<i>Xenopus</i> gastrulation without a blastocoel roof

Keller, Ray; Jansa, Sharon A.

doi:10.1002/aja.1001950303

Cited by 54 publications

(45 citation statements)

References 49 publications

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“…5Cb). In agreement with previous reports, such small incisions only affect blastopore closure rates in control embryos marginally (data not shown) (Keller and Jansa, 1992). The incision on the BCR presumably relieves tension within the AC and allows the mesodermal belt to move vegetally, suggesting that epiboly plays an essential but permissive role during Xenopus gastrulation.…”

Section: Research Articlesupporting

confidence: 79%

A dominant-negative provides new insights into FAK regulation and function in early embryonic morphogenesis

2013

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SUMMARYFAK is a non-receptor tyrosine kinase involved in a wide variety of biological processes and crucial for embryonic development. In this manuscript, we report the generation of a new FAK dominant negative (FF), composed of the C terminus (FRNK) and the FERM domain of the protein. FF, unlike FRNK and FERM, mimics the localization of active FAK in the embryo, demonstrating that both domains are necessary to target FAK to its complexes in vivo. We show that the FERM domain has a role in the recruitment of FAK on focal adhesions and controls the dynamics of the protein on these complexes. Expression of FF blocks focal adhesion turnover and, unlike FRNK, acts as a dominant negative in vivo. FF expression in Xenopus results in an overall phenotype remarkably similar to the FAK knockout in mice, including loss of mesodermal tissues. Expression of FF in the animal cap revealed a previously unidentified role of FAK in early morphogenesis and specifically epiboly. We show that a fibronectin-derived signal transduced by FAK governs polarity and cell intercalation. Finally, failure of epiboly results in severe gastrulation problems that can be rescued by either mechanical or pharmacological relief of tension within the animal cap, demonstrating that epiboly is permissive for gastrulation. Overall, this work introduces a powerful new tool for the study of FAK, uncovers new roles for FAK in morphogenesis and reveals new mechanisms through which the FERM domain regulates the localization and dynamics of FAK.

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Section: Research Articlesupporting

confidence: 79%

A dominant-negative provides new insights into FAK regulation and function in early embryonic morphogenesis

2013

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“…The role of the sti¡, forcefully extending mesoderm in shaping the embryo is illustrated by experiments in which the roof of the blastocoel was removed (Keller & Jansa 1992). Under these conditions, the axial and paraxial mesodermal tissues involute and extend into the liquid medium without an overlying blastocoel roof to serve as a substratum (¢gure 4d ).…”

Section: Amphibian Convergent Extension Is An Active Force-producingmentioning

confidence: 99%

“…An external substratum, such as the overlying blastocoel roof, is not essential for convergent extension of the mesodermal tissue of Xenopus (see Keller & Jansa 1992). Likewise, the neural tissue can converge and extend without the underlying mesoderm (Keller & Danilchik 1988;Elul & Keller 2000).…”

Section: Cell ±Matrix Model Of Cell Intercalationmentioning

confidence: 99%

Mechanisms of convergence and extension by cell intercalation

Keller

Davidson

Edlund

et al. 2000

Phil. Trans. R. Soc. Lond. B

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457

394

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The cells of many embryonic tissues actively narrow in one dimension (convergence) and lengthen in the perpendicular dimension (extension). Convergence and extension are ubiquitous and important tissue movements in metazoan morphogenesis. In vertebrates, the dorsal axial and paraxial mesodermal tissues, the notochordal and somitic mesoderm, converge and extend. In amphibians as well as a number of other organisms where these movements appear, they occur by mediolateral cell intercalation, the rearrangement of cells along the mediolateral axis to produce an array that is narrower in this axis and longer in the anteroposterior axis. In amphibians, mesodermal cell intercalation is driven by bipolar, mediolaterally directed protrusive activity, which appears to exert traction on adjacent cells and pulls the cells between one another. In addition, the notochordal^somitic boundary functions in convergence and extension bỳ capturing' notochordal cells as they contact the boundary, thus elongating the boundary. The prospective neural tissue also actively converges and extends parallel with the mesoderm. In contrast to the mesoderm, cell intercalation in the neural plate normally occurs by monopolar protrusive activity directed medially, towards the midline notoplate^£oor-plate region. In contrast, the notoplate^£oor-plate region appears to converge and extend by adhering to and being towed by or perhaps migrating on the underlying notochord. Converging and extending mesoderm sti¡ens by a factor of three or four and exerts up to 0.6 m N force. Therefore, active, force-producing convergent extension, the mechanism of cell intercalation, requires a mechanism to actively pull cells between one another while maintaining a tissue sti¡ness su¤cient to push with a substantial force. Based on the evidence thus far, a cell^cell traction model of intercalation is described. The essential elements of such a morphogenic machine appear to be (i) bipolar, mediolaterally orientated or monopolar, medially directed protrusive activity; (ii) this protrusive activity results in mediolaterally orientated or medially directed traction of cells on one another; (iii) tractive protrusions are con¢ned to the ends of the cells; (iv) a mechanically stable cell cortex over the bulk of the cell body which serves as a movable substratum for the orientated or directed cell traction. The implications of this model for cell adhesion, regulation of cell motility and cell polarity, and cell and tissue biomechanics are discussed.

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“…The main ones are: (1) radial cell intercalation (RCI) in the blastocoel roof; (2) formation of bottle-shaped cells in the marginal zone, starting from the dorsal side of an embryo; (3) convergent cell intercalation (CCI) in the suprablastoporal zone (SBZ) directed towards dorso-medial embryo midline (Keller, 1987;Keller and Danilchik, 1988;Wilson et al, 1989); (4) involution around the blastoporal lip (Holtfreter, 1944;Keller, 1981Keller, , 1984Keller and Hardin, 1987). Although it has long been known (Spemann, 1936;Holtfreter, 1944;Keller and Jansa, 1992) that all of these processes can proceed, in experimental conditions, independently from each other, their rates, locations and direc-tionality are, after such an isolation, largely distorted. Meanwhile, in an entire embryo they are perfectly coordinated and enhance each other.…”

Section: Introductionmentioning

confidence: 99%

Gastrulation in amphibian embryos, regarded as a succession of biomechanical feedback events

Beloussov¹,

Luchinskaya²,

Ермаков³

et al. 2006

Int. J. Dev. Biol.

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Gastrulation in amphibian embryos is a composition of several differently located morphogenetic movements which are perfectly coordinated with each other both in space and time. We hypothesize that this coordination is mediated by biomechanical interactions between different parts of a gastrulating embryo based upon the tendency of each part to hyper-restore the value of its mechanical stress (see Beloussov and Grabovsky, 2006). The entire process of gastrulation in amphibian embryos is considered as a chain of these mutually coupled reactions, which are largely dependent upon the geometry of a given embryo part. We divide gastrulation into several partly overlapped steps, give a theoretical interpretation for each of them, formulate the experiments for testing our interpretation and describe the experimental results which confirm our point of view. Among the predicted experimental results are: inhibition of radial cell intercalation by relaxation of tensile stresses at the blastula stage; inversion of convergent intercalation movements by relaxation of circumferential stresses at the early gastrula stage; stress-promoted reorientation of axial rudiments, and others. We also show that gastrulation is going on under a more or less constant average value of tensile stresses which may play a role as rate-limiting factors. A macromorphological biomechanical approach developed in this paper is regarded as complementary to exploring the molecular machinery of gastrulation.

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Xenopus gastrulation without a blastocoel roof

Cited by 54 publications

References 49 publications

A dominant-negative provides new insights into FAK regulation and function in early embryonic morphogenesis

A dominant-negative provides new insights into FAK regulation and function in early embryonic morphogenesis

Mechanisms of convergence and extension by cell intercalation

Gastrulation in amphibian embryos, regarded as a succession of biomechanical feedback events

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