Dynamic imaging of mammalian neural tube closure

Pyrgaki, Christina; Trainor, Paul A.; Hadjantonakis, Anna-Katerina; Niswander, Lee

doi:10.1016/j.ydbio.2010.06.010

Cited by 133 publications

(135 citation statements)

References 29 publications

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“…To enclose the lumen, ECs at the edges of the migrating sheet bend inwards, folding around the luminal space and therefore the blood stream. This morphogenetic process is very similar to the closure of the neural tube (Colas and Schoenwolf, 2001;Pyrgaki et al, 2010), suggesting a conserved role of this mechanism in lumen formation.…”

Section: Discussionmentioning

confidence: 72%

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

et al. 2013

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SUMMARYThe formation and lumenization of blood vessels has been studied in some detail, but there is little understanding of the morphogenetic mechanisms by which endothelial cells (ECs) forming large caliber vessels aggregate, align themselves and finally form a lumen that can support blood flow. Here, we focus on the development of the zebrafish common cardinal veins (CCVs), which collect all the blood from the embryo and transport it back to the heart. We show that the angioblasts that eventually form the definitive CCVs become specified as a separate population distinct from the angioblasts that form the lateral dorsal aortae. The subsequent development of the CCVs represents a novel mechanism of vessel formation, during which the ECs delaminate and align along the inner surface of an existing luminal space. Thereby, the CCVs are initially established as open-ended endothelial tubes, which extend as single EC sheets along the flow routes of the circulating blood and eventually enclose the entire lumen in a process that we term 'lumen ensheathment'. Furthermore, we found that the initial delamination of the ECs as well as the directional migration within the EC sheet depend on Cadherin 5 function. By contrast, EC proliferation within the growing CCV is controlled by Vascular endothelial growth factor C, which is provided by circulating erythrocytes. Our findings not only identify a novel mechanism of vascular lumen formation, but also suggest a new form of developmental crosstalk between hematopoietic and endothelial cell lineages.

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Section: Discussionmentioning

confidence: 72%

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

et al. 2013

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“…This could alter tissue tension or gradients of soluble factors, or suggest a distinct molecular mechanism active in mice. Live-imaging studies of neural tube closure have revealed both zipper-like and button-like mechanisms (Pyrgaki et al, 2010) and might provide insights into mechanisms underlying dorsal aorta fusion. It will be important to use the improved imaging methods established here to further delineate the mechanisms underlying these novel observations.…”

Section: Discussionmentioning

confidence: 99%

“…Previous work by several laboratories, including our own, has shown that mouse embryos can be cultured and imaged using light microscopy at early post-implantation stages prior to the formation of the chorioallantoic placenta, thereby revealing novel dynamic events required for early development (Garcia et al, 2011a;Jones et al, 2002;Kwon et al, 2008;Pyrgaki et al, 2010;Stuckey et al, 2011;Trichas et al, 2012;Udan et al, 2013). As these embryos are very delicate and expand significantly during development, which poses serious complications for lightsheet imaging, we developed a new method for mounting mouse embryos from E6.5-8.5 for multi-angle, light-sheet microscopy to enable long-term imaging of growing embryos at a range of postimplantation stages.…”

Section: Introductionmentioning

confidence: 98%

Quantitative imaging of cell dynamics in mouse embryos using light-sheet microscopy

et al. 2014

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Single/selective-plane illumination, or light-sheet, systems offer several advantages over other fluorescence microscopy methods for live, 3D microscopy. These systems are valuable for studying embryonic development in several animal systems, such as Drosophila, C. elegans and zebrafish. The geometry of the light path in this form of microscopy requires the sample to be accessible from multiple sides and fixed in place so that it can be rotated around a single axis. Popular methods for mounting include hanging the specimen from a pin or embedding it in 1-2% agarose. These methods can be particularly problematic for certain samples, such as postimplantation mouse embryos, that expand significantly in size and are very delicate and sensitive to mounting. To overcome the current limitations and to establish a robust strategy for long-term (24 h) time-lapse imaging of E6.5-8.5 mouse embryos with light-sheet microscopy, we developed and tested a method using hollow agarose cylinders designed to accommodate for embryonic growth, yet provide boundaries to minimize tissue drift and enable imaging in multiple orientations. Here, we report the first 24-h time-lapse sequences of post-implantation mouse embryo development with light-sheet microscopy. We demonstrate that light-sheet imaging can provide both quantitative data for tracking changes in morphogenesis and reveal new insights into mouse embryogenesis. Although we have used this approach for imaging mouse embryos, it can be extended to imaging other types of embryos as well as tissue explants.

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“…Recent advances in mouse embryo ex utero culture techniques have allowed for live imaging of NT closure and hence a more dynamic evaluation of cellular behaviors during this process. In such a study of cranial NT closure, cellular projections were also seen in the gap between the neural folds (Pyrgaki et al, 2010).…”

Section: Histological Studies Of Neural Tube Fusionmentioning

confidence: 99%

Mechanisms of tissue fusion during development

2012

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Tissue fusion events during embryonic development are crucial for the correct formation and function of many organs and tissues, including the heart, neural tube, eyes, face and body wall. During tissue fusion, two opposing tissue components approach one another and integrate to form a continuous tissue; disruption of this process leads to a variety of human birth defects. Genetic studies, together with recent advances in the ability to culture developing tissues, have greatly enriched our knowledge of the mechanisms involved in tissue fusion. This review aims to bring together what is currently known about tissue fusion in several developing mammalian organs and highlights some of the questions that remain to be addressed.

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Dynamic imaging of mammalian neural tube closure

Cited by 133 publications

References 29 publications

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment

Quantitative imaging of cell dynamics in mouse embryos using light-sheet microscopy

Mechanisms of tissue fusion during development

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