Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation

Jacobson, Antone G.; Gordon, Richard

doi:10.1002/jez.1401970205

Cited by 281 publications

(175 citation statements)

References 28 publications

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“…In the area studied during gastrulation, mitosis orientations were widely distributed, whereas during nerulation mitoses in the subject were quite strongly aligned with the medio-lateral axis. A number of biological studies have suggested that the long axes of cells (Jacobson and Gordon 1976) are key determinants of mitosis orientation (O'Connell and Wang 2000). Other relevant factors may include cell signalling, biochemical factors, mechanical stresses and tissue deformation (Brodland and Veldhuis 2002;Gong et al 2004;Nelson et al 2005).…”

Section: Results and Conclusionmentioning

confidence: 99%

Detection of mitoses in embryonic epithelia using motion field analysis

Siva¹,

Brodland²,

Clausi³

2009

Computer Methods in Biomechanics and Biomedical Engineering

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Although computer simulations indicate that mitosis may be important to the mechanics of morphogenetic movements, algorithms to identify mitoses in bright field images of embryonic epithelia have not previously been available. Here, the authors present an algorithm that identifies mitoses and their orientations based on the motion field between successive images. Within this motion field, the algorithm seeks 'mitosis motion field prototypes' characterised by convergent motion in one direction and divergent motion in the orthogonal direction, the local motions produced by the division process. The algorithm uses image processing, vector field analyses and pattern recognition to identify occurrences of this prototype and to determine its orientation. When applied to time-lapse images of gastrulation and neurulation-stage amphibian (Ambystoma mexicanum) embryos, the algorithm achieves identification accuracies of 68 and 67%, respectively and angular accuracies of the order of 308, values sufficient to assess the role of mitosis in these developmental processes.

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Section: Results and Conclusionmentioning

confidence: 99%

Detection of mitoses in embryonic epithelia using motion field analysis

Siva¹,

Brodland²,

Clausi³

2009

Computer Methods in Biomechanics and Biomedical Engineering

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“…The source of the forces causing these movements in amphibians remained a mystery until explants of tissue actively converged and extended in culture, mechanically isolated from the rest of the embryo (Schechtman 1942;Holtfreter 1944;Jacobson & Gordon 1976;Keller et al 1985). In 900 R. Keller Comparison of the convergence and extension movements in (a) the whole embryo, and (b) an explant of the dorsal sector of the gastrula.…”

Section: Amphibian Convergent Extension Is An Active Force-producingmentioning

confidence: 99%

“…When put in serial opposition with the mesodermal component by barricades at both ends of the extending explant, the neural region buckles in the face of extension of the mesodermal region, arguing that the neural region is the least sti¡ and thus probably weakest extender of the two. In the embryo, the mesodermal tissues are fastened to the overlying neural plate by a strong attachment of the notochord to the region of the neural plate overlying it, the`notoplate' ( Jacobson & Gordon 1976). These attached neural and mesodermal tissues extend together (A. Edlund and R. Keller, unpublished data;Keller et al 1992a).…”

Section: Amphibian Convergent Extension Is An Active Force-producingmentioning

confidence: 99%

Mechanisms of convergence and extension by cell intercalation

Keller

Davidson

Edlund

et al. 2000

Phil. Trans. R. Soc. Lond. B

467

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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“…We also must understand the cellular basis of the convergence and extension movements because of their fundamental role in shaping the nervous system and the early embryo (Jacobson and Gordon, 1976;Schoenwolf, 1985). Although the pattern and underlying cellular mechanisms of convergence and extension of the DIMZ has been investigated extensively (Keller et al, 1985a,b;Wilson et al, 1989;Wilson and Keller, 1991;Shih and Keller, 1992a,b;Keller et al, 1991a,b), we know little about these aspects of the convergence and extension of the DNIMZ (the prospective neural plate).…”

Section: Iymentioning

confidence: 99%

“…A more general significance of these results is that neural induction is best analyzed and understood in terms of the dynamics of the morphogenetic processes involved. INTRODUCTION Convergence (narrowing around the circumference toward the dorsal side of the embryo) and extension (elongation in the anterior-posterior direction) play fundamental roles in both gastrulation (Schechtman, 1942;Keller, 1986;Warga and Kimmel, 1990) and neurulation of vertebrates (Jacobson and Gordon, 1976;Jacobson, 1981;Schoenwolf, 1985;Schoenwolf and Alvarez, 1989). These movements occur autonomously in explants of amphibian embryos and were thought to be region-specific properties of the marginal zone (Spemann, 1938;Schechtman, 1942;reviewed in Keller, 1986;Keller and Winklbauer, 1992).…”

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confidence: 99%

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

Keller

Shih

Sater

1992

Developmental Dynamics

223

156

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There is great interest in the patterning and morphogenesis of the vertebrate nervous system, but the morphogenetic movements involved in early neural development and their underlying cellular mechanisms are poorly understood. This paper describes the cellular basis of the early neural morphogenesis of Xenopus laeuis. The results have important implications for neural induction. Mapping the fate map of the midneurula (Eagleson and Harris: J. Neurobiol. 21:427440, 1990) back to the early gastrula with time-lapse video recording demonstrates that the prospective hindbrain and spinal cord are initiaUy very wide and very short, and thus at the beginning of gastrulation all their precursor cells lie within a few cell diameters of the inducing mesoderm. In the midgastrula, the prospective hindbrain and spinal cord undergo very strong convergence and extension movements in two phases: In the first phase they primarily undergo thinning in the radial direction and lengthening (extension) in the animal-vegetal direction, and the second phase is characterized primarily by mediolateral narrowing (convergence) and anterior-posterior lengthening (extension). These movements also occur in sandwich explants of the gastrula, thus demonstrating the local automomy of the forces producing them. Tracing cell movements with fluorescein dextran-labeled cells in embryos or explants shows that the initial thinning and extension occurs by radial intercalation of deep cells to form fewer layers of greater area, all of which is expressed as increased length. The subsequent convergence and extension occurs by mediolatera1 intercalation of deep cells to form a longer, narrower array. These results establish that a similar if not identical sequence of radial and mediolateral cell intercalations underlie convergence and extension of the neural and the mesoderm tissues (Wilson and Keller: Development, 112:289-300, 1991). Moreover, these results establish that radial and mediolateral intercalation are the principal neural cell behaviors induced by the planar signals emanating from the dorsal involuting marginal zone (the Spemann organizer) in the early gastrula (Keller et al: Develop. Dynamics, 193: 218-234,1992 cord, thus producing the massive convergence and extension movements that narrow and elongate these regions of the nervous system in the late gastrula. A more general significance of these results is that neural induction is best analyzed and understood in terms of the dynamics of the morphogenetic processes involved.

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Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation

Cited by 281 publications

References 28 publications

Detection of mitoses in embryonic epithelia using motion field analysis

Detection of mitoses in embryonic epithelia using motion field analysis

Mechanisms of convergence and extension by cell intercalation

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

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