Literature DB >> 34739818

Polarized Dishevelled dissolution and reassembly drives embryonic axis specification in sea star oocytes.

S Zachary Swartz1, Tzer Han Tan2, Margherita Perillo3, Nikta Fakhri2, Gary M Wessel3, Athula H Wikramanayake4, Iain M Cheeseman5.   

Abstract

The organismal body axes that are formed during embryogenesis are intimately linked to intrinsic asymmetries established at the cellular scale in oocytes.1 However, the mechanisms that generate cellular asymmetries within the oocyte and then transduce that polarity to organismal scale body axes are poorly understood outside of select model organisms. Here, we report an axis-defining event in meiotic oocytes of the sea star Patiria miniata. Dishevelled (Dvl) is a cytoplasmic Wnt pathway effector required for axis development in diverse species,2-4 but the mechanisms governing its function and distribution remain poorly defined. Using time-lapse imaging, we find that Dvl localizes uniformly to puncta throughout the cell cortex in Prophase I-arrested oocytes but becomes enriched at the vegetal pole following meiotic resumption through a dissolution-reassembly mechanism. This process is driven by an initial disassembly phase of Dvl puncta, followed by selective reformation of Dvl assemblies at the vegetal pole. Rather than being driven by Wnt signaling, this localization behavior is coupled to meiotic cell cycle progression and influenced by Lamp1+ endosome association and Frizzled receptors pre-localized within the oocyte cortex. Our results reveal a cell cycle-linked mechanism by which maternal cellular polarity is transduced to the embryo through spatially regulated Dvl dynamics.
Copyright © 2021 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Dishevelled; Patiria miniata; Wnt; body axis; meiosis; oocyte; polarity; sea star; starfish

Mesh:

Year:  2021        PMID: 34739818      PMCID: PMC8692449          DOI: 10.1016/j.cub.2021.10.022

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  40 in total

1.  An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation.

Authors:  Athula H Wikramanayake; Melanie Hong; Patricia N Lee; Kevin Pang; Christine A Byrum; Joanna M Bince; Ronghui Xu; Mark Q Martindale
Journal:  Nature       Date:  2003-11-27       Impact factor: 49.962

Review 2.  A developmental perspective: changes in the position of the blastopore during bilaterian evolution.

Authors:  Mark Q Martindale; Andreas Hejnol
Journal:  Dev Cell       Date:  2009-08       Impact factor: 12.270

3.  Heads or Tails? Karl Ernst von Baer, Robert Remak, and characterization of the primary axis in animal eggs.

Authors:  Athula H Wikramanayake
Journal:  Mol Reprod Dev       Date:  2013-02       Impact factor: 2.609

Review 4.  Head-to-Tail Polymerization in the Assembly of Biomolecular Condensates.

Authors:  Mariann Bienz
Journal:  Cell       Date:  2020-08-20       Impact factor: 41.582

5.  Establishment of embryonic axes in larvae of the starfish, Asterina pectinifera.

Authors:  T Kominami
Journal:  J Embryol Exp Morphol       Date:  1983-06

6.  The DIX domain targets dishevelled to actin stress fibres and vesicular membranes.

Authors:  Daniel G S Capelluto; Tatiana G Kutateladze; Raymond Habas; Carla V Finkielstein; Xi He; Michael Overduin
Journal:  Nature       Date:  2002-10-17       Impact factor: 49.962

7.  Selective dephosphorylation by PP2A-B55 directs the meiosis I - meiosis II transition in oocytes.

Authors:  S Zachary Swartz; Hieu T Nguyen; Brennan C McEwan; Mark E Adamo; Iain M Cheeseman; Arminja N Kettenbach
Journal:  Elife       Date:  2021-08-03       Impact factor: 8.140

8.  Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation.

Authors:  J R Miller; B A Rowning; C A Larabell; J A Yang-Snyder; R L Bates; R T Moon
Journal:  J Cell Biol       Date:  1999-07-26       Impact factor: 10.539

9.  Secondary structure, 1H, 13C and 15N resonance assignments and molecular interactions of the dishevelled DIX domain.

Authors:  Daniel G S Capelluto; Michael Overduin
Journal:  J Biochem Mol Biol       Date:  2005-03-31

10.  Differential regulation of disheveled in a novel vegetal cortical domain in sea urchin eggs and embryos: implications for the localized activation of canonical Wnt signaling.

Authors:  ChiehFu Jeff Peng; Athula H Wikramanayake
Journal:  PLoS One       Date:  2013-11-13       Impact factor: 3.240

View more
  2 in total

1.  Lineage tracing shows that cell size asymmetries predict the dorsoventral axis in the sea star embryo.

Authors:  Vanessa Barone; Maria Byrne; Deirdre C Lyons
Journal:  BMC Biol       Date:  2022-08-15       Impact factor: 7.364

2.  Live imaging of echinoderm embryos to illuminate evo-devo.

Authors:  Vanessa Barone; Deirdre C Lyons
Journal:  Front Cell Dev Biol       Date:  2022-09-15
  2 in total

北京卡尤迪生物科技股份有限公司 © 2022-2023.