Cellular mechanism underlying neural convergent extension in Xenopus laevis embryos.
Convergent extension, the simultaneous narrowing and lengthening of a tissue, plays a major role in shaping and patterning the neural ectoderm in vertebrate embryos. In this paper, we characterize the cellular mechanism underlying convergent extension of the neural ectoderm in the Xenopus laevis late gastrula and neurula embryo. Neural ectoderm in X. laevis consists of two components, a superficial layer of epithelial cells overlying deep mesenchymal cells. To investigate the force contribution of the deep cells to convergent extension, we explanted single layers of neural deep cells from late gastrula stage embryos. These "neural deep cell explants" undergo active convergent extension autonomously, implying that these cells contribute force for neural convergent extension in vivo. Using time-lapse videorecording of these explants, we observed the neural deep cell behaviors (previously hidden behind an opaque epithelium) underlying convergent extension. We show that neural deep cells mediolaterally intercalate to form a longer, narrower tissue and that cell shape change and cell division contribute little to their convergent extension. Moreover, we characterize the neural deep cell motility driving mediolateral intercalation, also using time-lapse videorecordings. Analyses of these videos revealed that, on average, neural deep cells exhibit mediolaterally biased protrusive activity which is expressed in an episodic fashion. We propose that neural deep cells accomplish mediolateral intercalation by applying their protrusions upon one another, exerting traction, and pulling themselves between one another. This mechanism is similar to that previously described for convergent extension of the mesodermal cells. However, because the neural deep cells do not mediolaterally elongate during their convergent extension as the mesodermal cells do, we predict that a given intercalation will result in more extension for neural deep cells than for the mesodermal cells. Intercalation of neural cells also likely occurs in a more episodic manner than that of the mesodermal cells because the neural cells' mediolateral protrusive activity is episodic, whereas the protrusive activity of mesodermal cells is more continuous. These differences in protrusive activity and cell shape changes between the neural and mesodermal regions may reflect specializations of the same basic mechanism of mediolateral intercalation, tailored to accommodate other aspects of patterning and development of each tissue. These descriptions of the active cell motility underlying neural convergent extension in X. laevis are the first high-resolution video documentation of protrusive activity during neural convergent extension in any system. Our findings provide an important step in the investigation of neural convergent extension in X. laevis and further our understanding of convergent extension in general.
Elul
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Biophysics Graduate Group, University of California, Berkeley 94720, USA.
Koehl
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MA
Keller
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D000818:Animals; D019521:Body Patterning; D002454:Cell Differentiation; D002455:Cell Division; D002465:Cell Movement; D048429:Cell Size; D002490:Central Nervous System / Q000166:cytology / Q000196:embryology*; D046508:Culture Techniques; D004475:Ectoderm / Q000166:cytology*; D005455:Fluorescent Antibody Technique; D005775:Gastrula / Q000166:cytology; D018715:Microscopy, Video; D009417:Nerve Tissue / Q000166:cytology / Q000196:embryology*; D014982:Xenopus laevis / Q000196:embryology