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Cell motility driving mediolateral intercalation in explants of Xenopus laevis
Abstract
In Xenopus, convergence and extension are produced by active intercalation of the deep mesodermal cells between one another along the mediolateral axis (medi- olateral cell intercalation), to form a narrower, longer array. The cell motility driving this intercalation is poorly understood. A companion paper shows that the endodermal epithelium organizes the outermost meso- dermal cells immediately beneath it to undergo conver- gence and extension, and other evidence suggests that these deep cells are the most active participants in medi- olateral intercalation (Shih, J. and Keller, R. (1992) Development 116, 887-899). In this paper, we shave off the deeper layers of mesodermal cells, which allows us to observe the protrusive activity of the mesodermal cells next to the organizing epithelium with high reso- lution video microscopy. These mesodermal cells divide in the early gastrula and show rapid, randomly directed protrusive activity. At the early midgastrula stage, they begin to express a characteristic sequence of behaviors, called mediolateral intercalation behavior (MIB): (1) large, stable, filiform and lamelliform protrusions form in the lateral and medial directions, thus making the cells bipolar; (2) these protrusions are applied directly to adjacent cell surfaces and exert traction on them, without contact inhibition; (3) as a result, the cells elongate and align parallel to the mediolateral axis and perpendicular to the axis of extension; (4) the elongate, aligned cells intercalate between one another along the mediolateral axis, thus producing a longer, narrower array. Explants of essentially a single layer of deep mesodermal cells, made at stage 10.5, converge and extend by mediolateral intercalation. Thus by stage 10.5 (early midgastrula), expression of MIB among deep mesodermal cells is physiologically and mechanically independent of the organizing influence of the endoder- mal epithelium, described previously (Shih, J. and Keller, R. (1992) Development 116 887-899), and is the fundamental cell motility underlying mediolateral inter- calation and convergence and extension of the body axis.
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Citations
Cited by
FORMATION AND FUNCTION OF SPEMANN'S ORGANIZER
Harland, R., & Gerhart, J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.611 · Cited by 839
Dishevelled controls cell polarity during Xenopus gastrulation
Wallingford, J. B., Rowning, B. A., Vogeli, K. M., Rothbächer, U., Fraser, S. E., & Harland, R. M. (2000) · Nature · doi:10.1038/35011077 · Cited by 751
Wallingford, J. B., Fraser, S. E., & Harland, R. M. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00197-1 · Cited by 613
Force Generation, Transmission, and Integration during Cell and Tissue Morphogenesis
Lecuit, T., Lenne, P.-F., & Munro, E. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104027 · Cited by 621
Planar cell polarity in development and disease
Butler, M. T., & Wallingford, J. B. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.11 · Cited by 580
Metadata
- Authors
- Shih, J., & Keller, R.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 1992-12-01
- Volume
- 116
- Issue
- 4
- Pages
- 901-914
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2110759931
- Cited by
- 333
- References
- 0
- FWCI
- 3.52
- Type
- journal article
- Language
- en
- Open access
- closed
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- Shih, J., & Keller, R. (1992). Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development. https://doi.org/10.1242/dev.116.4.901
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