Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination

Development

Volumn 137, Issue 3, 2010, Pages 405-415

  Plageman Jr , Timothy F ^a   Chung, Mei I ^b   Lou, Ming ^c   Smith, April N ^a   Hildebrand, Jeffrey D ^d   Wallingford, John B ^b,e   Lang, Richard A ^a,f  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c LAMAR UNIVERSITY   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Chicken; Lens; Mena (Enah); Morphogenesis; Mouse; Pax6; Shroom3; Vasp; Xenopus

Indexed keywords

CYTOSKELETON PROTEIN; F ACTIN; MYOSIN II; PROTEIN SHROOM3; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; CELL SHAPE; CHICKEN; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; EYE DEVELOPMENT; FETUS; GENE INDUCTION; GENETIC TRANSCRIPTION; LENS EPITHELIUM; LENS MORPHOGENESIS; LENS PLACODE INVAGINATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; XENOPUS;

ACTINS; ANIMALS; CELL ADHESION MOLECULES; CELL LINE; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; EYE PROTEINS; HOMEODOMAIN PROTEINS; LENS, CRYSTALLINE; MICE; MICE, MUTANT STRAINS; MICROFILAMENT PROTEINS; MORPHOGENESIS; MYOSIN TYPE II; PAIRED BOX TRANSCRIPTION FACTORS; PHOSPHOPROTEINS; REPRESSOR PROTEINS;

VERTEBRATA;

EID: 74349118452     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.045369     Document Type: Article

References (42)

1. Altmann, C. R., Chow, R. L., Lang, R. A. and Hemmati-Brivanlou, A. (1997). Lens induction by Pax-6 in Xenopus laevis. Dev. Biol. 185, 119-123.
2. Ashery-Padan, R., Marquardt, T., Zhou, X. and Gruss, P. (2000). 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.
3. Ball, L. J., Kuhne, R., Hoffmann, B., Hafner, A., Schmieder, P., Volkmer-Engert, R., Hof, M., Wahl, M., Schneider-Mergener, J., Walter, U. et al. (2000). Dual epitope recognition by the VASP EVH1 domain modulates polyproline ligand specificity and binding affinity. EMBO J. 19, 4903-4914.
4. Ball, L. J., Jarchau, T., Oschkinat, H. and Walter, U. (2002). EVH1 domains: structure, function and interactions. FEBS Lett. 513, 45-52.
5. Barrett, K., Leptin, M. and Settleman, J. (1997). The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91, 905-915.
6. Baum, B. and Perrimon, N. (2001). Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat. Cell Biol. 3, 883-890.
7. Chauhan, B. K., Disanza, A., Choi, S.-Y., Lou, M., Beggs, H. E., Scita, G., Zheng, Y. and Lang, R. A. (2009). Cdc42 and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development 136, 3657-3667.
8. Chow, R. L., Altmann, C. R., Lang, R. A. and Hemmati-Brivanlou, A. (1999). Pax6 induces ectopic eyes in a vertebrate. Development 126, 4213-4222.
9. Collinson, J. M., Hill, R. E. and West, J. D. (2000). Different roles for Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127, 945-956.
10. Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H. and Wieschaus, E. F. (2005). Folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178.
11. Dietz, M. L., Bernaciak, T. M., Vendetti, F., Kielec, J. M. and Hildebrand, J. D. (2006). Differential actin-dependent localization modulates the evolutionarily conserved activity of Shroom family proteins. J. Biol. Chem. 281, 20542-20554.
12. Eigenthaler, M., Engelhardt, S., Schinke, B., Kobsar, A., Schmitteckert, E., Gambaryan, S., Engelhardt, C. M., Krenn, V., Eliava, M., Jarchau, T. et al. (2003). Disruption of cardiac Ena-VASP protein localization in intercalated disks causes dilated cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 285, H2471-H2481.
13. Fujiwara, M., Uchida, T., Osumi-Yamashita, N. and Eto, K. (1994). Uchida rat (rSey): a new mutant rat with craniofacial abnormalities resembling those of the mouse Sey mutant. Differentiation 57, 31-38.
14. Gates, J., Mahaffey, J. P., Rogers, S. L., Emerson, M., Rogers, E. M., Sottile, S. L., Van Vactor, D., Gertler, F. B. and Peifer, M. (2007). Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134, 2027-2039.
15. Gates, J., Nowotarski, S. H., Yin, H., Mahaffey, J. P., Bridges, T., Herrera, C., Homem, C. C., Janody, F., Montell, D. J. and Peifer, M. (2009). Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev. Biol. 333, 90-107.
16. Gotoh, N., Ito, M., Yamamoto, S., Yoshino, I., Song, N., Wang, Y., Lax, I., Schlessinger, J., Shibuya, M. and Lang, R. A. (2004). Tyrosine phosphorylation sites on FRS2alpha responsible for Shp2 recruitment are critical for induction of lens and retina. Proc. Natl. Acad. Sci. USA 101, 17144-17149.
17. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995). The role of and nasal development. Development 121, 1433-1442
18. Hacker, U. and Perrimon, N. (1998). DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 12, 274-284.
19. Haigo, S. L., Hildebrand, J. D., Harland, R. M. and Wallingford, J. B. (2003). Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol. 13, 2125-2137.
20. Hendrix, R. W. and Zwaan, J. (1974). Cell shape regulation and cell cycle in embryonic lens cells. Nature 247, 145-147.
21. Hendrix, R. W. and Zwaan, J. (1975). The matrix of the optic vesicle-presumptive lens interface during induction of the lens in the chicken embryo. J. Embryol. Exp. Morphol. 33, 1023-1049.
22. Hildebrand, J. D. (2005). Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 118, 5191-5203.
23. Hildebrand, J. D. and Soriano, P. (1999). Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 99, 485-497.
24. Inoue, M., Kamachi, Y., Matsunami, H., Imada, K., Uchikawa, M. and Kondoh, H. (2007). PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 12, 1049-1061.
25. Kinoshita, N., Sasai, N., Misaki, K. and Yonemura, S. (2008). Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol. Biol. Cell 19, 2289-2299.
26. Kolsch, V., Seher, T., Fernandez-Ballester, G. J., Serrano, L. and Leptin, M. (2007). Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315, 384-386.
27. Krause, M., Dent, E. W., Bear, J. E., Loureiro, J. J. and Gertler, F. B. (2003). Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564.
28. Kwiatkowski, A. V., Rubinson, D. A., Dent, E. W., Edward van Veen, J., Leslie, J. D., Zhang, J., Mebane, L. M., Philippar, U., Pinheiro, E. M., Burds, A. A. et al. (2007). Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 56, 441-455.
29. Lang, R. A. (2004). Pathways regulating lens induction in the mouse. Int. J. Dev. Biol. 48, 783-791.
30. Lecuit, T. and Lenne, P. F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644.
31. Lee, C., Scherr, H. M. and Wallingford, J. B. (2007). Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development 134, 1431-1441.
32. Lee, C., Le, M. P. and Wallingford, J. B. (2009). The shroom family proteins play broad roles in the morphogenesis of thickened epithelial sheets. Dev. Dyn. 238, 1480-1491.
33. Lee, J. Y. and Harland, R. M. (2007). Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. Dev. Biol. 311, 40-52.
34. Menzies, A. S., Aszodi, A., Williams, S. E., Pfeifer, A., Wehman, A. M., Goh, K. L., Mason, C. A., Fassler, R. and Gertler, F. B. (2004). Mena and vasodilator-stimulated phosphoprotein are required for multiple actin-dependent processes that shape the vertebrate nervous system. J. Neurosci. 24, 8029-8038.
35. Nikolaidou, K. K. and Barrett, K. (2004). A Rho GTPase signaling pathway is used reiteratively in epithelial folding and potentially selects the outcome of Rho activation. Curr. Biol. 14, 1822-1826.
36. Nishimura, T. and Takeichi, M. (2008). Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502.
37. Roffers-Agarwal, J., Xanthos, J. B., Kragtorp, K. A. and Miller, J. R. (2008). Enabled (Xena) regulates neural plate morphogenesis, apical constriction, and cellular adhesion required for neural tube closure in Xenopus. Dev. Biol. 314, 393-403.
38. Smith, A. N., Miller, L. A., Song, N., Taketo, M. M. and Lang, R. A. (2005). 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.
39. Smith, A. N., Miller, L.-A., Radice, G., Ashery-Padan, R. and Lang, R. A. (2009). Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 136, 2977-2985.
40. Taylor, J., Chung, K. H., Figueroa, C., Zurawski, J., Dickson, H. M., Brace, E. J., Avery, A. W., Turner, D. L. and Vojtek, A. B. (2008). The scaffold protein POSH regulates axon outgrowth. Mol. Biol. Cell 19, 5181-5192.
41. Vasioukhin, V., Bauer, C., Yin, M. and Fuchs, E. (2000). Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219.
42. Wawersik, S., Purcell, P., Rauchman, M., Dudley, A. T., Robertson, E. J. and Maas, R. (1999). BMP7 acts in murine lens placode development. Dev. Biol. 207, 176-188.