Optogenetic control of morphogenesis goes 3D

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Abstract

The generation of form in living embryos, a process termed “morphogenesis” from the Greek word μορφογένεση, is one of the most fascinating unsolved problems in biology. In embryonic epithelia, most attention has been paid to events occurring at the apical surface of epithelia, particularly the regulation of actomyosin contractility during morphogenetic change. In a new report, De Renzis and colleagues demonstrate a key role for regulated actomyosin contractility at the basal surface of the epithelium during formation of the first epithelial fold in Drosophila (the “ventral furrow”) (Krueger et al, 2018).

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Most cited references 11

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Global tissue revolutions in a morphogenetic movement controlling elongation.

Saori L. Haigo, David Bilder (2011)

Polarized cell behaviors drive axis elongation in animal embryos, but the mechanisms underlying elongation of many tissues remain unknown. Eggs of Drosophila undergo elongation from a sphere to an ellipsoid during oogenesis. We used live imaging of follicles (developing eggs) to elucidate the cellular basis of egg elongation. We find that elongating follicles undergo repeated rounds of circumferential rotation around their long axes. Follicle epithelia mutant for integrin or collagen IV fail to rotate and elongate, which results in round eggs. We present evidence that polarized rotation is required to build a polarized, fibrillar extracellular matrix (ECM) that constrains tissue shape. Thus, global tissue rotation is a morphogenetic behavior that uses planar polarity information in the ECM to control tissue elongation.

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Tissue elongation requires oscillating contractions of a basal actomyosin network

Li-Li He, Xiaobo Wang, Ho Lam Tang … (2010)

Understanding how molecular dynamics lead to cellular behaviors that ultimately sculpt organs and tissues is a major challenge not only in basic developmental biology but also in tissue engineering and regenerative medicine. Here we use live imaging to show that the basal surfaces of Drosophila follicle cells undergo a series of directional, oscillating contractions driven by periodic myosin accumulation on a polarized actin network. Inhibition of the actomyosin contractions or their coupling to extracellular matrix (ECM) blocked elongation of the whole tissue, whereas enhancement of the contractions exaggerated it. Myosin accumulated in a periodic manner prior to each contraction and was regulated by the small GTPase Rho, its downstream kinase ROCK and cytosolic calcium. Disrupting the link between the actin cytoskeleton and the ECM decreased, while enhancing cell-ECM adhesion increased, the amplitude and period of the contractions. In contrast, disrupting cell-cell adhesions resulted in loss of the actin network. Our findings reveal a novel mechanism controlling organ shape and a new model for the study of the effects of oscillatory actomyosin activity within a coherent cell sheet.

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Cell shape changes during gastrulation in Drosophila.

B Grünewald, M Leptin (1990)

The first morphogenetic movement during Drosophila development is the invagination of the mesoderm, an event that folds a one-layered epithelium into a multilayered structure. In this paper, we describe the shape changes and behaviour of the cells participating in this process and show how mutations that change cell fate affect this behaviour. We divide the formation of the mesodermal germ layer into two phases. During the first phase, the ventral epithelium folds into a tube by a series of concerted cell shape changes (ventral furrow formation). Based on the behaviour of cells in this phase, we conclude that the prospective mesoderm is not a homogeneous cell population, but consists of two subpopulations. Each subpopulation goes through a distinctive sequence of specific cell shape changes which together mediate the invagination of the ventral furrow. In the second phase, the invaginated tube of mesoderm loses its epithelial character, the mesoderm cells disperse, divide and then spread out along the ectoderm to form a single cell layer. To test how ventral furrow formation depends on cell fates in the mesoderm and in neighbouring cells we alter these fates genetically using maternal and zygotic mutations. These experiments show that some of the aspects of cell behaviour specific for ventral furrow cells are part of an autonomous differentiation programme. The force driving the invagination is generated within the region of the ventral furrow, with the lateral and dorsal cell populations contributing little or none of the force. Two known zygotic genes that are required for the formation of the mesoderm, twist and snail, are expressed in ventral furrow cells, and the correct execution of cell shape changes in the mesoderm depends on both. Finally, we show that the region where the ventral furrow forms is determined by the expression of mesoderm-specific genes, and not by mechanical or other epigenetic properties of the egg.

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Contributors

Barry James Thompson:

ORCID: http://orcid.org/0000-0002-0103-040X

barry.thompson@crick.ac.uk

Journal

Journal ID (nlm-ta): EMBO J

Journal ID (iso-abbrev): EMBO J

Journal ID (doi): 10.1002/(ISSN)1460-2075

Journal ID (publisher-id): EMBJ

Journal ID (hwp): embojnl

Title: The EMBO Journal

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 0261-4189

ISSN (Electronic): 1460-2075

Publication date (Electronic): 22 November 2018

Publication date (Print): 03 December 2018

Publication date PMC-release: 22 November 2018

Volume: 37

Issue: 23 ( doiID: 10.1002/embj.v37.23 )

Electronic Location Identifier: e100961

Affiliations

[ ¹ ] Cancer Research UK London UK

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Barry James Thompson http://orcid.org/0000-0002-0103-040X

Article

Publisher ID: EMBJ2018100961

DOI: 10.15252/embj.2018100961

PMC ID: 6276872

PubMed ID: 30467222

SO-VID: 891f8499-26a8-4b94-8f93-4f53fd936650

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This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Figures: 0, Tables: 0, Pages: 2, Words: 1002

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source-schema-version-number 2.0

component-id embj2018100961

cover-date 03 December 2018

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.3 mode:remove_FC converted:03.12.2018

ScienceOpen disciplines: Molecular biology

Keywords: cell adhesion, polarity & cytoskeleton,development & differentiation

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ScienceOpen disciplines: Molecular biology

Keywords: cell adhesion, polarity & cytoskeleton, development & differentiation

Optogenetic control of morphogenesis goes 3D

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Abstract

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Higher order chromatin architecture

Most cited references 11

Global tissue revolutions in a morphogenetic movement controlling elongation.

Tissue elongation requires oscillating contractions of a basal actomyosin network

Cell shape changes during gastrulation in Drosophila.

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