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

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

doi:10.1242/dev.181099

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

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

Research output: Contribution to journal › Article › peer-review

18 Scopus citations

Abstract

Although cytokinesis has been intensely studied, theway 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 alterationsto cytokinesis, including apicalmidbody 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.

Original language	English
Article number	dev181099
Journal	Development (Cambridge)
Volume	147
Issue number	1
DOIs	https://doi.org/10.1242/dev.181099
State	Published - 2020

Funding

Lattice light-sheet microscopy was performed at the Advanced Imaging Center at HHMI Janelia Research Campus, a facility jointly supported by the Gordon and Betty Moore Foundation and the Howard Hughes Medical Institute. CGC and Wormbase provided C. elegans strains and information, funded by the NIH (P40 OD010440) and NHGRI (U41 HG002223). We thank Martha Soto, Julie Ahringer, Arshad Desai, Karen Oegema, Barth Grant, Tony Hyman and Asako Sugimoto for sharing strains and members of the Bembenek laboratory for support. We also thank Dr Max Heiman, Dr Zhirong Bao, Dr Amy Maddox, Dr Pablo Lara-Gonzalez and Sophia Hirsch for discussions, and Dr Don Fox, Dr John White, Dr John Heddleston, Dr Heidi Hehnley-Chang, Lindsay Rathbun and Erica Colicino for manuscript feedback. Funding was provided by the Ministry of Science and Technology, Taiwan (105-2119-M-001-026-MY2 to B.-C.C.), the Howard Hughes Medical Institute (E.B.), the Wellcome Trust (208833 and 203149 to D.C.), and the National Institutes of Health (R01 GM114471 to J.N.B.). Deposited in PMC for immediate release.

Funders	Funder number
National Institutes of Health	P40 OD010440, R01 GM114471
National Institutes of Health
Howard Hughes Medical Institute
National Human Genome Research Institute	U41HG002223
National Human Genome Research Institute
Gordon and Betty Moore Foundation
Wellcome Trust	203149, 208833
Wellcome Trust
Ministry of Science and Technology, Taiwan	105-2119-M-001-026-MY2
Ministry of Science and Technology, Taiwan

Keywords

Apical surface
Aurora B kinase
Cytokinesis
Midbody
Morphogenesis

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10.1242/dev.181099

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Bai, X., Melesse, M., Turpin, C. G. S., Sloan, D. E., Chen, C. Y., Wang, W. C., Lee, P. Y., Simmons, J. R., Nebenfuehr, B., Mitchell, D., Klebanow, L. R., Mattson, N., Betzig, E., Chen, B. C., Cheerambathur, D., & Bembenek, J. N. (2020). Aurora B functions at the apical surface after specialized cytokinesis during morphogenesis in C. elegans. Development (Cambridge), 147(1), Article dev181099. https://doi.org/10.1242/dev.181099

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abstract = "Although cytokinesis has been intensely studied, theway 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 alterationsto cytokinesis, including apicalmidbody 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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author = "Xiaofei Bai and Michael Melesse and Turpin, {Christopher G.Sorensen} and Sloan, {Dillon E.} and Chen, {Chin Yi} and Wang, {Wen Cheng} and Lee, {Po Yi} and Simmons, {James R.} and Benjamin Nebenfuehr and Diana Mitchell and Klebanow, {Lindsey R.} and Nicholas Mattson and Eric Betzig and Chen, {Bi Chang} and Dhanya Cheerambathur and Bembenek, {Joshua N.}",

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Bai, X, Melesse, M, Turpin, CGS, Sloan, DE, Chen, CY, Wang, WC, Lee, PY, Simmons, JR, Nebenfuehr, B, Mitchell, D, Klebanow, LR, Mattson, N, Betzig, E, Chen, BC, Cheerambathur, D & Bembenek, JN 2020, 'Aurora B functions at the apical surface after specialized cytokinesis during morphogenesis in C. elegans', Development (Cambridge), vol. 147, no. 1, dev181099. https://doi.org/10.1242/dev.181099

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AU - Bai, Xiaofei

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AU - Turpin, Christopher G.Sorensen

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AU - Chen, Chin Yi

AU - Wang, Wen Cheng

AU - Lee, Po Yi

AU - Simmons, James R.

AU - Nebenfuehr, Benjamin

AU - Mitchell, Diana

AU - Klebanow, Lindsey R.

AU - Mattson, Nicholas

AU - Betzig, Eric

AU - Chen, Bi Chang

AU - Cheerambathur, Dhanya

AU - Bembenek, Joshua N.

PY - 2020

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N2 - Although cytokinesis has been intensely studied, theway 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 alterationsto cytokinesis, including apicalmidbody 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.

AB - Although cytokinesis has been intensely studied, theway 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 alterationsto cytokinesis, including apicalmidbody 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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ER -

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

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