β-Catenin–dependent mechanotransduction dates back to the common ancestor of Cnidaria and Bilateria

Although the genetic regulation of cellular differentiation processes is well established, recent studies have revealed the role of mechanotransduction on a variety of biological processes, including regulation of gene expression. However, it remains unclear how universal and widespread mechanotrans...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 115; no. 24; pp. 6231 - 6236
Main Authors Pukhlyakova, Ekaterina, Aman, Andrew J., Elsayad, Kareem, Technau, Ulrich
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 12.06.2018
Subjects
Antisense RNA
Bilateria
Biochemistry
Biological activity
Biological Sciences
Cnidaria
CRISPR
Data processing
Differentiation (biology)
Embryogenesis
Embryonic growth stage
Embryos
Fruit flies
Gastrulation
Gene expression
Genetics
Mechanotransduction
Myosin
Nematostella vectensis
Regulatory mechanisms (biology)
Vertebrates
β-Catenin
β-catenin
Nematostella
mechanotransduction
brachyury
gastrulation
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Summary:Although the genetic regulation of cellular differentiation processes is well established, recent studies have revealed the role of mechanotransduction on a variety of biological processes, including regulation of gene expression. However, it remains unclear how universal and widespread mechanotransduction is in embryonic development of animals. Here, we investigate mechanosensitive gene expression during gastrulation of the starlet sea anemone Nematostella vectensis, a cnidarian model organism. We show that the blastoporal marker gene brachyury is downregulated by blocking myosin II-dependent gastrulation movements. Brachyury expression can be restored by applying external mechanical force. Using CRISPR/Cas9 and morpholino antisense technology, we also show that mechanotransduction leading to brachyury expression is β-catenin dependent, similar to recent findings in fish and Drosophila [Brunet T, et al. (2013) Nat Commun 4:1–15]. Finally, we demonstrate that prolonged application of mechanical stress on the embryo leads to ectopic brachyury expression. Thus, our data indicate that β-catenin–dependent mechanotransduction is an ancient gene regulatory mechanism, which was present in the common ancestor of cnidarians and bilaterians, at least 600 million years ago.
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Edited by Richard M. Harland, University of California, Berkeley, CA, and approved April 30, 2018 (received for review August 3, 2017)
Author contributions: E.P., A.J.A., and U.T. designed research; E.P. and A.J.A. performed research; K.E. contributed new reagents/analytic tools; E.P., A.J.A., K.E., and U.T. analyzed data; and E.P., A.J.A., and U.T. wrote the paper.
1Present address: Department of Biology, University of Virginia, Charlottesville, VA 22904.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1713682115