Myosin II regulatory light chain phosphorylation and formin availability modulate cytokinesis upon changes in carbohydrate metabolism

Abstract

Cytokinesis, the separation of daughter cells at the end of mitosis, relies in animal cells on a contractile actomyosin ring (CAR) composed of actin and class II myosins, whose activity is strongly influenced by regulatory light chain (RLC) phosphorylation. However, in simple eukaryotes such as the fission yeast Schizosaccharomyces pombe, RLC phosphorylation appears dispensable for regulating CAR dynamics. We found that redundant phosphorylation at Ser35 of the S. pombe RLC homolog Rlc1 by the p21-activated kinases Pak1 and Pak2, modulates myosin II Myo2 activity and becomes essential for cytokinesis and cell growth during respiration. Previously, we showed that the stress activated protein kinase pathway (SAPK) MAPK Sty1 controls fission yeast CAR integrity by downregulating formin For3 levels (Gomez-Gil et al.,2020). Here, we report that the reduced availability of formin For3-nucleated actin filaments for the CAR is the main reason for the required control of myosin II contractile activity by RLC phosphorylation during respiration-induced oxidative stress. Thus, the restoration of For3 levels by antioxidants overrides the control of myosin II function regulated by RLC phosphorylation, allowing cytokinesis and cell proliferation during respiration. Therefore, fine-tuned interplay between myosin II function through Rlc1 phosphorylation and environmentally controlled actin filament availability is critical for a successful cytokinesis in response to a switch to a respiratory carbohydrate metabolism.

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Author details

  1. Francisco Prieto-Ruiz

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Elisa Gómez-Gil

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Rebeca Martín-García

    Instituto de Biología Funcional y Genómica, Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Armando Jesus Perez-Diaz

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5494-0087
  5. Jero Vicente-Soler

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8759-6545
  6. Alejandro Franco

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7461-3414
  7. Teresa Soto

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2965-318X
  8. Pilar Pérez

    Instituto de Biología Funcional y Genómica, Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Marisa Madrid

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    marisa@um.es
    Competing interests
    The authors declare that no competing interests exist.
  10. Jose Cansado

    Department of Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    jcansado@um.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2342-8152

Funding

Agencia Estatal de Investigación (PID2020-112569GB-I00)

  • Jose Cansado

Agencia Estatal de Investigación (PGC2018-098924-B-I00)

  • Pilar Pérez

Regional Government of Castile and Leon (CSI150P20)

  • Pilar Pérez

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Prieto-Ruiz et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Francisco Prieto-Ruiz
  2. Elisa Gómez-Gil
  3. Rebeca Martín-García
  4. Armando Jesus Perez-Diaz
  5. Jero Vicente-Soler
  6. Alejandro Franco
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid
  10. Jose Cansado
(2023)
Myosin II regulatory light chain phosphorylation and formin availability modulate cytokinesis upon changes in carbohydrate metabolism
eLife 12:e83285.
https://doi.org/10.7554/eLife.83285

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https://doi.org/10.7554/eLife.83285