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Development
2008 Aug 01;13514:2435-44. doi: 10.1242/dev.014704.
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Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network.
Skoglund P
,
Rolo A
,
Chen X
,
Gumbiner BM
,
Keller R
.
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Force-producing convergence (narrowing) and extension (lengthening) of tissues by active intercalation of cells along the axis of convergence play a major role in axial morphogenesis during embryo development in both vertebrates and invertebrates, and failure of these processes in human embryos leads to defects including spina bifida and anencephaly. Here we use Xenopus laevis, a system in which the polarized cell motility that drives this active cell intercalation has been related to the development of forces that close the blastopore and elongate the body axis, to examine the role of myosin IIB in convergence and extension. We find that myosin IIB is localized in the cortex of intercalating cells, and show by morpholino knockdown that this myosin isoform is essential for the maintenance of a stereotypical, cortical actin cytoskeleton as visualized with time-lapse fluorescent confocal microscopy. We show that this actin network consists of foci or nodes connected by cables and is polarized relative to the embryonic axis, preferentially cyclically shortening and lengthening parallel to the axis of cell polarization, elongation and intercalation, and also parallel to the axis of convergence forces during gastrulation. Depletion of MHC-B results in disruption of this polarized cytoskeleton, loss of the polarized protrusive activity characteristic of intercalating cells, eventual loss of cell-cell and cell-matrix adhesion, and dose-dependent failure of blastopore closure, arguably because of failure to develop convergence forces parallel to the myosin IIB-dependent dynamics of the actin cytoskeleton. These findings bridge the gap between a molecular-scale motor protein and tissue-scale embryonic morphogenesis.
Fig. 3. Myosin IIB MO-mediated failure of gastrulation is dose dependent. (A-D) Still images from simultaneous time-lapse videorecordings showing vegetal views of control (A) and morphant Xenopus embryos injected with 2.5 μM (B), 5 μM (C) and 10 μM (D) MHC-B MO. Embryos are oriented with their dorsal side up. At stage 10 (t=0), bottle cells form in the dorsal lip of the blastopore of all control and morphant embryos. By control stage 12 (t=2.5), ventral bottle cells have formed in all control and morphant embryos, but blastopore closure is delayed in a MHC-B MO dose-dependent manner. The site of blastopore closure in 2.5 μM (B, t=7.5) morphant embryos is not located as ventrally as in control embryos (A, t=7.5). Asterisks indicate the center of the yolk plug at t=0 and the point of blastopore closure at t=7.5. (E-H) RNA in situ hybridizations of stage-13 embryos for brachyury expression reveals the extent of notochordal morphogenesis in a control embryo (E), and reduced notochordal morphogenesis in a 5 μM morphant (F). The 5μ M morphant embryos exhibit some variability in notochordal extension (G), but 10 μM morphant embryos essentially lack notochord extension (H).
Amaya,
FGF signalling in the early specification of mesoderm in Xenopus.
1993, Pubmed,
Xenbase
Amaya,
FGF signalling in the early specification of mesoderm in Xenopus.
1993,
Pubmed
,
Xenbase
Beningo,
Flexible substrata for the detection of cellular traction forces.
2002,
Pubmed
Beningo,
Flexible polyacrylamide substrata for the analysis of mechanical interactions at cell-substratum adhesions.
2002,
Pubmed
Berg,
A millennial myosin census.
2001,
Pubmed
Bertet,
Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation.
2004,
Pubmed
Bhatia-Dey,
Cloning of the cDNA encoding a myosin heavy chain B isoform of Xenopus nonmuscle myosin with an insert in the head region.
1993,
Pubmed
,
Xenbase
Bhatia-Dey,
Differential expression of non-muscle myosin heavy chain genes during Xenopus embryogenesis.
1998,
Pubmed
,
Xenbase
Blankenship,
Multicellular rosette formation links planar cell polarity to tissue morphogenesis.
2006,
Pubmed
Brieher,
Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps.
1994,
Pubmed
,
Xenbase
Chen,
Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity.
2006,
Pubmed
,
Xenbase
Conti,
Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice.
2004,
Pubmed
Finnemann,
Cadherin transfection of Xenopus XTC cells downregulates expression of substrate adhesion molecules.
1995,
Pubmed
,
Xenbase
Geeves,
The molecular mechanism of muscle contraction.
2005,
Pubmed
Geeves,
Structural mechanism of muscle contraction.
1999,
Pubmed
Glickman,
Shaping the zebrafish notochord.
2003,
Pubmed
Golomb,
Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family.
2004,
Pubmed
Goto,
The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus.
2002,
Pubmed
,
Xenbase
Hardin,
The behaviour and function of bottle cells during gastrulation of Xenopus laevis.
1988,
Pubmed
,
Xenbase
Harris,
Silicone rubber substrata: a new wrinkle in the study of cell locomotion.
1980,
Pubmed
Heisenberg,
Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation.
2000,
Pubmed
Holmes,
The structural basis of muscle contraction.
2000,
Pubmed
Iwaki,
drumstick, bowl, and lines are required for patterning and cell rearrangement in the Drosophila embryonic hindgut.
2001,
Pubmed
Jaffe,
Differential effects of the cytoplasmic domains of cell adhesion molecules on cell aggregation and sorting-out.
1990,
Pubmed
Keller,
An experimental analysis of the role of bottle cells and the deep marginal zone in gastrulation of Xenopus laevis.
1981,
Pubmed
,
Xenbase
Keller,
Mechanisms of convergence and extension by cell intercalation.
2000,
Pubmed
Keller,
Shaping the vertebrate body plan by polarized embryonic cell movements.
2002,
Pubmed
Keller,
How we are shaped: the biomechanics of gastrulation.
2003,
Pubmed
,
Xenbase
Keller,
Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis.
1988,
Pubmed
,
Xenbase
Keller,
Cell intercalation during notochord development in Xenopus laevis.
1989,
Pubmed
,
Xenbase
Keller,
The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser.
1992,
Pubmed
,
Xenbase
Keller,
Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer.
1976,
Pubmed
,
Xenbase
Kelley,
Xenopus nonmuscle myosin heavy chain isoforms have different subcellular localizations and enzymatic activities.
1996,
Pubmed
,
Xenbase
Kintner,
Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction.
1987,
Pubmed
,
Xenbase
Kolega,
Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture.
1986,
Pubmed
Kolega,
Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells.
1998,
Pubmed
Laevsky,
Under-agarose folate chemotaxis of Dictyostelium discoideum amoebae in permissive and mechanically inhibited conditions.
2001,
Pubmed
Laevsky,
Cross-linking of actin filaments by myosin II is a major contributor to cortical integrity and cell motility in restrictive environments.
2003,
Pubmed
Landsverk,
Genetic analysis of myosin II assembly and organization in model organisms.
2005,
Pubmed
Lee,
Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin.
1995,
Pubmed
,
Xenbase
Lengyel,
It takes guts: the Drosophila hindgut as a model system for organogenesis.
2002,
Pubmed
Litman,
Imaging of dynamic changes of the actin cytoskeleton in microextensions of live NIH3T3 cells with a GFP fusion of the F-actin binding domain of moesin.
2000,
Pubmed
Lo,
Cell movement is guided by the rigidity of the substrate.
2000,
Pubmed
Lo,
Nonmuscle myosin IIb is involved in the guidance of fibroblast migration.
2004,
Pubmed
Marsden,
Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus.
2003,
Pubmed
,
Xenbase
Maupin,
Differential localization of myosin-II isozymes in human cultured cells and blood cells.
1994,
Pubmed
Myers,
Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity?
2002,
Pubmed
Niessen,
Cadherin-mediated cell sorting not determined by binding or adhesion specificity.
2002,
Pubmed
,
Xenbase
Ninomiya,
Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning.
2004,
Pubmed
,
Xenbase
O'Toole,
Integrin cytoplasmic domains mediate inside-out signal transduction.
1994,
Pubmed
Rayment,
The three-dimensional structure of a molecular motor.
1994,
Pubmed
Rochlin,
Localization of myosin II A and B isoforms in cultured neurons.
1995,
Pubmed
Sepich,
Role of the zebrafish trilobite locus in gastrulation movements of convergence and extension.
2000,
Pubmed
Shewan,
Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts.
2005,
Pubmed
Shih,
Cell motility driving mediolateral intercalation in explants of Xenopus laevis.
1992,
Pubmed
,
Xenbase
Shih,
Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis.
1992,
Pubmed
,
Xenbase
Skoglund,
Xenopus fibrillin is expressed in the organizer and is the earliest component of matrix at the developing notochord-somite boundary.
2006,
Pubmed
,
Xenbase
Skoglund,
Xenopus fibrillin regulates directed convergence and extension.
2007,
Pubmed
,
Xenbase
Tada,
Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway.
2000,
Pubmed
,
Xenbase
Tao,
G-protein-coupled signals control cortical actin assembly by controlling cadherin expression in the early Xenopus embryo.
2007,
Pubmed
,
Xenbase
Vicente-Manzanares,
Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells.
2007,
Pubmed
Winklbauer,
Conditions for fibronectin fibril formation in the early Xenopus embryo.
1998,
Pubmed
,
Xenbase
Xu,
During multicellular migration, myosin ii serves a structural role independent of its motor function.
2001,
Pubmed
Xu,
Cell-cell adhesion prevents mutant cells lacking myosin II from penetrating aggregation streams of Dictyostelium.
1996,
Pubmed
Zallen,
Patterned gene expression directs bipolar planar polarity in Drosophila.
2004,
Pubmed
Zallen,
Planar polarity and tissue morphogenesis.
2007,
Pubmed
Zhong,
Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody.
1999,
Pubmed
,
Xenbase
