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Developmental biology - Gene Function

600 Million Year Old Molecular Principles

Embryo genes regulated by mechanical forces...


During embryonic development, gene cascades are a series of chemical reactions that initiate gene activity and cell differentiation. In the journal PNAS, a team of scientists led by Ulrich Technau PhD, in the Department of Molecular Evolution and Development at the University of Vienna, Austria, report that besides gene programming - mechanical cues can also influence the regulation of gene function during development. In fact, comparisons with other animals suggests this regulatory principle is ancient.

It is generally thought embryo development and cellular differentiation in animals and humans follows a very precise genetic program of spatio-temporal, meaning changes that occur in both space and time to gene function. However, a number of recent studies suggest that mechano-transduction, or the ability of cells to transform mechanically forces biochemical signals that also contribute to regulation of gene function and may play an important role in overall development.

While most of these studies were done in cell cultures, Ulrich Technau's team reports how their experiments with mechano-sensitive gene expression in early development of the starlet sea anemone — Nematostella vectensis — reveals a mechano-transduction process.
Chemical inhibition of cellular myosin blocks cell movement in gastrulation - the process where inner and outer cell layers form by invagination. It does this by abolishing a crucial developmental gene — brachyury.

The brachyury gene has a crucial ancient role in regulating development in virtually all animals.

Surprisingly, external mechanical pressure applied to such embryos can restore the expression of brachyury. Furthermore, brachyury operates via mechano-transduction in the sea anemone via ß-catenin, a key protein playing a dual role in cell-to-cell adhesion and gene regulation following a signaling cascade. Based on their findings, the authors propose a feedback loop where mechanical and genetic regulation act together to ensure robust brachyury function.
Because ß-catenin-dependent mechano-transduction occurs in other animals like zebrafish and the fruitfly, it suggests this form of gene regulation dates back at least 600 million years — when an evolutionary split occured between vertebrates, insects and sea anemones.

Signifcance
Besides genetic regulation, mechanical forces have been identified as important cues in numerous developmental processes. Mechanical forces can activate biochemical cascades in a process called mechanotransduction. Recent studies in vertebrates and flies elucidated the role of mechanical forces for mesodermal gene expression. However, it remains unclear whether mechanotransduction is a universal regulatory mechanism throughout Metazoa. Here, we show in the sea anemone Nematostella vectensis that mechanical pressure can ectopically activate or restore brachyury expression. This mechanotransduction is dependent on ß-catenin, similar to vertebrates. We propose that a regulatory feedback loop between genetic and mechanical gene activation exists during gastrulation and the ß-catenin–dependent mechanotransduction is an ancient regulatory mechanism, which was present in the common ancestor of cnidarians and bilaterians.

Abstract
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 down-regulated 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 ß-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 ß-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.

Authors: Ekaterina Pukhlyakova, Andrew J. Aman, Kareem Elsayad, and Ulrich Technau.


Thank you to L. Enquist and the Center for Neuroanatomy with Neurotropic Viruses (CNNV; NIH grant P40RR018604) at Princeton University for providing PRVs; E. Callaway for rabies viruses; A. Joyner, C. Wright, A. Pierani, Y. Nakagawa, L. Sussel, R. Johnson, A. Kania, J. Robbins, and G. Feng for providing mice; J. Martin, N. Serradj, and J. Kalambogias (CUNY School of Medicine) for instruction on ICMS; K. Katayama, F. Imai, P. Thanh, A. Epstein, and M. Sandy (CCHMC) for their technical assistance; M. Masujima (NRIFS) for helping with heatmap analyses; M. Kamoshita, J. Ito (Azabu Univ), X. Sun (CCHMC), and T. Daikoku (Kanazawa University) for help in sperm cryopreservation; T. Yamashita (Osaka University), K. Shibuki, and O. Onodera (Niigata University) for supporting materials; and J. Martin for critical reading of the manuscript. This work was supported by NINDS-NS093002 (Y.Y.); PRESTO (JST; JPMJPR13M8); JSPS KAKENHI 17H04985, 17H05556, and 17K19443; JSPS Postdoctoral Fellowships for Research Abroad; the KANAE Foundation for the Promotion of Medical Science; the Kato Memorial Bioscience Foundation; Grant-in-Aid from the Tokyo Biochemical Research Foundation; the Narishige Neuroscience Research Foundation; and a Japan Heart Foundation Research Grant (M.U.).

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May 24, 2018   Fetal Timeline   Maternal Timeline   News   News Archive




TOP: Highly magnified invagination of embryo inner cell layer of endoderm. Blastopore lip cells show a strong inward deformation. The lower four frames depict single Sea Anemone embryo: C. Embryo in earliest stage of blastopore formation; F. Embryo brachyury ring formation in late gastrula stage; I. Inhibition of myosin blocks gastrulation and stops brachyury ring involuting; L. Treatment with ML-7 rescues embryo which then thrives. Image credit: Copyright, Ulrich Technau.


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