Literature DB >> 32644039

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early Caenorhabditis elegans development.

Lokesh G Pimpale1,2,3, Teije C Middelkoop1,2,3, Alexander Mietke1,4,5,6,7, Stephan W Grill1,2,3.   

Abstract

Proper positioning of cells is essential for many aspects of development. Daughter cell positions can be specified via orienting the cell division axis during cytokinesis. Rotatory actomyosin flows during division have been implied in specifying and reorienting the cell division axis, but how general such reorientation events are, and how they are controlled, remains unclear. We followed the first nine divisions of Caenorhabditis elegans embryo development and demonstrate that chiral counter-rotating flows arise systematically in early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify a mechanism by which chiral counter-rotating actomyosin flows arise in the AB lineage only, and show that they drive lineage-specific spindle skew and cell reorientation events. In conclusion, our work sheds light on the physical processes that underlie chiral morphogenesis in early development.
© 2020, Pimpale et al.

Entities:  

Keywords:  C. elegans; active chiral matter; actomyosin flows; cell lineage; chirality; cytokinesis; developmental biology; physics of living systems; spindle skew

Mesh:

Substances:

Year:  2020        PMID: 32644039      PMCID: PMC7394549          DOI: 10.7554/eLife.54930

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.713


  84 in total

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Authors:  S W Grill; P Gönczy; E H Stelzer; A A Hyman
Journal:  Nature       Date:  2001-02-01       Impact factor: 49.962

2.  Mitotic spindle rotation and mode of cell division in the developing telencephalon.

Authors:  Tarik F Haydar; Eugenius Ang; Pasko Rakic
Journal:  Proc Natl Acad Sci U S A       Date:  2003-02-14       Impact factor: 11.205

3.  Hydrodynamics of cellular cortical flows and the formation of contractile rings.

Authors:  G Salbreux; J Prost; J F Joanny
Journal:  Phys Rev Lett       Date:  2009-07-31       Impact factor: 9.161

4.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans.

Authors:  J E Sulston; H R Horvitz
Journal:  Dev Biol       Date:  1977-03       Impact factor: 3.582

5.  Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis.

Authors:  Christian Pohl; Zhirong Bao
Journal:  Dev Cell       Date:  2010-09-14       Impact factor: 12.270

6.  Sequential functioning of the ECT-2 RhoGEF, RHO-1 and CDC-42 establishes cell polarity in Caenorhabditis elegans embryos.

Authors:  Fumio Motegi; Asako Sugimoto
Journal:  Nat Cell Biol       Date:  2006-08-20       Impact factor: 28.824

7.  Combinatorial Contact Cues Specify Cell Division Orientation by Directing Cortical Myosin Flows.

Authors:  Kenji Sugioka; Bruce Bowerman
Journal:  Dev Cell       Date:  2018-07-19       Impact factor: 12.270

8.  Mitotic Spindle Positioning in the EMS Cell of Caenorhabditis elegans Requires LET-99 and LIN-5/NuMA.

Authors:  Małgorzata J Liro; Lesilee S Rose
Journal:  Genetics       Date:  2016-09-26       Impact factor: 4.562

9.  Formin Is Associated with Left-Right Asymmetry in the Pond Snail and the Frog.

Authors:  Angus Davison; Gary S McDowell; Jennifer M Holden; Harriet F Johnson; Georgios D Koutsovoulos; M Maureen Liu; Paco Hulpiau; Frans Van Roy; Christopher M Wade; Ruby Banerjee; Fengtang Yang; Satoshi Chiba; John W Davey; Daniel J Jackson; Michael Levin; Mark L Blaxter
Journal:  Curr Biol       Date:  2016-02-25       Impact factor: 10.834

10.  PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos.

Authors:  T J Hung; K J Kemphues
Journal:  Development       Date:  1999-01       Impact factor: 6.868

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2.  CYK-1/Formin activation in cortical RhoA signaling centers promotes organismal left-right symmetry breaking.

Authors:  Teije C Middelkoop; Júlia Garcia-Baucells; Porfirio Quintero-Cadena; Lokesh G Pimpale; Shahrzad Yazdi; Paul W Sternberg; Peter Gross; Stephan W Grill
Journal:  Proc Natl Acad Sci U S A       Date:  2021-05-18       Impact factor: 11.205

3.  Establishment of a morphological atlas of the Caenorhabditis elegans embryo using deep-learning-based 4D segmentation.

Authors:  Jianfeng Cao; Guoye Guan; Vincy Wing Sze Ho; Ming-Kin Wong; Lu-Yan Chan; Chao Tang; Zhongying Zhao; Hong Yan
Journal:  Nat Commun       Date:  2020-12-07       Impact factor: 14.919

4.  Computable early Caenorhabditis elegans embryo with a phase field model.

Authors:  Xiangyu Kuang; Guoye Guan; Ming-Kin Wong; Lu-Yan Chan; Zhongying Zhao; Chao Tang; Lei Zhang
Journal:  PLoS Comput Biol       Date:  2022-01-14       Impact factor: 4.475

5.  Septins and a formin have distinct functions in anaphase chiral cortical rotation in the Caenorhabditis elegans zygote.

Authors:  Adhham Zaatri; Jenna A Perry; Amy Shaub Maddox
Journal:  Mol Biol Cell       Date:  2021-05-19       Impact factor: 4.138

6.  spheresDT/Mpacts-PiCS: Cell Tracking and Shape Retrieval in Membrane-labeled Embryos.

Authors:  Wim Thiels; Bart Smeets; Maxim Cuvelier; Francesca Caroti; Rob Jelier
Journal:  Bioinformatics       Date:  2021-07-30       Impact factor: 6.937

  6 in total

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