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      aura ( mid1ip1l) regulates the cytoskeleton at the zebrafish egg-to-embryo transition

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          ABSTRACT

          Embryos from females homozygous for a recessive maternal-effect mutation in the gene aura exhibit defects including reduced cortical integrity, defective cortical granule (CG) release upon egg activation, failure to complete cytokinesis, and abnormal cell wound healing. We show that the cytokinesis defects are associated with aberrant cytoskeletal reorganization during furrow maturation, including abnormal F-actin enrichment and microtubule reorganization. Cortical F-actin prior to furrow formation fails to exhibit a normal transition into F-actin-rich arcs, and drug inhibition is consistent with aura function promoting F-actin polymerization and/or stabilization. In mutants, components of exocytic and endocytic vesicles, such as Vamp2, Clathrin and Dynamin, are sequestered in unreleased CGs, indicating a need for CG recycling in the normal redistribution of these factors. However, the exocytic targeting factor Rab11 is recruited to the furrow plane normally at the tip of bundling microtubules, suggesting an alternative anchoring mechanism independent of membrane recycling. A positional cloning approach indicates that the mutation in aura is associated with a truncation of Mid1 interacting protein 1 like (Mid1ip1l), previously identified as an interactor of the X-linked Opitz G/BBB syndrome gene product Mid1. A Cas9/CRISPR-induced mutant allele in mid1ip1l fails to complement the originally isolated aura maternal-effect mutation, confirming gene assignment. Mid1ip1l protein localizes to cortical F-actin aggregates, consistent with a direct role in cytoskeletal regulation. Our studies indicate that maternally provided aura ( mid1ip1l) acts during the reorganization of the cytoskeleton at the egg-to-embryo transition and highlight the importance of cytoskeletal dynamics and membrane recycling during this developmental period.

          Abstract

          Summary: The zebrafish maternal-effect gene aura encodes Mid1ip1l, which is involved in cytoskeletal rearrangements during the egg-to-embryo transition.

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          Author and article information

          Journal
          Development
          Development
          DEV
          develop
          Development (Cambridge, England)
          The Company of Biologists Ltd
          0950-1991
          1477-9129
          1 May 2016
          1 May 2017
          : 143
          : 9
          : 1585-1599
          Affiliations
          Laboratory of Genetics, University of Wisconsin – Madison , 425-G Henry Mall, Room 2455 Genetics, Madison, WI 53706, USA
          Author notes
          [* ]Author for correspondence ( fjpelegri@ 123456wisc.edu )
          Article
          PMC4986165 PMC4986165 4986165 DEV130591
          10.1242/dev.130591
          4986165
          26965374
          20539822-00a8-4815-8094-179bf800250d
          © 2016. Published by The Company of Biologists Ltd
          History
          : 9 September 2015
          : 1 March 2016
          Funding
          Funded by: National Institutes of Health, http://dx.doi.org/10.13039/100000002;
          Award ID: GM065303
          Award ID: GM108449
          Categories
          Research Article

          Opitz G/BBB syndrome,Mid1,Mid1ip1l,Cytoskeleton,Cortical granules,Membrane exocytosis,Cytokinesis,F-actin,Zebrafish

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