Cell intercalation during notochord development in <i>Xenopus laevis</i>

Keller, Ray; Cooper, Mark S.; Danilchik, Michael V.; Tibbetts, Paul; Wilson, P. David

doi:10.1002/jez.1402510204

Cited by 132 publications

(133 citation statements)

References 25 publications

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“…For example, by early tailbud stages the notochord is surrounded by XF and the other matrix molecules that comprise the rounded notochordal sheath. In this context, cell behavior becomes uniform around the periphery of the notochord as cells adopt the "pizza slice" morphology characteristic of differentiated notochord, distinct from MIB (Keller et al, 1989). XF becomes widely expressed at this stage and is also found surrounding the neural tube, somites, and other tissue boundaries, consistent with the idea of it having a role in boundary-dependent signaling events or as a mechanical element in the early embryo.…”

Section: Possible Functions For Xf In Convergence and Extensionsupporting

confidence: 53%

Xenopus fibrillin is expressed in the organizer and is the earliest component of matrix at the developing notochord‐somite boundary

Skoglund

Dzamba

Coffman

et al. 2006

Developmental Dynamics

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We identify a Xenopus fibrillin homolog (XF), and show that its earliest developmental expression is in presumptive dorsal mesoderm at gastrulation, and that XF expression is regulated by mesoderm-inducing factors in animal cap assays. XF protein is also first detected in presumptive mesoderm, but is concentrated specifically into extracellular-matrix structures that begin to develop de novo by mid-gastrulation at both of the bilateral presumptive notochord-somite boundaries. Later in embryogenesis, XF protein is localized to the extracellular matrix at tissue boundaries, where it is found surrounding the notochord, the somites, and the neural tube, as well as under the epidermis. This pattern of protein deposition combines to give the appearance of an "embryonic skeleton," suggesting that one role for XF is to serve as a mechanical element in the embryo prior to bone deposition.

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Section: Possible Functions For Xf In Convergence and Extensionsupporting

confidence: 53%

Xenopus fibrillin is expressed in the organizer and is the earliest component of matrix at the developing notochord‐somite boundary

Skoglund

Dzamba

Coffman

et al. 2006

Developmental Dynamics

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“…In these embryos, the labeled cells were pushed ahead of the extending axial mesoderm, but they remained as a thick clump (Fig. 12a-d) and did not spread in a thin sheet as they do in normal development (Keller and Tibbetts, 1989; …”

Section: Failure Of Mesoderm Migration In Absence Of the Ac And Nimzmentioning

confidence: 92%

“…The specimens were then processed for sectioning by returning them to Histosol, embedding in Paraplast, and sectioning at 9 km. For cell marking, fluorescein dextran amine (FDA) was in-jected after fertilization and labeled cells were grafted from labeled to unlabeled embryos a t the desired stage, as described previously (Keller and Tibbetts, 1989). All staging was done according to the staging series of Nieuwkoop and Faber (1967).…”

Section: Methodsmentioning

confidence: 99%

“…Migration and spreading of the mesodermal cells at the leading edge of the mesodermal mantle are severely affected by removal of the blastocoel roof. In absence of their normal substratum, the migratory mesodermal cells are pushed into their normal anterior position by the powerful convergence and extension movements of the axial and paraxial mesoderm behind them, but they do not spread out to form a thin layer on the inner surface of the AC-NIMZ as they do in normal development (Nakatsuji, 1975;Keller, 1976;Keller and Tibbetts, 1989). In contrast, convergence and extension of the mesoderm do not appear to be affected by absence of the NIMZ, other than the bending that occurs in absence of the apparent stiffening effect of its association with the NIMZ .…”

Section: Proper Mesodermal Cell Migration and Guidancementioning

confidence: 99%

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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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“…More often, however, convergence produces thickening as well as lengthening, the proportion of each depending on the speci¢c case (¢gure 1b). For example, the notochordal and somitic mesoderm of the amphibian both converge, extend and thicken, but convergence results in less extension and more thickening in the case of the somitic mesoderm (see Keller et al 1989a;Keller 2000). Thus the collective term `convergent extension' can be used for convenience, but it can be misleading unless one remembers that the relationship between convergence, extension and thickening can be and usually is more complex than this term suggests.…”

Section: Introductionmentioning

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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472

401

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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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Cell intercalation during notochord development in Xenopus laevis

Cited by 132 publications

References 25 publications

Xenopus fibrillin is expressed in the organizer and is the earliest component of matrix at the developing notochord‐somite boundary

Xenopus fibrillin is expressed in the organizer and is the earliest component of matrix at the developing notochord‐somite boundary

Xenopus gastrulation without a blastocoel roof

Mechanisms of convergence and extension by cell intercalation

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