Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry DOI Creative Commons
Ioakeim Ampartzidis, Christoforos Efstathiou, Francesco Paonessa

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: June 16, 2022

Abstract Neuroepithelial cells balance tissue growth requirement with the morphogenetic imperative of closing neural tube. They apically constrict to generate mechanical forces which elevate folds, but are thought dilate during mitosis. However, we previously reported that mitotic neuroepithelial in mouse posterior neuropore have smaller apical surfaces than non-mitotic cells. Here, document progressive enrichment non-muscle myosin-II mitotic, not non-mitotic, areas. Live-imaging chick confirms constriction synchronised mitosis, reaching maximal by anaphase, before division and re-dilation. Mitotic amplitude is significantly greater interphase constrictions. To investigate conservation humans, characterised early stages iPSC differentiation through dual SMAD-inhibition robustly produce pseudostratified neuroepithelia enriched actomyosin. These cultured achieve an equivalent area those embryos. iPSC-derived large areas G2 M phase retain this G1/S. Given method produces anterior identities, studied neuroepithelium elevating mid-brain Instead constricting, larger Tissue geometry differs between convex midbrain flat neuropore. Culturing human on equivalently prevents constriction. Thus, undergo high-amplitude cell cycle progression timing their if influenced geometry.

Language: Английский

Distinct spatiotemporal contribution of morphogenetic events and mechanical tissue coupling during Xenopus neural tube closure DOI Creative Commons
Neophytos Christodoulou, Paris A. Skourides

Development, Journal Year: 2022, Volume and Issue: 149(13)

Published: June 6, 2022

Neural tube closure (NTC) is a fundamental process during vertebrate development and indispensable for the formation of central nervous system. Here, using Xenopus laevis embryos, live imaging, single-cell tracking, optogenetics loss-of-function experiments, we examine roles convergent extension apical constriction, define role surface ectoderm NTC. We show that NTC two-stage with distinct spatiotemporal contributions constriction at each stage. Convergent takes place first stage spatially restricted posterior tissue, whereas occurs second throughout neural plate. also mechanically coupled plate its movement driven by morphogenesis. Finally, an increase in resistive forces detrimental

Language: Английский

Citations

21
Prickle2 regulates apical junction remodeling and tissue fluidity during vertebrate neurulation DOI
Miho Matsuda, Sergei Y. Sokol

The Journal of Cell Biology, Journal Year: 2025, Volume and Issue: 224(4)

Published: Jan. 22, 2025

The process of folding the flat neuroectoderm into an elongated neural tube depends on tissue fluidity, a property that allows epithelial deformation while preserving integrity. Neural also requires planar cell polarity (PCP) pathway. Here, we report Prickle2 (Pk2), core PCP component, increases fluidity by promoting remodeling apical junctions (AJs) in Xenopus embryos. This Pk2 activity is mediated unique evolutionarily conserved Ser/Thr-rich region (STR) carboxyterminal half protein. Mechanistically, effects require Rac1 and are accompanied increased dynamics C-cadherin tricellular junctions, hotspots AJ remodeling. Notably, depletion leads to accumulation mediolaterally oriented cells neuroectoderm, whereas overexpression or Pk1 containing Pk2-derived STR promotes elongation along anteroposterior axis. We propose Pk2-dependent regulation contributes response extrinsic cues.

Language: Английский

Citations

0
Global analysis of cell behavior and protein dynamics reveals region-specific roles for Shroom3 and N-cadherin during neural tube closure DOI Creative Commons
Austin T. Baldwin, Juliana H. Kim, Hyemin Seo

et al.

eLife, Journal Year: 2022, Volume and Issue: 11

Published: March 3, 2022

Failures of neural tube closure are common and serious birth defects, yet we have a poor understanding the interaction genetics cell biology during closure. Additionally, mutations that cause defects (NTDs) tend to affect anterior or posterior regions but rarely both, indicating regional specificity NTD genetics. To better understand behaviors closure, analyzed dynamic localization actin N-cadherin via high-resolution tissue-level time-lapse microscopy Xenopus investigate regionality gene function, generated mosaic in shroom3 , key regulator This new analytical approach elucidates several differences between cranial/anterior spinal/posterior provides mechanistic insight into function shroom3, demonstrates ability imaging analysis generate biological insights

Language: Английский

Citations

14
Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development DOI Creative Commons
Neophytos Christodoulou, Paris A. Skourides

Frontiers in Cell and Developmental Biology, Journal Year: 2023, Volume and Issue: 10

Published: Jan. 9, 2023

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

Language: Английский

Citations

7
The cellular dynamics of neural tube formation DOI Creative Commons
Marise van der Spuy,

Jian Xiong Wang,

Dagmara Kociszewska

et al.

Biochemical Society Transactions, Journal Year: 2023, Volume and Issue: 51(1), P. 343 - 352

Published: Feb. 16, 2023

The vertebrate brain and spinal cord arise from a common precursor, the neural tube, which forms very early during embryonic development. To shape forming changes in cellular architecture must be tightly co-ordinated space time. Live imaging of different animal models has provided valuable insights into dynamics driving tube formation. most well-characterised morphogenetic processes underlying this transformation are convergent extension apical constriction, elongate bend plate. Recent work focused on understanding how these two spatiotemporally integrated tissue- to subcellular scale. Various mechanisms closure have also been visualised, yielding growing movements, junctional remodelling interactions with extracellular matrix promote fusion zippering tube. Additionally, live now revealed mechanical role for apoptosis plate bending, cell intercalation lumen secondary Here, we highlight latest research formation provide some perspectives future.

Language: Английский

Citations

5
The RhoGEF protein Plekhg5 regulates medioapical and junctional actomyosin dynamics of apical constriction during Xenopus gastrulation DOI
Austin T. Baldwin,

Ivan K. Popov,

Ray Keller

et al.

Molecular Biology of the Cell, Journal Year: 2023, Volume and Issue: 34(7)

Published: April 12, 2023

Apical constriction results in apical surface reduction epithelial cells and is a widely used mechanism for morphogenesis. Both medioapical junctional actomyosin remodeling are involved constriction, but the deployment of medial versus their genetic regulation vertebrate embryonic development have not been fully described. In this study, we investigate dynamics by RhoGEF protein Plekhg5 Xenopus bottle cells. Using live imaging quantitative image analysis, show that assume different shapes, with rounding constricting earlier small clusters followed fusiform forming between clusters. signals increase as area decreases, though correlation localization appears to be stronger. F-actin bundles perpendicular form constricted cells, which may correspond microvilli previously observed membrane. Knockdown plekhg5 disrupts activity does affect initial dynamics. Taking together, our study reveals distinct cell morphologies, uncovers behaviors, demonstrates crucial role controlling during gastrulation.

Language: Английский

Citations

4
Mechanical control of neural plate folding by apical domain alteration DOI Creative Commons
Miho Matsuda, Jan Rozman, Sassan Ostvar

et al.

Nature Communications, Journal Year: 2023, Volume and Issue: 14(1)

Published: Dec. 20, 2023

Abstract Vertebrate neural tube closure is associated with complex changes in cell shape and behavior, however, the relative contribution of these processes to tissue folding not well understood. At onset Xenopus folding, we observed alternation apically constricted expanded cells. This apical domain heterogeneity was accompanied by biased orientation along anteroposterior axis, especially at plate hinges, required planar polarity signaling. Vertex models suggested that dispersed isotropically constricting cells can cause elongation adjacent Consistently, ectoderm, cell-autonomous constriction neighbor expansion. Thus, a subset may initiate bending, whereas ‘tug-of-war’ contest between force-generating responding reduces its shrinking body axis. mechanism an alternative anisotropic junctions are perpendicular We propose reflect polarity-dependent mechanical forces operating during folding.

Language: Английский

Citations

4
In vivo high-content imaging and regression analysis reveal non-cell autonomous functions of Shroom3 during neural tube closure DOI Creative Commons
Austin T. Baldwin, Juliana H. Kim, John B. Wallingford

et al.

Developmental Biology, Journal Year: 2022, Volume and Issue: 491, P. 105 - 112

Published: Sept. 13, 2022

Language: Английский

Citations

6
Dilute to Enrich for Deeper Proteomics: A Yolk-Depleted Carrier for Limited Populations of Embryonic (Frog) Cells DOI Open Access
Leena R. Pade, Camille Lombard‐Banek, Jie Li

et al.

Journal of Proteome Research, Journal Year: 2023, Volume and Issue: 23(2), P. 692 - 703

Published: Nov. 23, 2023

Abundant proteins challenge deep mass spectrometry (MS) analysis of the proteome. Yolk, source food in many developing vertebrate embryos, complicates chemical separation and interferes with detection. We report here a strategy that enhances bottom-up proteomics yolk-laden specimens by diluting interferences using yolk-depleted carrier (YODEC) proteome via isobaric multiplexing quantification. This method was tested on embryos South African Clawed Frog (Xenopus laevis), where >90% yolk content challenges proteomics. As proof concept, we isolated neural epidermal fated cell clones from embryo dissection or fluorescence-activated sorting. Compared standard approach, YODEC more than doubled detectable X. laevis proteome, identifying 5,218 D11 dissected embryo. Ca. ∼80% were quantified without dropouts any analytical channels. high-pH fractionation 3,133 ∼8,000 V11 cells sorted ca. 2 (1.5 μg total, 150 ng yolk-free proteome), marking 15-fold improvement coverage vs approach. About 60% these only quantifiable YODEC, including molecular adaptors, transporters, translation, transcription factors. While this study tailored to limited populations Xenopus cells, anticipate approach "dilute enrich" depleted be adaptable other biological models which abundant MS

Language: Английский

Citations

2
Molecular and morphogenetic features of neurulation DOI Creative Commons

N. M. Nevmerzhytska,

O. M. Grabovyi,

L. M. Yaremenko

et al.

Zaporozhye Medical Journal, Journal Year: 2024, Volume and Issue: 26(1), P. 72 - 77

Published: Feb. 5, 2024

Neurulation occurs by two different mechanisms, called primary and secondary neurulation. In humans, neurulation along most of the rostrocaudal axis embryo, while caudally, only in lower sacral coccygeal regions. Primary is responsible for a change neural plate shape, lateral edges which rise then converge at dorsal midline to merge into tube. Initially, tube, formed as result neurulation, open both ends through so-called rostral caudal neuropores. These neuropores connect inner part tube with environment (amniotic cavity) later (by end neurulation) are closed. During brain spinal cord up upper region (up level junction between S1 S2 vertebral bodies), however, this anatomical (sacral-coccygeal division cord, conus medullaris filum terminale) due elongation cavitation cell mass medulla, transforms Thus, main differences that folds invaginates body embryo separates from surface ectoderm, forming an underlying hollow Mesenchymal сlusters form dense undergoes mesenchymal-epithelial transition forms cavities empty during terminal cord. Conclusions. Understanding detailed molecular genetic mechanisms each stage relevant widespread congenital defects, perfect knowledge on aspect all possible factors potential influence it will help develop modern options influencing some them, probably, cause decrease defects.

Language: Английский

Citations

0