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Science 300 (5616): 145-149

Copyright © 2003 by the American Association for the Advancement of Science

Forces for Morphogenesis Investigated with Laser Microsurgery and Quantitative Modeling

M. Shane Hutson,1 Yoichiro Tokutake,1 Ming-Shien Chang,1* James W. Bloor,2dagger Stephanos Venakides,3 Daniel P. Kiehart,2ddagger § Glenn S. Edwards1ddagger §

We investigated the forces that connect the genetic program of development to morphogenesis in Drosophila. We focused on dorsal closure, a powerful model system for development and wound healing. We found that the bulk of progress toward closure is driven by contractility in supracellular "purse strings" and in the amnioserosa, whereas adhesion-mediated zipping coordinates the forces produced by the purse strings and is essential only for the end stages. We applied quantitative modeling to show that these forces, generated in distinct cells, are coordinated in space and synchronized in time. Modeling of wild-type and mutant phenotypes is predictive; although closure in myospheroid mutants ultimately fails when the cell sheets rip themselves apart, our analysis indicates that beta PS integrin has an earlier, important role in zipping.

1 Department of Physics and Free Electron Laser Laboratory,
2 Department of Biology,
3 Department of Mathematics, Duke University, Durham, NC 27708, USA.
*   Present address: School of Physics, Georgia Institute of Technology, Atlanta, GA 30332, USA.

dagger    Present address: Research School of Biosciences, University of Kent, Canterbury, Kent CT2 7NJ, UK.

ddagger    These authors contributed equally to this work.

§   To whom correspondence should be addressed. E-mail: dkiehart{at}duke.edu (D.P.K.); edwards{at}fel.duke.edu (G.S.E.)



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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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