The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo

Rozario, Tania; Dzamba, Bette J.; Weber, Gregory F.; Davidson, Lance A.; DeSimone, Douglas W.

doi:10.1016/j.ydbio.2008.12.025

Cited by 94 publications

(110 citation statements)

References 62 publications

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“…The mild defects induced by FF in mesodermal morphogenesis are in contrast to the severe defects induced in the AC and in agreement with the requirement of fibrillar FN for epiboly but not for convergent extension (Davidson et al, 2006;Marsden and DeSimone, 2001;Rozario et al, 2009). Here, we show that, despite the presence of a fibrillar matrix, both radial intercalation and cell polarity are lost in FF expressors, suggesting that an integrin-dependent polarizing signal is required for both processes.…”

Section: Research Articlesupporting

confidence: 88%

“…We postulated that this is due to the fact that in the absence of radial intercalation and BCR thinning, the mesodermal belt and the blastopore are held back, unable to move vegetally. This, coupled with the fact that mediolateral intercalation proceeds normally, leads to constriction of the embryo at the equatorial region and produces the characteristic mushroom-shaped embryos also seen in the 70 kDa FN experiments (Rozario et al, 2009). If this explanation is correct, one would expect increased tension in FF ACs.…”

Section: Epiboly Plays An Essential But Permissive Role During Xenopumentioning

confidence: 93%

“…Studies in Xenopus have shown that FNintegrin interactions are essential for proper embryonic development, regulating major morphogenetic movements during 4267 RESEARCH ARTICLE FAK in Xenopus development gastrulation and neurulation. Disruption of these interactions leads to radial intercalation failure and loss of polarity in the deep ectodermal cells of the animal cap (AC) (Davidson et al, 2006;Marsden and DeSimone, 2001;Rozario et al, 2009). Both processes are required for epiboly, the morphogenetic movement that drives the thinning and expansion that allow the ectoderm to encompass the entire embryo by the end of gastrulation (Keller, 1980).…”

Section: Introductionmentioning

confidence: 99%

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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: 88%

Section: Epiboly Plays An Essential But Permissive Role During Xenopumentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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

2013

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“…Therefore, aligned ECM fibrils appear to orient mesodermal cell migration on the BCR through a contact guidance mechanism (Nakatsuji and Johnson, 1984). This mechanism appears to involve fibronectin (FN), which is a major component of the BCR fibrillar network (Boucaut and Darribere, 1983;Davidson et al, 2004;Johnson et al, 1992); blockage of FN synthesis, function or fibrillar assembly, as well as abrogation of the integrin α5β1 receptor, leads to abnormal adhesion, spreading and migration of mesodermal cells (Boucaut et al, 1990;Darribere and Schwarzbauer, 2000;Davidson et al, 2002;Nagel and Winklbauer, 1999;Rozario et al, 2009). Upon contact with FN, mesodermal cells relocalise their intrinsic protrusive activity along the BCR surface and replace filopodia with lamelliform protrusions (Winklbauer and Keller, 1996;Winklbauer and Nagel, 1991;Winklbauer and Selchow, 1992).…”

Section: Ecm-and Cell Contact-guided Migration During Developmentmentioning

confidence: 99%

Cell migration: from tissue culture to embryos

2014

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Cell migration is a fundamental process that occurs during embryo development. Classic studies using in vitro culture systems have been instrumental in dissecting the principles of cell motility and highlighting how cells make use of topographical features of the substrate, cell-cell contacts, and chemical and physical environmental signals to direct their locomotion. Here, we review the guidance principles of in vitro cell locomotion and examine how they control directed cell migration in vivo during development. We focus on developmental examples in which individual guidance mechanisms have been clearly dissected, and for which the interactions among guidance cues have been explored. We also discuss how the migratory behaviours elicited by guidance mechanisms generate the stereotypical patterns of migration that shape tissues in the developing embryo.

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“…It has been reported that the assembly and three-dimensional fibrillar organization of FN regulate cell adhesion, spreading and migration in Xenopus embryos (Darribere and Schwarzbauer, 2000;Rozario et al, 2009). The 70-kD N-terminal fragment of FN (70 kD-FN) was shown to obstruct FN matrix formation (Rozario et al, 2009). We confirmed that 70 kD-FN perturbed the formation of the FN fibrils in vitro and in zebrafish embryos (supplementary material Fig.…”

Section: Stat3-efemp2a Controls the Configuration Of The Ecm For The mentioning

confidence: 99%

Stat3-Efemp2a modulates the fibrillar matrix for cohesive movement of prechordal plate progenitors

et al. 2014

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Recently, emerging evidence has shown that Stat3 controls tumor cell migration and invasion. However, the molecular mechanisms by which Stat3 controls the cell movement remain largely unknown. Embryonic gastrula progenitors display coordinated and orientated migration, called collective cell migration. Collective cell migration is the simultaneous movement of multiple cells and is universally involved in physiological and pathological programs. Stat3 activity is required for the migration of gastrula progenitors, but it does not affect cell specification, thus suggesting that gastrula movements are an excellent model to provide insight into Stat3 control of cell migration in vivo. In this study, we reveal a novel mechanism by which Stat3 modulates extracellular matrix (ECM) assembly to control the coherence of collective migration of prechordal plate progenitors during zebrafish embryonic gastrulation. We show that Stat3 regulates the expression of Efemp2a in the prechordal plate progenitors that migrate anteriorly during gastrulation. Alteration of Stat3-Efemp2a signaling activity disrupted the configuration of fibronectin (FN) and laminin (LM) matrices, resulting in defective coherence of prechordal plate progenitor movements in zebrafish embryos. We demonstrate that Efemp2a acts as a downstream effector of Stat3 to promote ECM configuration for coherent collective cell migrations in vivo.

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The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo

Cited by 94 publications

References 62 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

Cell migration: from tissue culture to embryos

Stat3-Efemp2a modulates the fibrillar matrix for cohesive movement of prechordal plate progenitors

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