Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination.
Journal: 2010/March - Development (Cambridge)
ISSN: 1477-9129
Abstract:
Embryonic development requires a complex series of relative cellular movements and shape changes that are generally referred to as morphogenesis. Although some of the mechanisms underlying morphogenesis have been identified, the process is still poorly understood. Here, we address mechanisms of epithelial morphogenesis using the vertebrate lens as a model system. We show that the apical constriction of lens epithelial cells that accompanies invagination of the lens placode is dependent on Shroom3, a molecule previously associated with apical constriction during morphogenesis of the neural plate. We show that Shroom3 is required for the apical localization of F-actin and myosin II, both crucial components of the contractile complexes required for apical constriction, and for the apical localization of Vasp, a Mena family protein with F-actin anti-capping function that is also required for morphogenesis. Finally, we show that the expression of Shroom3 is dependent on the crucial lens-induction transcription factor Pax6. This provides a previously missing link between lens-induction pathways and the morphogenesis machinery and partly explains the absence of lens morphogenesis in Pax6-deficient mutants.
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Development 137(3): 405-415

Pax6-dependent <em>Shroom3</em> expression regulates apical constriction during lens placode invagination

The Visual Systems Group, Children's Hospital Research Foundation, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA
Divisions of Pediatric Ophthalmology, Children's Hospital Research Foundation, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA
Molecular, Cell and Developmental Biology, University of Texas at Austin, Austin, TX 78712, USA
Department of Chemistry and Physics, Lamar University, Beaumont, TX 77710, USA
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA
Howard Hughes Medical Institute, 4000 Jones Bridge Road, Chevy Chase, MD 20815-6789, USA
Developmental Biology, Children's Hospital Research Foundation, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA
Department of Ophthalmology, University of Cincinnati, Cincinnati, OH 45229, USA
Author for correspondence (gro.cmhcc@gnaL.drahciR)
Accepted 2009 Dec 3.

Summary

Embryonic development requires a complex series of relative cellular movements and shape changes that are generally referred to as morphogenesis. Although some of the mechanisms underlying morphogenesis have been identified, the process is still poorly understood. Here, we address mechanisms of epithelial morphogenesis using the vertebrate lens as a model system. We show that the apical constriction of lens epithelial cells that accompanies invagination of the lens placode is dependent on Shroom3, a molecule previously associated with apical constriction during morphogenesis of the neural plate. We show that Shroom3 is required for the apical localization of F-actin and myosin II, both crucial components of the contractile complexes required for apical constriction, and for the apical localization of Vasp, a Mena family protein with F-actin anti-capping function that is also required for morphogenesis. Finally, we show that the expression of Shroom3 is dependent on the crucial lens-induction transcription factor Pax6. This provides a previously missing link between lens-induction pathways and the morphogenesis machinery and partly explains the absence of lens morphogenesis in Pax6-deficient mutants.

Keywords: Mena (Enah), Pax6, Shroom3, Vasp, Lens, Morphogenesis, Mouse, Chicken, Xenopus
Summary

Acknowledgements

We thank Paul Speeg for excellent technical assistance and Dr Frank Gertler for kindly providing the antibody to mouse Vasp. J.B.W. is an early career scientist of the Howard Hughes Medical Institute. We also acknowledge grant support from the NIH to J.B.W. (NIGMS) and R.A.L. (EY15766;, EY16241;, EY17848;, CA131270) and from the Abrahamson Pediatric Eye Institute Endowment at the Children's Hospital Medical Center of Cincinnati to R.A.L. Deposited in PMC for release after 6 months.

Acknowledgements

Footnotes

Competing interests statement

The authors declare no competing financial interests.

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