Neural crest cells organize the eye via TGF-β and canonical Wnt signalling

Nature Communications

Volumn 2, Issue 1, 2011, Pages

  Grocott, Timothy ^a   Johnson, Samuel ^a   Bailey, Andrew P ^a,b   Streit, Andrea ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR PAX6; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN; WNT2 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICK; CONTROLLED STUDY; DOWN REGULATION; ECTODERM; EMBRYO; LENS; NEURAL CREST CELL; NONHUMAN; PROTEIN FUNCTION; RETINA; SENSORY NERVE; TRANSCRIPTION INITIATION; ANIMAL; BIOLOGICAL MODEL; CHICK EMBRYO; CHICKEN; CYTOLOGY; EYE; GENETICS; METABOLISM; NEURAL CREST; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

VERTEBRATA;

ANIMALS; CHICK EMBRYO; CHICKENS; EYE; LENS, CRYSTALLINE; MODELS, BIOLOGICAL; NEURAL CREST; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TGF-BETA SUPERFAMILY PROTEINS; TRANSFORMING GROWTH FACTOR BETA; WNT2 PROTEIN;

EID: 79953790741     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1269     Document Type: Article

References (47)

1. Chow, R. L. & Lang, R. A. Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17, 255-296 (2001).
2. Spemann, H. Über Korrelationen in der Entwicklung des Auges. Verh. der Anat. Ges. 15, 61-79 (1901).
3. Saha, M. S., Spann, C. L. & Grainger, R. M. Embryonic lens induction: more than meets the optic vesicle. Cell Differ. Dev. 28, 153-171 (1989).
4. Bailey, A. P., Bhattacharyya, S., Bronner-Fraser, M. & Streit, A. Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity. Dev. Cell 11, 505-517 (2006).
5. Sullivan, C. H. et al. A re-examination of lens induction in chicken embryos: in vitro studies of early tissue interactions. Int. J. Dev. Biol. 48, 771-782 (2004).
6. von Woellwarth, C. Die rolle des neuralleistenmaterials und der temperatur bei der determination der augenlinse. Embryologia 6, 219-242 (1961).
7. Henry, J. J. & Grainger, R. M. Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis. Dev. Biol. 124, 200-214 (1987).
8. Le Douarin, N. M. & Kalcheim, C. The neural Crest 2nd edn (Cambridge University Press, 1999).
9. O'Rahilly, R. & Muller, F. The development of the neural crest in the human. J. Anat. 211, 335-351 (2007).
10. Grindley, J. C., Davidson, D. R. & Hill, R. E. The role of Pax-6 in eye and nasal development. Development 121, 1433-1442 (1995).
11. Collinson, J. M., Hill, R. E. & West, J. D. Different roles for Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127, 945-956 (2000).
12. Ashery-Padan, R., Marquardt, T., Zhou, X. & Gruss, P. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 14, 2701-2711 (2000).
13. Aota, S. et al. Pax6 autoregulation mediated by direct interaction of Pax6 protein with the head surface ectoderm-specific enhancer of the mouse Pax6 gene. Dev. Biol. 257, 1-13 (2003).
14. Kleinjan, D. A., Seawright, A., Childs, A. J. & van Heyningen, V. Conserved elements in Pax6 intron 7 involved in (auto)regulation and alternative transcription. Dev. Biol. 265, 462-477 (2004).
15. Grocott, T. et al. The MH1 domain of Smad3 interacts with Pax6 and represses autoregulation of the Pax6 P1 promoter. Nucleic Acids Res. 35, 890-901 (2007).
16. García-Campmany, L. & Martí, E. The TGFβ intracellular effector Smad3 regulates neuronal differentiation and cell fate specification in the developing spinal cord. Development 134, 65-75 (2007).
17. Watabe, T. & Miyazono, K. Roles of TGF-β family signaling in stem cell renewal and differentiation. Cell Res. 19, 103-115 (2009).
18. Honda, A., Hirose, M. & Ogura, A. Basic FGF and Activin/Nodal but not LIF signaling sustain undifferentiated status of rabbit embryonic stem cells. Exper. Cell Res. 315, 2033-2042 (2009).
19. Inman, G. J. et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74 (2002).
20. Smith, A. N., Miller, L. A., Song, N., Taketo, M. M. & Lang, R. A. The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev. Biol. 285, 477-489 (2005).
21. Blauwkamp, T. A., Chang, M. V. & Cadigan, K. M. Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 27, 1436-1446 (2008).
22. Hoverter, N. P. & Waterman, M. L. A Wnt-fall for gene regulation: repression. Sci. Signal. 1, pe43 (2008).
23. Zheng, J. B., Zhou, Y. H., Maity, T., Liao, W. S. & Saunders, G. F. Activation of the human PAX6 gene through the exon 1 enhancer by transcription factors SEF and Sp1. Nucleic Acids Res. 29, 4070-4078 (2001).
24. Swindell, E. C. et al. Eye formation in the absence of retina. Dev. Biol. 322, 56-64 (2008).
25. Wu, D. & Pan, W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 35, 161-168 (2010).
26. Xu, C., Kim, N. G. & Gumbiner, B. M. Regulation of protein stability by GSK3 mediated phosphorylation. Cell Cycle 8, 4032-4039 (2009).
27. Guo, X. et al. Axin and GSK3- control Smad3 protein stability and modulate TGF- signaling. Genes Dev. 22, 106-120 (2008).
28. Machon, O. et al. Lens morphogenesis is dependent on Pax6-mediated inhibition of the canonical Wnt/beta-catenin signaling in the lens surface ectoderm. Genesis 48, 86-95 (2010).
29. Fuhrmann, S., Levine, E. M. & Reh, T. A. Extraocular mesenchyme patterns the optic vesicle during early eye development in the embryonic chick. Development 127, 4599-4609 (2000).
30. Furuta, Y. & Hogan, B. L. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12, 3764-3775 (1998).
31. Rajagopal, R. et al. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev. Biol. 335, 305-316 (2009).
32. Mathers, P. H., Grinberg, A., Mahon, K. A. & Jamrich, M. The Rx homeobox gene is essential for vertebrate eye development. Nature 387, 603-607 (1997).
33. Porter, F. D. et al. Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124, 2935-2944 (1997).
34. Begbie, J. & Graham, A. Integration between the epibranchial placodes and the hindbrain. Science 294, 595-598 (2001).
35. Coppola, E. et al. Epibranchial ganglia orchestrate the development of the cranial neurogenic crest. Proc. Natl Acad. Sci. USA 107, 2066-2071 (2010).
36. Northcutt, R. G. A reassessment of Goodrich's model of cranial nerve phylogeny. Acta. Anat. 148, 71-80 (1993).
37. Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92 (1951).
38. Bhattacharyya, S., Bailey, A. P., Bronner-Fraser, M. & Streit, A. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 271, 403-414 (2004).
39. Litsiou, A., Hanson, S. & Streit, A. A balance of FGF, Wnt and BMP signalling positions the future placode territory in the head. Development 132, 4051-4062 (2005).
40. de Almeida, I. et al. Unexpected activities of Smad7 in Xenopus mesodermal and neural induction. Mech. Dev. 125, 421-431 (2008).
41. Garcia-Martinez, V. et al. State of commitment of prospective neural plate and prospective mesoderm in late gastrula/early neurula stages of avian embryos. Dev. Biol. 181, 102-115 (1997).
42. Streit, A. et al. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125, 507-519 (1998).
43. Mishima, N. & Tomarev, S. Chicken eyes absent 2 gene: isolation and expression pattern during development. Int. J. Dev. Biol. 42, 1109-1115 (1998).
44. Li, H. S., Yang, J. M., Jacobson, R. D., Pasko, D. & Sundin, O. Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: implications for stepwise determination of the lens. Dev. Biol. 162, 181-194 (1994).
45. Ogino, H. & Yasuda, K. Induction of lens differentiation by activation of a bZIP transcription factor, L-Maf. Science 280, 115-118 (1998).
46. Stern, C. D. et al. Activin and its receptors during gastrulation and the later phases of mesoderm development in the chick embryo. Dev. Biol. 172, 192-205 (1995).
47. Levin, M., Johnson, R. L., Stern, C. D., Kuehn, M. & Tabin, C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82, 803-814 (1995).