Literature DB >> 26240178

The fission yeast cytokinetic contractile ring regulates septum shape and closure.

Sathish Thiyagarajan1, Emilia Laura Munteanu2, Rajesh Arasada3, Thomas D Pollard4, Ben O'Shaughnessy5.   

Abstract

During cytokinesis, fission yeast and other fungi and bacteria grow a septum that divides the cell in two. In fission yeast closure of the circular septum hole by the β-glucan synthases (Bgs) and other glucan synthases in the plasma membrane is tightly coupled to constriction of an actomyosin contractile ring attached to the membrane. It is unknown how septum growth is coordinated over scales of several microns to maintain septum circularity. Here, we documented the shapes of ingrowing septum edges by measuring the roughness of the edges, a measure of the deviation from circularity. The roughness was small, with spatial correlations indicative of spatially coordinated growth. We hypothesized that Bgs-mediated septum growth is mechanosensitive and coupled to contractile ring tension. A mathematical model showed that ring tension then generates almost circular septum edges by adjusting growth rates in a curvature-dependent fashion. The model reproduced experimental roughness statistics and showed that septum synthesis sets the mean closure rate. Our results suggest that the fission yeast cytokinetic ring tension does not set the constriction rate but regulates septum closure by suppressing roughness produced by inherently stochastic molecular growth processes.
© 2015. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Cell wall growth; Cytokinesis; Mechanosensitivity; Schizosaccharomyces pombe; Septation

Mesh:

Substances:

Year:  2015        PMID: 26240178      PMCID: PMC4610208          DOI: 10.1242/jcs.166926

Source DB:  PubMed          Journal:  J Cell Sci        ISSN: 0021-9533            Impact factor:   5.285


  42 in total

1.  Tension modulates actin filament polymerization mediated by formin and profilin.

Authors:  Naomi Courtemanche; Ja Yil Lee; Thomas D Pollard; Eric C Greene
Journal:  Proc Natl Acad Sci U S A       Date:  2013-05-28       Impact factor: 11.205

2.  A computational approach to edge detection.

Authors:  J Canny
Journal:  IEEE Trans Pattern Anal Mach Intell       Date:  1986-06       Impact factor: 6.226

Review 3.  Comparing contractile apparatus-driven cytokinesis mechanisms across kingdoms.

Authors:  Mohan K Balasubramanian; Ramanujam Srinivasan; Yinyi Huang; Kian-Hong Ng
Journal:  Cytoskeleton (Hoboken)       Date:  2012-10-17

4.  Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe.

Authors:  C Kitayama; A Sugimoto; M Yamamoto
Journal:  J Cell Biol       Date:  1997-06-16       Impact factor: 10.539

5.  Septum pattern in ts mutants of Schizosaccharomyces pombe defective in genes cdc3, cdc4, cdc8 and cdc12.

Authors:  E Streiblová; J Hasek; E Jelke
Journal:  J Cell Sci       Date:  1984-07       Impact factor: 5.285

6.  Sid2p, a spindle pole body kinase that regulates the onset of cytokinesis.

Authors:  C A Sparks; M Morphew; D McCollum
Journal:  J Cell Biol       Date:  1999-08-23       Impact factor: 10.539

7.  The contractile ring coordinates curvature-dependent septum assembly during fission yeast cytokinesis.

Authors:  Zhou Zhou; Emilia Laura Munteanu; Jun He; Tristan Ursell; Mark Bathe; Kerwyn Casey Huang; Fred Chang
Journal:  Mol Biol Cell       Date:  2014-10-29       Impact factor: 4.138

8.  The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring.

Authors:  Rachel H Roberts-Galbraith; Jun-Song Chen; Jianqiu Wang; Kathleen L Gould
Journal:  J Cell Biol       Date:  2009-01-12       Impact factor: 10.539

9.  Model of fission yeast cell shape driven by membrane-bound growth factors and the cytoskeleton.

Authors:  Tyler Drake; Dimitrios Vavylonis
Journal:  PLoS Comput Biol       Date:  2013-10-17       Impact factor: 4.475

10.  Extracellular cell wall β(1,3)glucan is required to couple septation to actomyosin ring contraction.

Authors:  Javier Muñoz; Juan Carlos G Cortés; Matthias Sipiczki; Mariona Ramos; José Angel Clemente-Ramos; M Belén Moreno; Ivone M Martins; Pilar Pérez; Juan Carlos Ribas
Journal:  J Cell Biol       Date:  2013-10-28       Impact factor: 10.539

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  21 in total

Review 1.  Molecular form and function of the cytokinetic ring.

Authors:  MariaSanta C Mangione; Kathleen L Gould
Journal:  J Cell Sci       Date:  2019-06-17       Impact factor: 5.285

Review 2.  Molecular mechanisms of contractile-ring constriction and membrane trafficking in cytokinesis.

Authors:  Kenneth S Gerien; Jian-Qiu Wu
Journal:  Biophys Rev       Date:  2018-11-17

Review 3.  Mechanisms of contractile ring tension production and constriction.

Authors:  Ben O'Shaughnessy; Sathish Thiyagarajan
Journal:  Biophys Rev       Date:  2018-11-19

4.  Fission yeast myosin Myo2 is down-regulated in actin affinity by light chain phosphorylation.

Authors:  Luther W Pollard; Carol S Bookwalter; Qing Tang; Elena B Krementsova; Kathleen M Trybus; Susan Lowey
Journal:  Proc Natl Acad Sci U S A       Date:  2017-08-14       Impact factor: 11.205

Review 5.  Coordinating septum formation and the actomyosin ring during cytokinesis in Schizosaccharomyces pombe.

Authors:  Brian S Hercyk; Udo N Onwubiko; Maitreyi E Das
Journal:  Mol Microbiol       Date:  2019-09-30       Impact factor: 3.501

Review 6.  Beyond force generation: Why is a dynamic ring of FtsZ polymers essential for bacterial cytokinesis?

Authors:  Carla Coltharp; Jie Xiao
Journal:  Bioessays       Date:  2016-11-07       Impact factor: 4.345

Review 7.  Molecular Mechanism of Cytokinesis.

Authors:  Thomas D Pollard; Ben O'Shaughnessy
Journal:  Annu Rev Biochem       Date:  2019-01-16       Impact factor: 23.643

8.  A Cdc42 GEF, Gef1, through endocytosis organizes F-BAR Cdc15 along the actomyosin ring and promotes concentric furrowing.

Authors:  Udo N Onwubiko; Paul J Mlynarczyk; Bin Wei; Julius Habiyaremye; Amanda Clack; Steven M Abel; Maitreyi E Das
Journal:  J Cell Sci       Date:  2019-02-28       Impact factor: 5.285

Review 9.  The Cell Biology of Fission Yeast Septation.

Authors:  Juan C García Cortés; Mariona Ramos; Masako Osumi; Pilar Pérez; Juan Carlos Ribas
Journal:  Microbiol Mol Biol Rev       Date:  2016-07-27       Impact factor: 11.056

Review 10.  The price of independence: cell separation in fission yeast.

Authors:  Rebeca Martín-García; Beatriz Santos
Journal:  World J Microbiol Biotechnol       Date:  2016-03-01       Impact factor: 3.312

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