Aurora B functions at the apical surface after specialized cytokinesis during morphogenesis in C. elegans

Bai, Xiaofei; Melesse, Michael; Sorensen Turpin, Christopher G.; Sloan, Dillon E.; Chen, Chin-Yi; Wang, Wen-Cheng; Lee, Po-Yi; Simmons, James R.; Nebenfuehr, Benjamin; Mitchell, Diana; Klebanow, Lindsey R.; Mattson, Nicholas; Betzig, Eric; Chen, Bi-Chang; Cheerambathur, Dhanya; Bembenek, Joshua N.

doi:10.1242/dev.181099

Title: Aurora B functions at the apical surface after specialized cytokinesis during morphogenesis in C. elegans

Journal Article · 07 January 2020 · Development (Cambridge)

DOI: https://doi.org/10.1242/dev.181099 · OSTI ID:1669750

Bai, Xiaofei ^[1];

^[2]; Sorensen Turpin, Christopher G. ^[3];

^[4]; Chen, Chin-Yi ^[5]; Wang, Wen-Cheng ^[5]; Lee, Po-Yi ^[5]; Simmons, James R. ^[3]; Nebenfuehr, Benjamin ^[6];

^[7];

^[8];

^[9]; Betzig, Eric ^[10];

^[11]; Cheerambathur, Dhanya ^[12];

^[4]

University of Tennessee, Knoxville, TN (United States); National Institutes of Health, Bethesda, MD (United States)
University of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
University of Tennessee, Knoxville, TN (United States)
University of Michigan, Ann Arbor, MI (United States); University of Tennessee, Knoxville, TN (United States)
Academia Sinica, Taipei (Taiwan)
University of Tennessee, Knoxville, TN (United States); University of Colorado, Boulder, CO (United States)
University of Michigan, Ann Arbor, MI (United States); University of Idaho, Moscow, ID (United States)
University of Tennessee, Knoxville, TN (United States); Parker Hannifin Corporation, Macedonia, OH (United States)
University of Tennessee, Knoxville, TN (United States); United States Food and Drug Administration, Silver Springs, MD (United States)
HHMI, Ashburn, VA (United States)
HHMI, Ashburn, VA (United States); Academia Sinica, Taipei (Taiwan)
University of Edinburgh (United Kingdom)

Although cytokinesis has been intensely studied, the way it is executed during development is not well understood, despite a long-standing appreciation that various aspects of cytokinesis vary across cell and tissue types. To address this, we investigated cytokinesis during the invariant Caenorhabditis elegans embryonic divisions and found several parameters that are altered at different stages in a reproducible manner. During early divisions, furrow ingression asymmetry and midbody inheritance is consistent, suggesting specific regulation of these events. During morphogenesis, we found several unexpected alterations to cytokinesis, including apical midbody migration in polarizing epithelial cells of the gut, pharynx and sensory neurons. Aurora B kinase, which is essential for several aspects of cytokinesis, remains apically localized in each of these tissues after internalization of midbody ring components. Aurora B inactivation disrupts cytokinesis and causes defects in apical structures, even if inactivated post-mitotically. Therefore, we demonstrate that cytokinesis is implemented in a specialized way during epithelial polarization and that Aurora B has a role in the formation of the apical surface.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1669750

Journal Information:: Development (Cambridge), Journal Name: Development (Cambridge) Journal Issue: 1 Vol. 147; ISSN 0950-1991

Publisher:: Company of BiologistsCopyright Statement

Country of Publication:: United States

Language:: English

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High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes Paix, Alexandre; Folkmann, Andrew; Rasoloson, Dominique Genetics, Vol. 201, Issue 1 https://doi.org/10.1534/genetics.115.179382	journal	July 2015
Endoreplication and polyploidy: insights into development and disease J., Duronio, Robert; T., Fox, Donald The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/4f6c-yh54	text	January 2013
Quantitative Analysis of Cytokinesis In Situ during C. elegans Postembryonic Development S., Maddox, Amy; Benjamin, Lacroix,; F., Dorn, Jonas The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/598d-kh06	text	January 2014
Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination Bob, Goldstein,; D., Ward, Jordan; J., Dickinson, Daniel The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/9bsr-9y51	text	January 2013
MRCK-1 Drives Apical Constriction in C. elegans by Linking Developmental Patterning to Force Generation Bob, Goldstein,; D., Higgins, Christopher; H., Cox, Amanda The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/jxgq-p045	text	January 2016
The C. elegans pharynx: a model for organogenesis Mango, Susan WormBook https://doi.org/10.1895/wormbook.1.129.1	journal	January 2007
Epidermal morphogenesis Hardin, Jeff WormBook https://doi.org/10.1895/wormbook.1.35.1	journal	January 2005
Cell division Oegema, Karen WormBook https://doi.org/10.1895/wormbook.1.72.1	journal	January 2006
C. elegans as a model for membrane traffic Sato, Ken WormBook https://doi.org/10.1895/wormbook.1.77.2	journal	April 2014
The Dawn of Aurora Kinase Research: From Fly Genetics to the Clinic Carmena, Mar; Earnshaw, William C.; Glover, David M. Frontiers in Cell and Developmental Biology, Vol. 3 https://doi.org/10.3389/fcell.2015.00073	journal	November 2015
Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development Haglund, Kaisa; Nezis, Ioannis P.; Stenmark, Harald Communicative & Integrative Biology, Vol. 4, Issue 1 https://doi.org/10.4161/cib.13550	journal	January 2011
Centriolar remodeling underlies basal body maturation during ciliogenesis in Caenorhabditis elegans Nechipurenko, Inna V.; Berciu, Cristina; Sengupta, Piali eLife, Vol. 6 https://doi.org/10.7554/eLife.25686	journal	April 2017
Cell-intrinsic and -extrinsic mechanisms promote cell-type-specific cytokinetic diversity Davies, Tim; Kim, Han X.; Romano Spica, Natalia eLife, Vol. 7 https://doi.org/10.7554/eLife.36204	journal	July 2018
CYK-4 functions independently of its centralspindlin partner ZEN-4 to cellularize oocytes in germline syncytia Lee, Kian-Yong; Green, Rebecca A.; Gutierrez, Edgar eLife, Vol. 7 https://doi.org/10.7554/eLife.36919	journal	July 2018
A multicellular rosette-mediated collective dendrite extension Fan, Li; Kovacevic, Ismar; Heiman, Maxwell G. eLife, Vol. 8 https://doi.org/10.7554/eLife.38065	journal	February 2019
Cell-intrinsic and -extrinsic mechanisms promote cell-type-specific cytokinetic diversity Davies, Tim; Kim, Han X.; Romano Spica, Natalia Columbia University https://doi.org/10.7916/d8vm5w87	text	January 2018

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