morphants.

Citing Articles

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References

Scheer N, Groth A, Hans S, Campos-Ortega J . An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development. 2001; 128(7):1099-107. DOI: 10.1242/dev.128.7.1099. View

Millimaki B, Sweet E, Riley B . Sox2 is required for maintenance and regeneration, but not initial development, of hair cells in the zebrafish inner ear. Dev Biol. 2009; 338(2):262-9. PMC: 2815045. DOI: 10.1016/j.ydbio.2009.12.011. View

Dufourcq P, Rastegar S, Strahle U, Blader P . Parapineal specific expression of gfi1 in the zebrafish epithalamus. Gene Expr Patterns. 2003; 4(1):53-7. DOI: 10.1016/s1567-133x(03)00148-0. View

Parrinello S, Napoli I, Ribeiro S, Wingfield Digby P, Fedorova M, Parkinson D . EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell. 2010; 143(1):145-55. PMC: 3826531. DOI: 10.1016/j.cell.2010.08.039. View

Graham V, Khudyakov J, Ellis P, Pevny L . SOX2 functions to maintain neural progenitor identity. Neuron. 2003; 39(5):749-65. DOI: 10.1016/s0896-6273(03)00497-5. View

Perez-Perez J, Candela H, Micol J . Understanding synergy in genetic interactions. Trends Genet. 2009; 25(8):368-76. DOI: 10.1016/j.tig.2009.06.004. View

Snelson C, Gamse J . Building an asymmetric brain: development of the zebrafish epithalamus. Semin Cell Dev Biol. 2008; 20(4):491-7. PMC: 2729063. DOI: 10.1016/j.semcdb.2008.11.008. View

Concha M, Burdine R, Russell C, Schier A, Wilson S . A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron. 2001; 28(2):399-409. DOI: 10.1016/s0896-6273(00)00120-3. View

Lu P, Lund C, Khuansuwan S, Schumann A, Harney-Tolo M, Gamse J . Failure in closure of the anterior neural tube causes left isomerization of the zebrafish epithalamus. Dev Biol. 2012; 374(2):333-44. PMC: 6067013. DOI: 10.1016/j.ydbio.2012.11.025. View

10.

Roussigne M, Bianco I, Wilson S, Blader P . Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development. 2009; 136(9):1549-57. PMC: 2675782. DOI: 10.1242/dev.034793. View

11.

Frambach I, Rossler W, Winkler M, Schurmann F . F-actin at identified synapses in the mushroom body neuropil of the insect brain. J Comp Neurol. 2004; 475(3):303-14. DOI: 10.1002/cne.20165. View

12.

Matsumata M, Uchikawa M, Kamachi Y, Kondoh H . Multiple N-cadherin enhancers identified by systematic functional screening indicate its Group B1 SOX-dependent regulation in neural and placodal development. Dev Biol. 2005; 286(2):601-17. DOI: 10.1016/j.ydbio.2005.08.005. View

13.

Hagstrom S, Pauer G, Reid J, Simpson E, Crowe S, Maumenee I . SOX2 mutation causes anophthalmia, hearing loss, and brain anomalies. Am J Med Genet A. 2005; 138A(2):95-8. DOI: 10.1002/ajmg.a.30803. View

14.

Cau E, Quillien A, Blader P . Notch resolves mixed neural identities in the zebrafish epiphysis. Development. 2008; 135(14):2391-401. DOI: 10.1242/dev.013482. View

15.

Xiao T, Roeser T, Staub W, Baier H . A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development. 2005; 132(13):2955-67. DOI: 10.1242/dev.01861. View

16.

Concha M, Russell C, Regan J, Tawk M, Sidi S, Gilmour D . Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron. 2003; 39(3):423-38. DOI: 10.1016/s0896-6273(03)00437-9. View

17.

Taranova O, Magness S, Fagan B, Wu Y, Surzenko N, Hutton S . SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 2006; 20(9):1187-202. PMC: 1472477. DOI: 10.1101/gad.1407906. View

18.

Rossler W, Kuduz J, Schurmann F, Schild D . Aggregation of f-actin in olfactory glomeruli: a common feature of glomeruli across phyla. Chem Senses. 2002; 27(9):803-10. DOI: 10.1093/chemse/27.9.803. View

19.

Okuda Y, Ogura E, Kondoh H, Kamachi Y . B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLoS Genet. 2010; 6(5):e1000936. PMC: 2865518. DOI: 10.1371/journal.pgen.1000936. View

20.

Barth K, Kishimoto Y, Rohr K, Seydler C, Schulte-Merker S, Wilson S . Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development. 1999; 126(22):4977-87. DOI: 10.1242/dev.126.22.4977. View