Cell Motility, Control and Function of Convergence and Extension during Gastrulation in Xenopus

Keller, Ray; Shih, John; Wilson, P. David

doi:10.1007/978-1-4684-6027-8_6

Cited by 125 publications

(189 citation statements)

References 37 publications

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“…Collectively, these movements of convergence (narrowing or constriction) and extension (lengthening or stretching) of the IMZ are thought to squeeze the blastopore shut and elongate the anterior-posterior body axis (Vogt 1929;Keller et al 1992a). In the early amphibian embryos, tissue volume is conserved, and convergence produces predominantly extension, in which case it is often called 'convergent extension', or produces predominantly thickening, in which case it is called 'convergent thickening' (Keller & Danilchik 1988;. In Xenopus, the African clawed frog, convergent extension is driven by active mediolateral intercalation of cells in the presumptive notochordal and somitic mesoderm, which generates hoop stress, an arc of tension, around the inside of the blastoporal lip, thus aiding involution of the IMZ and the squeezing of the blastopore shut, while simultaneously elongating the body axis (figure 1a).…”

Section: Summary Of the Function Of Convergent Extension And Convergementioning

confidence: 99%

“…The expression of convergent extension in the presumptive notochordal and somitic mesoderm (see fusiform shapes, dark and light grey areas in figure 1a) on the dorsal side of the gastrula is complemented by the expression of convergent thickening on the ventral side (rectangles, medium grey in figure 1a). In convergent thickening, convergence appears to generate a thicker tissue rather than a longer one, but the cellular basis is not known (Keller & Danilchik 1988). Because convergence on the dorsolateral aspect of the gastrula produces much extension, whereas convergence on the ventral aspect produces little extension and more thickening, the blastopore closes asymmetrically towards the ventral side (arrows, figure 1a,d ).…”

Section: Summary Of the Function Of Convergent Extension And Convergementioning

confidence: 99%

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Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore

Keller

Shook

2008

Phil. Trans. R. Soc. B

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We review the dynamic patterns of cell behaviours in the marginal zone of amphibians with a focus on how the progressive nature and the geometry of these behaviours drive blastopore closure. Mediolateral cell intercalation behaviour and epithelial-mesenchymal transition are used in different combinations in several species of amphibian to generate a conserved pattern of circumblastoporal hoop stresses. Although these cell behaviours are quite different and involve different germ layers and tissue organization, they are expressed in similar patterns. They are expressed progressively along presumptive lateral-medial and anterior-posterior axes of the body plan in highly ordered geometries of functional significance in the context of the biomechanics of blastopore closure, thereby accounting for the production of similar patterns of circumblastoporal forces. It is not the nature of the cell behaviour alone, but the context, the biomechanical connectivity and spatial and temporal pattern of its expression that determine specificity of morphogenic output during gastrulation and blastopore closure. Understanding the patterning of these dynamic features of cell behaviour is important and will require analysis of signalling at much greater spatial and temporal resolution than that has been typical in the analysis of patterning tissue differentiation.

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Section: Summary Of the Function Of Convergent Extension And Convergementioning

confidence: 99%

Section: Summary Of the Function Of Convergent Extension And Convergementioning

confidence: 99%

Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore

Keller

Shook

2008

Phil. Trans. R. Soc. B

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“…Dorsoventral patterning of the mesoderm affects CE movements indirectly by impacting cell fates in the DMZ (Keller and Danilchik, 1988). To examine this possibility, RT-PCR analysis was performed using several marker genes.…”

Section: Rok␣ Is Involved In Xenopus Ce Movements Without Affecting Gmentioning

confidence: 99%

JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

Kim

Han

2005

Developmental Dynamics

105

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The Wnt/planar cell polarity (PCP) pathway plays a critical role in wing, eye, and sensory bristle development of Drosophila and in convergent extension (CE) movements during vertebrate gastrulation. In Drosophila, Jun N-terminal kinase (JNK) and Rho-associated kinase (ROK) participate in RhoA-mediated PCP pathway during eye and wing development. In mammalian cells, Rac1 and Cdc42 but not RhoA are required for JNK activation by Wnt/PCP signals. However, there has been no evidence that Rho GTPases regulate JNK activation in Wnt/PCP pathway during Xenopus CE movements. Here, we report that Xenopus RhoA (XRhoA), but not Xenopus Cdc42 (XCdc42), is essential for JNK activation downstream of the Wnt/PCP pathway during Xenopus CE movements, and the phenotypic effect of loss of XRhoA function was rescued by Xenopus JNK1 (XeJNK1). In addition, XRhoA rescues the inhibition of CE movements by the DEP domain deletion mutant of Xenopus Dsh (Xdsh-⌬DEP), which has dominant negative (DN) effects on JNK activation, and the PDZ domain deletion mutant of Xdsh (Xdsh-⌬PDZ). Moreover, we demonstrate that Xenopus Rho-associated kinase ␣ (xROK␣), which is expressed mainly in mesoderm and ectoderm that undergo extensive cell rearrangements, regulates CE movements without affecting gene expression, and injection of xROK␣ rescued the inhibition of CE movements caused by DN XRhoA. Finally, we show that ROK␣ and JNK synergistically rescued embryos overexpressing DN XRhoA, which exhibit gastrulation defects, although ROK␣ is not required for JNK activation. Together, these data suggest that JNK and ROK␣ function in the noncanonical Wnt/RhoA pathway to regulate Xenopus CE movements. Developmental Dynamics 232: 958 -968, 2005.

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“…Sandwich explants of the dorsal sector of the Xenopus early gastrula exhibit two regions of convergence and extension during gastrulation and neurulation (Keller et al, 1985a,b;Keller and Danilchik, 1988). The dorsal involuting marginal zone (DIMZ) converges and extends, forming the axial and paraxial mesodermal tissues and the archenteron roof.…”

Section: Introductionmentioning

confidence: 99%

“…There is evidence that the lateral limits of the neural plate are established by homeogenetic, planar signals passing laterally from the midline of the prospective neural plate (Nieuwkoop, 1985;Servetnick and Grainger, 1991). A number of investigators (Akers et al, 1986;London et al, 1988;Savage and Phillips, 1989;Kintner and Melton, 1987;Keller and Danilchik, 1988;Jacobson and Sater, 1988;Dixon and Kintner, 1989;Sater et al, 1992;Doniach et al, 1992; reviewed in Phillips, 1991) have presented new evidence for planar neural-inducing signals emanating from the animal end of the organizer in the early gastrula stage. But the absence of vertical interactions in these experiments has generally not been documented rigorously.…”

Section: Introductionmentioning

confidence: 99%

Planar induction of convergence and extension of the neural plate by the organizer of Xenopus

Keller

Shih

Sater

et al. 1992

Developmental Dynamics

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122

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This paper demonstrates that convergence and extension within the neural plate of Xenopus laevis are regulated by planar inductive interactions with the adjacent Spemann organizer. The companion article (Keller et al.: Developmental Dynamics 193:199-217, 1992) showed that the prospective hindbrain and spinal cord occupy a very short and very wide area just above the Spemann organizer in the early gastrula and that these regions converge and extend greatly during gastrulation and neurulation, using a sequence of radial and mediolateral cell intercalations. In this article, we show that "planar" contact of these regions with the organizer at their vegetal edge until stage 11 is sufficient to induce convergence and extension, after which their convergence and extension become autonomous. Grafts of the organizer in planar contact with uninduced ectodermal tissues induce these ectoderma1 tissues to converge and extend by a planar inductive signal from the organizer. Labeling of the inducing or responding tissues confirms that only planar interactions occur. Neural convergence and extension are actually hindered in explants deliberately constructed so that vertical interactions occur. These results show unambiguously that the Spemann organizer induces the extraordinary and precocious convergence and extension movements of the Xenopus neural plate by planar interactions acting over short distances.

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Cell Motility, Control and Function of Convergence and Extension during Gastrulation in Xenopus

Cited by 125 publications

References 37 publications

Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore

Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore

JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

Planar induction of convergence and extension of the neural plate by the organizer of Xenopus

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