The cellular basis of the convergence and extension of the <i>Xenopus</i> neural plate

Keller, Ray; Shih, John; Sater, Amy K.

doi:10.1002/aja.1001930302

Cited by 223 publications

(164 citation statements)

References 44 publications

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“…In the experimental embryo, the sharp bend (at the third square from the left) is a place where the notochord extends some distance directly toward the viewer, and thus the axis of extension is considerably longer than is apparent in profile. appear to stick tightly to one another by the late gastrula (see Keller et al, 1992b), and then the two extend together and plunge ventrally into the endoderm, forming a pit as early as stage 12 (pointer, Fig. 8b), which subsequently deepens ( Fig.…”

Section: Extension Of Axial Mesoderm In the Absence Of The Ac And Nimzmentioning

confidence: 99%

Xenopus gastrulation without a blastocoel roof

Keller

Jansa

1992

Developmental Dynamics

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The objective of this paper is to determine the function in gastrulation of several of the five major regional morphogenetic processes in the African clawed frog, Xenopus laevis. These regional processes are (1) epiboly of the animal cap (AC); (2) migration of the mesoderm on the roof of the blastocoel; (3) convergence and extension of the dorsal, noninvoluting marginal zone (NIMZ); (4) formation of the bottle cells at the site of blastopore formation; and ( 5 ) convergence and extension of the involuting marginal zone (IMZ). After the AC and the NIMZ were removed, thus eliminating the first three of these processes, the IMZ involuted, constricted, and closed the blastopore. It also converged and extended to form notochord and somites, although these tissues were often crooked and sank into or were covered over by the vegetal endoderm. When the AC was removed, the dorsal axial mesoderm involuted and stuck to the inner surface of the NIMZ. The IMZ and NIMZ converged and extended together to form a longer, straighter axis than that formed by the IMZ alone. Moreover, presence of the NIMZ also prevented the sinking of the IMZ into the endoderm. Misalignment of the available AC-NIMZ substratum and the IMZ at the beginning of gastrulation suggested that the IMZ determines the general direction of its own extension. Absence of the AC-NIMZ accelerated and increased the normal effects of bottle cell formation on the IMZ and vegetal endoderm. In absence of the AC-NIMZ as a substratum on which to migrate, prechordal mesoderm was pushed anteriorly by the converging and extending mesoderm behind it, but it did not spread normally. We conclude that (1) involution and blastopore closure by the IMZ can occur without pushing by epiboly and convergence and extension of the NIMZ-AC; (2) involution and blastopore closure can occur without migration of the mesoderm on the blastocoel roof; (3) convergence and extension of the IMZ are sufficient to bring about IMZ involution and blastopore closure; (4) the function of bottle cells in initiating involution is retarded by presence of the NJMZ-AC; (5) the associated dorsal NIMZ and IMZ together form an axis that extends better and is perhaps stiffer than the IMZ alone; and (6) the dorsal axial and paraxial mesoderm form the "skeleton" around which the mechanics of the other parts of the embryo are organized. These findings are important for the

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Section: Extension Of Axial Mesoderm In the Absence Of The Ac And Nimzmentioning

confidence: 99%

Xenopus gastrulation without a blastocoel roof

Keller

Jansa

1992

Developmental Dynamics

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“…The tissue immediately animal to the DIMZ, the dorsal noninvoluting marginal zone (DNIMZ), also converges and 0 1992 WILEY-LISS, INC. extends in sandwich explants (Keller et al, 1985a,b;Keller and Danilchick, 1988) (see Fig. 1 of the companion article, Keller et al, 1992), but it differentiates as neural rather than mesodermal and endodermal tissue (Keller and Danilchik, 1988;Sater et al, 1992). This tissue corresponds to prospective hindbrain and spinal cord .…”

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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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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“…In vertebrates, convergent extension occurs in the prospective hindbrain and spinal chord neuroectoderm, whereas the fore-and midbrain neuroectoderm is devoid of these movements at open neural plate stages (6,7). The boundary between these regions (the later midbrain-hindbrain boundary) is set at gastrula stages, where it is first apparent as a molecular boundary between the anterior otx-expressing region and the posteriorly adjacent stripe of gbx expression (33).…”

Section: An Otx-gbx Morphogenetic Boundary Anteriorly Delimitates Thementioning

confidence: 99%

“…1 A). Such reshaping of tissue is reminiscent of the convergent extension movements of the trunk neuroectoderm (and underlying mesoderm) in Xenopus (7,17), chick (18), and zebrafish (5), which is driven, at least in large part, by polarized cell rearrangement such as mediolateral cell intercalation (19). This prompted us to investigate convergent extension movements of the polychaete neuroectoderm on the cellular level.…”

Section: P Dumerilii Undergoes Convergent Extension By Mediolateral mentioning

confidence: 99%

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Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Steinmetz

Zelada-Gonzáles

Burgtorf

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball-into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.amphistomy ͉ axis formation ͉ convergent extension ͉ gastrulation

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The cellular basis of the convergence and extension of the Xenopus neural plate

Cited by 223 publications

References 44 publications

Xenopus gastrulation without a blastocoel roof

Xenopus gastrulation without a blastocoel roof

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

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

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