Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation

Rozbicki, Emil; Chuai, Manli; Karjalainen, Antti; Song, Feifei; Sang, Helen; Martin, René; Knölker, Hans‐Joachim; MacDonald, Michael P.; Weijer, Cornelis J.

doi:10.1038/ncb3138

Cited by 192 publications

(243 citation statements)

References 68 publications

(78 reference statements)

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“…Therefore, cell intercalation is a direct consequence of local and tissue-scale forces and is a major cause of tissue elongation in the Drosophila germband. MyoII activity has also been shown to be required for intercalation during chicken primitive streak formation (Rozbicki et al, 2015) and mouse renal tube elongation (Lienkamp et al, 2012). Therefore, most intercalation processes mechanistically closely resemble GBE in the Drosophila embryo and use locally produced forces to drive junction and cell-neighbour remodelling.…”

Section: Discussionmentioning

confidence: 99%

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Myosin II is not required forDrosophilatracheal branch elongation and cell intercalation

et al. 2017

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The Drosophila tracheal system consists of an interconnected network of monolayered epithelial tubes that ensures oxygen transport in the larval and adult body. During tracheal dorsal branch (DB) development, individual DBs elongate as a cluster of cells, led by tip cells at the front and trailing cells in the rear. Branch elongation is accompanied by extensive cell intercalation and cell lengthening of the trailing stalk cells. Although cell intercalation is governed by Myosin II (MyoII)-dependent forces during tissue elongation in the Drosophila embryo that lead to germ-band extension, it remained unclear whether MyoII plays a similar active role during tracheal branch elongation and intercalation. Here, we have used a nanobody-based approach to selectively knock down MyoII in tracheal cells. Our data show that, despite the depletion of MyoII function, tip cell migration and stalk cell intercalation (SCI) proceed at a normal rate. This confirms a model in which DB elongation and SCI in the trachea occur as a consequence of tip cell migration, which produces the necessary forces for the branching process. ABSTRACTThe Drosophila tracheal system consists of an interconnected network of monolayered epithelial tubes that ensures oxygen transport in the larval and adult body. During tracheal dorsal branch (DB) development, individual DBs elongate as a cluster of cells, led by tip cells at the front and trailing cells in the rear. Branch elongation is accompanied by extensive cell intercalation and cell lengthening of the trailing stalk cells. Although cell intercalation is governed by Myosin II (MyoII)-dependent forces during tissue elongation in the Drosophila embryo that lead to germ-band extension, it remained unclear whether MyoII plays a similar active role during tracheal branch elongation and intercalation. Here, we have used a nanobodybased approach to selectively knock down MyoII in tracheal cells. Our data show that, despite the depletion of MyoII function, tip cell migration and stalk cell intercalation (SCI) proceed at a normal rate. This confirms a model in which DB elongation and SCI in the trachea occur as a consequence of tip cell migration, which produces the necessary forces for the branching process.

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Section: Discussionmentioning

confidence: 99%

“…1C,D). Furthermore, it has been suggested previously that a loss of MyoII function results in cortical relaxation (Mason et al, 2013;Royou et al, 2002;Rozbicki et al, 2015). We therefore investigated whether knockdown of Sqh-GFP resulted in aberrant cell morphology.…”

Section: Introductionmentioning

confidence: 99%

Myosin II is not required forDrosophilatracheal branch elongation and cell intercalation

et al. 2017

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“…The acquisition of time-lapse images of these embryos requires either the use of a climate-controlled incubator around the whole microscope or a temperature-controlled container with a heated lid to prevent condensation in the light path 14 . However, chick embryos can also develop ex ovo completely submerged in culture medium as filter paper cultures 25 , sandwiched between a layer of heavy mineral oil and albumen in adaptions of New's technique 2,21 , or as folded blastoderm explants in the "Cornish Pasty Culture" 23,26 , without direct contact with the air.…”

Section: Introductionmentioning

confidence: 99%

A Submerged Filter Paper Sandwich for Long-term <em>Ex Ovo</em> Time-lapse Imaging of Early Chick Embryos

Schmitz

Nelemans

Smit

2016

JoVE

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Due to its availability, low cost, flat geometry, and transparency, the ex ovo chick embryo has become a major vertebrate animal model for the study of morphogenetic events, such as gastrulation 2 , neurulation [3][4][5] , somitogenesis 6 , heart bending 7,8 , and brain formation [9][10][11][12][13] , during early embryogenesis. Key to understanding morphogenetic processes is to follow them dynamically by time-lapse imaging. The acquisition of timelapse movies of chick embryogenesis ex ovo has been limited either to short time windows or to the need for an incubator to control temperature and humidity around the embryo 14 . Here, we present a new technique to culture chick embryos ex ovo for high-resolution time-lapse imaging using transmitted light microscopy. The submerged filter paper sandwich is a variant of the well-established filter paper carrier technique (ECculture) 1 and allows for the culturing of chick embryos without the need for a climate chamber. The embryo is sandwiched between two identical filter paper carriers and is kept fully submerged in a simple, temperature-controlled medium covered by a layer of light mineral oil. Starting from the primitive streak stage (Hamburger-Hamilton stage 5, HH5) 15 up to at least the 28-somite stage (HH16) 15, embryos can be cultured with either their ventral or dorsal side up. This allows the acquisition of time-lapse movies covering about 30 hr of embryonic development. Representative time-lapse frames and movies are shown. Embryos are compared morphologically to an embryo cultured in the standard EC-culture.The submerged filter paper sandwich provides a stable environment to study early dorsal and ventral morphogenetic processes. It also allows for live fluorescence imaging and micromanipulations, such as microsurgery, bead implantation, microinjection, gene silencing, and electroporation, and has a strong potential to be combined with immersion objectives for laser-based imaging (including light-sheet microscopy). Video LinkThe video component of this article can be found at

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“…Frequently applied to imaging of zebrafish and fruit flies, it was used to produce their digital embryos and has advanced the understanding of their development. The technique is also suitable to studying the development of higher organisms, as demonstrated on the primitive streak formation of the chick embryo [6]. The primitive streak formation is a part of the gastrulation stage in embryonic development, and initiates the germ layer formation.…”

Section: Imaging In Developmental Biologymentioning

confidence: 99%

“…With this system, the development of chick embryos with a size of several millimetres can be imaged at cellular resolution over long periods of time, with a temporal resolution of about 3 minutes per full time point (complete 3D stack of data). Further details on the basic optical setup and mounting technique can be found elsewhere [6]. Biological samples are often highly scattering, and lightsheet images of chick embryos suffer from noise caused by deflected excitation and emission photons.…”

Section: Digitally Scanned Lightsheet Microscopy and Confocal Scanninmentioning

confidence: 99%

Gaussian vs. Bessel light-sheets: performance analysis in live large sample imaging

Reidt

Correia

Donnachie

et al. 2017

Optical Trapping and Optical Micromanipulation XIV

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Lightsheet fluorescence microscopy (LSFM) has rapidly progressed in the past decade from an emerging technology into an established methodology. This progress has largely been driven by its suitability to developmental biology, where it is able to give excellent spatial-temporal resolution over relatively large fields of view with good contrast and low phototoxicity. In many respects it is superseding confocal microscopy. However, it is no magic bullet and still struggles to image deeply in more highly scattering samples. Many solutions to this challenge have been presented, including, Airy and Bessel illumination, 2-photon operation and deconvolution techniques. In this work, we show a comparison between a simple but effective Gaussian beam illumination and Bessel illumination for imaging in chicken embryos. Whilst Bessel illumination is shown to be of benefit when a greater depth of field is required, it is not possible to see any benefits for imaging into the highly scattering tissue of the chick embryo.

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Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation

Cited by 192 publications

References 68 publications

Myosin II is not required forDrosophilatracheal branch elongation and cell intercalation

Myosin II is not required forDrosophilatracheal branch elongation and cell intercalation

A Submerged Filter Paper Sandwich for Long-term <em>Ex Ovo</em> Time-lapse Imaging of Early Chick Embryos

Gaussian vs. Bessel light-sheets: performance analysis in live large sample imaging

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