Distinct spatiotemporal contribution of morphogenetic events and mechanical tissue coupling during <i>Xenopus</i> neural tube closure

Christodoulou, Neophytos; Skourides, Paris A.

doi:10.1242/dev.200358

Cited by 13 publications

(22 citation statements)

References 62 publications

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“…As expected, unilateral targeted injections of FF-GFP led to thickening of the surface ectoderm. This was accompanied by defects in neural tube closure (Figure 2E), as previously described (Christodoulou and Skourides, 2022). In contrast to the effect on neural plate, SE thickening did not affect somitic mesoderm convergent extension during neural tube closure stages (Figure 2F).…”

Section: Somitic Mesoderm Convergent Extension Is Independent Of Neur...supporting

confidence: 83%

“…We have recently shown that the surface ectoderm is mechanically coupled with the neural plate and its development is permissive for neural tube closure in Xenopus embryos ( Christodoulou and Skourides, 2022 ). Specifically, our recent work revealed that the medial movement of the surface ectoderm during neural tube closure is passive and driven by the remodeling of the neural plate.…”

Section: Resultsmentioning

confidence: 99%

“…Additionally during this stage of development the somitic mesoderm undergoes convergent extension ( Wilson et al, 1989 ) which results in its anteroposterior lengthening, mediolateral thinning and dorsoventral expansion ( Leise and Mueller, 2004 ). At the same time the neural plate lengthens along its anteroposterior axis, thins along the mediolateral axis and bends to form the neural tube ( Christodoulou and Skourides, 2015 ; Christodoulou and Skourides, 2022 ). We hypothesize that in the event that mesodermal morphogenesis is required for neural plate morphogenesis the evolution of tissue shape changes will be temporally linked.…”

Section: Resultsmentioning

confidence: 99%

“…Specifically, 20 ng Vangl2 MO was previously used and validated via immunofluorescence (Darken et al, 2002;Ossipova et al, 2015). Furthermore, this morpholino at this concentration phenocopies convergent extension defects elicited by dominant negative constructs for PCP proteins (Butler and Wallingford, 2018;Christodoulou and Skourides, 2022). The Shroom3 morpholino has been validated previously and successfully phenocopies the phenotypes induced by a Shroom3 dominant negative construct (Haigo et al, 2003;Lee et al, 2007;Chung et al, 2010).…”

Section: Morpholino Oligonucleotidesmentioning

confidence: 99%

“…In addition to neural plate generated forces, it has been suggested that extrinsic forces stemming from the adjacent surface ectoderm and the underlying somitic mesoderm actively contribute to neural tube closure ( Schroeder, 1970 ; Karfunkel, 1974 ; Jacobson and Gordon, 1976 ; Moury and Schoenwolf, 1995 ). Recently, we showed that the surface ectoderm does not actively contribute to neural tube closure, but its proper development is permissive for proper neural plate morphogenesis ( Christodoulou and Skourides, 2022 ). However, the role of somitic mesoderm morphogenesis during neural tube closure is not well defined.…”

Section: Introductionmentioning

confidence: 99%

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Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development

Christodoulou

Skourides

2023

Front. Cell Dev. Biol.

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Neural tube closure is a fundamental process during vertebrate embryogenesis, which leads to the formation of the central nervous system. Defective neural tube closure leads to neural tube defects which are some of the most common human birth defects. While the intrinsic morphogenetic events shaping the neuroepithelium have been studied extensively, how tissues mechanically coupled with the neural plate influence neural tube closure remains poorly understood. Here, using Xenopus laevis embryos, live imaging in combination with loss of function experiments and morphometric analysis of fixed samples we explore the reciprocal mechanical communication between the neural plate and the somitic mesoderm and its impact on tissue morphogenesis. We show that although somitic mesoderm convergent extension occurs independently from neural plate morphogenesis neural tube closure depends on somitic mesoderm morphogenesis. Specifically, impaired somitic mesoderm remodelling results in defective apical constriction within the neuroepithelium and failure of neural tube closure. Last, our data reveal that mild abnormalities in somitic mesoderm and neural plate morphogenesis have a synergistic effect during neurulation, leading to severe neural tube closure defects. Overall, our data reveal that defective morphogenesis of tissues mechanically coupled with the neural plate can not only drastically exacerbate mild neural tube defects that may arise from abnormalities within the neural tissue but can also elicit neural tube defects even when the neural plate is itself free of inherent defects.

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Section: Somitic Mesoderm Convergent Extension Is Independent Of Neur...supporting

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Morpholino Oligonucleotidesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development

Christodoulou

Skourides

2023

Front. Cell Dev. Biol.

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Engineering the Physical Microenvironment into Neural Organoids for Neurogenesis and Neurodevelopment

Li,

Sun,

Hou

et al. 2023

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Understanding the signals from the physical microenvironment is critical for deciphering the processes of neurogenesis and neurodevelopment. The discovery of how surrounding physical signals shape human developing neurons is hindered by the bottleneck of conventional cell culture and animal models. Notwithstanding neural organoids provide a promising platform for recapitulating human neurogenesis and neurodevelopment, building neuronal physical microenvironment that accurately mimics the native neurophysical features is largely ignored in current organoid technologies. Here, it is discussed how the physical microenvironment modulates critical events during the periods of neurogenesis and neurodevelopment, such as neural stem cell fates, neural tube closure, neuronal migration, axonal guidance, optic cup formation, and cortical folding. Although animal models are widely used to investigate the impacts of physical factors on neurodevelopment and neuropathy, the important roles of human stem cell‐derived neural organoids in this field are particularly highlighted. Considering the great promise of human organoids, building neural organoid microenvironments with mechanical forces, electrophysiological microsystems, and light manipulation will help to fully understand the physical cues in neurodevelopmental processes. Neural organoids combined with cutting‐edge techniques, such as advanced atomic force microscopes, microrobots, and structural color biomaterials might promote the development of neural organoid‐based research and neuroscience.

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The surface ectoderm exhibits spatially heterogenous tension that correlates with YAP localisation during spinal neural tube closure in mouse embryos

Marshall¹,

Galea²,

Copp³

et al. 2023

Cells & Development

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Distinct spatiotemporal contribution of morphogenetic events and mechanical tissue coupling during Xenopus neural tube closure

Cited by 13 publications

References 62 publications

Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development

Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development

Engineering the Physical Microenvironment into Neural Organoids for Neurogenesis and Neurodevelopment

The surface ectoderm exhibits spatially heterogenous tension that correlates with YAP localisation during spinal neural tube closure in mouse embryos

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