Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning

Abstract

Remodelling its shape, or morphogenesis, is a fundamental property of living tissue. It underlies much of embryonic development and numerous pathologies. Convergent extension (CE) of the axial mesoderm of vertebrates is an intensively studied model for morphogenetic processes that rely on cell rearrangement. It involves the intercalation of polarized cells perpendicular to the antero-posterior (AP) axis, which narrows and lengthens the tissue1,2. Several genes have been identified that regulate cell behaviour underlying CE in zebrafish and Xenopus. Many of these are homologues of genes that control epithelial planar cell polarity in Drosophila1,2,3,4,5. However, elongation of axial mesoderm must be also coordinated with the pattern of AP tissue specification to generate a normal larval morphology. At present, the long-range control that orients CE with respect to embryonic axes is not understood. Here we show that the chordamesoderm of Xenopus possesses an intrinsic AP polarity that is necessary for CE, functions in parallel to Wnt/planar cell polarity signalling, and determines the direction of tissue elongation. The mechanism that establishes AP polarity involves graded activin-like signalling and directly links mesoderm AP patterning to CE.

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Figure 1: AP polarity and chordamesoderm explant elongation.
Figure 2: Activin-induced elongation.
Figure 3: Convergent extension and Wnt/PCP signalling.

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Acknowledgements

We thank the National Hormone & Pituitary Program and A. F. Parlow for recombinant human activin A; F. Watt for MZ15 antibody; P. Hausen for 8C8 antibody; E. M. DeRobertis, R. Harland and J. Smith for plasmids; Y. Masui and the members of the Elinson and Winklbauer laboratories for help and encouragement; and M. Makowiecki for manuscript suggestions. This work was supported by an International Collaborative Grant from the Human Frontier Science Program Organization to R.P.E. and by grants from the Natural Sciences and Engineering Research Council of Canada, the Canadian Institutes of Health Research, and the Canada Foundation for Innovation to R.W.

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Correspondence to Rudolf Winklbauer.

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Includes information on embryological manipulations and immunohistochemistry and in situ hybridization. (DOC 30 kb)

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Ninomiya, H., Elinson, R. & Winklbauer, R. Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 430, 364–367 (2004). https://doi.org/10.1038/nature02620

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