Journal of Cell Science, Vol 114, Issue 3 493-501, Copyright © 2001 by Company of Biologists

JOURNAL ARTICLES

Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells

H Oda and S Tsukita
Tsukita Cell Axis Project, Exploratory Research for Advanced Technology, Japan Science and Technology Corporation, Kyoto Research Park, Chudoji Minami-machi, Shimogyo-ku, Kyoto 600-8813, Japan. hoda@cell.tsukita.jst.go.jp

Invagination of the epithelial cell sheet of the prospective mesoderm in Drosophila gastrulation is a well-studied, relatively simple morphogenetic event that results from dynamic cell shape changes and cell movements. However, these cell behaviors have not been followed at a sufficiently short time resolution. We examined mesoderm invagination in living wild-type embryos by real-time imaging of fluorescently labeled cell-cell adherens junctions, which are located at the apical zones of cell-cell contact. Low-light fluorescence video microscopy directly visualized the onset and progression of invagination. In an initial period of approximately 2 minutes, cells around the ventral midline reduced their apical surface areas slowly in a rather synchronous manner. Next, the central and more lateral cells stochastically accelerated or initiated their apical constriction, giving rise to random arrangements of cells with small and relatively large apices. Thus, we found that mesoderm invagination began with slow synchronous and subsequent fast stochastic phases of cell apex constriction. Furthermore, we showed that the mesoderm invagination of folded gastrulation mutant embryos lacked the normal two constriction phases, and instead began with asynchronous, feeble cell shape changes. Our observations suggested that Folded gastrulation-mediated signaling enabled synchronous activation of the contractile cortex, causing competition among the individual mesodermal cells for apical constriction. Movies available on-line: http://www.biologists.com/JCS/movies/jcs2073.html
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				M. Bischoff and Z. Cseresnyes Cell rearrangements, cell divisions and cell death in a migrating epithelial sheet in the abdomen of Drosophila Development, July 15, 2009; 136(14): 2403 - 2411. [Abstract] [Full Text] [PDF]

				M. A. McGill, R.F. A. McKinley, and T. J.C. Harris Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions J. Cell Biol., June 1, 2009; 185(5): 787 - 796. [Abstract] [Full Text] [PDF]

				N. Gorfinkiel, G. B. Blanchard, R. J. Adams, and A. Martinez Arias Mechanical control of global cell behaviour during dorsal closure in Drosophila Development, June 1, 2009; 136(11): 1889 - 1898. [Abstract] [Full Text] [PDF]

				J. Huang, W. Zhou, W. Dong, A. M. Watson, and Y. Hong From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering PNAS, May 19, 2009; 106(20): 8284 - 8289. [Abstract] [Full Text] [PDF]

				K. L. Pope and T. J. C. Harris Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis in Drosophila Development, July 1, 2008; 135(13): 2227 - 2238. [Abstract] [Full Text] [PDF]

				M. Zmojdzian, J. P. Da Ponte, and K. Jagla Cellular components and signals required for the cardiac outflow tract assembly in Drosophila PNAS, February 19, 2008; 105(7): 2475 - 2480. [Abstract] [Full Text] [PDF]

				N. Dyer, E. Rebollo, P. Dominguez, N. Elkhatib, P. Chavrier, L. Daviet, C. Gonzalez, and M. Gonzalez-Gaitan Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes Development, December 15, 2007; 134(24): 4437 - 4447. [Abstract] [Full Text] [PDF]

				M. Nishimura, Y. Inoue, and S. Hayashi A wave of EGFR signaling determines cell alignment and intercalation in the Drosophila tracheal placode Development, December 1, 2007; 134(23): 4273 - 4282. [Abstract] [Full Text] [PDF]

				N. Gorfinkiel and A. M. Arias Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila J. Cell Sci., September 15, 2007; 120(18): 3289 - 3298. [Abstract] [Full Text] [PDF]

				D. Chandraratna, N. Lawrence, D. P. Welchman, and B. Sanson An in vivo model of apoptosis: linking cell behaviours and caspase substrates in embryos lacking DIAP1 J. Cell Sci., August 1, 2007; 120(15): 2594 - 2608. [Abstract] [Full Text] [PDF]

				N. Ninov, D. A. Chiarelli, and E. Martin-Blanco Extrinsic and intrinsic mechanisms directing epithelial cell sheet replacement during Drosophila metamorphosis Development, January 15, 2007; 134(2): 367 - 379. [Abstract] [Full Text] [PDF]

				S. Simoes, B. Denholm, D. Azevedo, S. Sotillos, P. Martin, H. Skaer, J. C.-G. Hombria, and A. Jacinto Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis Development, November 1, 2006; 133(21): 4257 - 4267. [Abstract] [Full Text] [PDF]

				P. S. Pereira, A. Teixeira, S. Pinho, P. Ferreira, J. Fernandes, C. Oliveira, R. Seruca, G. Suriano, and F. Casares E-cadherin missense mutations, associated with hereditary diffuse gastric cancer (HDGC) syndrome, display distinct invasive behaviors and genetic interactions with the Wnt and Notch pathways in Drosophila epithelia Hum. Mol. Genet., May 15, 2006; 15(10): 1704 - 1712. [Abstract] [Full Text] [PDF]

				R. E. Dawes-Hoang, K. M. Parmar, A. E. Christiansen, C. B. Phelps, A. H. Brand, and E. F. Wieschaus folded gastrulation, cell shape change and the control of myosin localization Development, September 15, 2005; 132(18): 4165 - 4178. [Abstract] [Full Text] [PDF]

				B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration J. Cell Biol., February 14, 2005; 168(4): 567 - 573. [Abstract] [Full Text] [PDF]

				C. W. Larsen, E. Hirst, C. Alexandre, and J.-P. Vincent Segment boundary formation in Drosophila embryos Development, December 1, 2003; 130(23): 5625 - 5635. [Abstract] [Full Text] [PDF]

				F. Schock and N. Perrimon Retraction of the Drosophila germ band requires cell-matrix interaction Genes & Dev., March 1, 2003; 17(5): 597 - 602. [Abstract] [Full Text] [PDF]