Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Published Online February 6, 2003
Science DOI: 10.1126/science.1079552

Reports

Submitted on October 18, 2002
Accepted on January 24, 2003

Forces for Morphogenesis Investigated with Laser Microsurgery and Quantitative Modeling

M. Shane Hutson 1, Yoichiro Tokutake 1, Ming-Shien Chang 2, James W. Bloor 3, Stephanos Venakides 4, Daniel P. Kiehart 5*, Glenn S. Edwards 6*

1 Department of Physics and Free Electron Laser Laboratory, Duke University, Durham, NC 27708, USA.
2 Department of Physics and Free Electron Laser Laboratory, Duke University, Durham, NC 27708, USA; Present Address: School of Physics, Georgia Institute of Technology, Atlanta, GA 30332, USA.
3 Department of Biology, Duke University, Durham, NC 27708, USA; Present Address: Research School of Biosciences, University of Kent, Canterbury, Kent, CT2 7NJ, United Kingdom.
4 Department of Mathematics, Duke University, Durham, NC 27708, USA.
5 Department of Biology, Duke University, Durham, NC 27708, USA.
6 Department of Physics and Free Electron Laser Laboratory, Duke University, Durham, NC 27708, USA.

* To whom correspondence should be addressed. E-mail: dkiehart{at}duke.edu, edwards{at}fel.duke.edu.

We investigate forces that connect the genetic program of development to morphogenesis in Drosophila. We focus on dorsal closure, a powerful model system for development and wound healing. We find that the bulk of progress towards closure is driven by contractility in supracellular purse-strings and the amnioserosa, while adhesion-mediated zipping coordinates the forces produced by the purse-strings and is essential only for the end stages. We apply 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, significant role in zipping.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Cell Mechanics and Feedback Regulation of Actomyosin Networks.
R. Fernandez-Gonzalez and J. A. Zallen (2009)
Science Signaling 2, pe78
   Abstract »    Full Text »    PDF »
Towards a unified theory for morphomechanics.
L. A. Taber (2009)
Phil Trans R Soc A 367, 3555-3583
   Abstract »    Full Text »    PDF »
From the Cover: Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues.
W. R. Legant, A. Pathak, M. T. Yang, V. S. Deshpande, R. M. McMeeking, and C. S. Chen (2009)
PNAS 106, 10097-10102
   Abstract »    Full Text »    PDF »
Mechanical control of global cell behaviour during dorsal closure in Drosophila.
N. Gorfinkiel, G. B. Blanchard, R. J. Adams, and A. Martinez Arias (2009)
Development 136, 1889-1898
   Abstract »    Full Text »    PDF »
Apoptotic Force and Tissue Dynamics During Drosophila Embryogenesis.
Y. Toyama, X. G. Peralta, A. R. Wells, D. P. Kiehart, and G. S. Edwards (2008)
Science 321, 1683-1686
   Abstract »    Full Text »    PDF »
Mechanical Control of Tissue Morphogenesis.
P. Patwari and R. T. Lee (2008)
Circ. Res. 103, 234-243
   Abstract »    Full Text »    PDF »
Measurement Techniques for Cellular Biomechanics In Vitro.
K. A. Addae-Mensah and J. P. Wikswo (2008)
Experimental Biology and Medicine 233, 792-809
   Abstract »    Full Text »    PDF »
Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen.
Ab. M. Rafiqi, S. Lemke, S. Ferguson, M. Stauber, and U. Schmidt-Ott (2008)
PNAS 105, 234-239
   Abstract »    Full Text »    PDF »
Using Bcr-Abl to Examine Mechanisms by Which Abl Kinase Regulates Morphogenesis in Drosophila.
T. L. Stevens, E. M. Rogers, L. M. Koontz, D. T. Fox, C. C.F. Homem, S. H. Nowotarski, N. B. Artabazon, and M. Peifer (2008)
Mol. Biol. Cell 19, 378-393
   Abstract »    Full Text »    PDF »
Zasp is required for the assembly of functional integrin adhesion sites.
K. Jani and F. Schock (2007)
J. Cell Biol. 179, 1583-1597
   Abstract »    Full Text »    PDF »
A wave of EGFR signaling determines cell alignment and intercalation in the Drosophila tracheal placode.
M. Nishimura, Y. Inoue, and S. Hayashi (2007)
Development 134, 4273-4282
   Abstract »    Full Text »    PDF »
Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila.
N. Gorfinkiel and A. M. Arias (2007)
J. Cell Sci. 120, 3289-3298
   Abstract »    Full Text »    PDF »
Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila.
J. Gates, J. P. Mahaffey, S. L. Rogers, M. Emerson, E. M. Rogers, S. L. Sottile, D. Van Vactor, F. B. Gertler, and M. Peifer (2007)
Development 134, 2027-2039
   Abstract »    Full Text »    PDF »
Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio)..
T. van der Meulen, H. Schipper, J. G. M. van den Boogaart, M. O. Huising, S. Kranenbarg, and J. L. van Leeuwen (2006)
Am J Physiol Regulatory Integrative Comp Physiol 291, R1040-R1048
   Abstract »    Full Text »    PDF »
Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila.
C. Laplante and L. A. Nilson (2006)
Development 133, 3255-3264
   Abstract »    Full Text »    PDF »
Effects of decreased muscle activity on developing axial musculature in nicb107 mutant zebrafish (Danio rerio).
T. van der Meulen, H. Schipper, J. L. van Leeuwen, and S. Kranenbarg (2005)
J. Exp. Biol. 208, 3675-3687
   Abstract »    Full Text »    PDF »
ROCK-I and ROCK-II cooperatively regulate closure of eyelid and ventral body wall in mouse embryo.
D. Thumkeo, Y. Shimizu, S. Sakamoto, S. Yamada, and S. Narumiya (2005)
Genes Cells 10, 825-834
   Abstract »    Full Text »    PDF »
Balance of actively generated contractile and resistive forces controls cytokinesis dynamics.
W. Zhang and D. N. Robinson (2005)
PNAS 102, 7186-7191
   Abstract »    Full Text »    PDF »
ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles.
Y. Shimizu, D. Thumkeo, J. Keel, T. Ishizaki, H. Oshima, M. Oshima, Y. Noda, F. Matsumura, M. M. Taketo, and S. Narumiya (2005)
J. Cell Biol. 168, 941-953
   Abstract »    Full Text »    PDF »
Armadillo/{beta}-catenin-dependent Wnt signalling is required for the polarisation of epidermal cells during dorsal closure in Drosophila.
V. Morel and A. M. Arias (2004)
Development 131, 3273-3283
   Abstract »    Full Text »    PDF »
Parallels between tissue repair and embryo morphogenesis.
P. Martin and S. M. Parkhurst (2004)
Development 131, 3021-3034
   Abstract »    Full Text »    PDF »
Cell movements controlled by the Notch signalling cascade during foregut development in Drosophila.
B. Fuss, F. Josten, M. Feix, and M. Hoch (2004)
Development 131, 1587-1595
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)