TOR complex 1 negatively regulates NDR kinase Cbk1 to control cell separation in budding yeast

PLoS Biol. 2023 Aug 30;21(8):e3002263. doi: 10.1371/journal.pbio.3002263. eCollection 2023 Aug.

Abstract

The target of rapamycin (TOR) signalling pathway plays a key role in the coordination between cellular growth and the cell cycle machinery in eukaryotes. The underlying molecular mechanisms by which TOR might regulate events after anaphase remain unknown. We show for the first time that one of the 2 TOR complexes in budding yeast, TORC1, blocks the separation of cells following cytokinesis by phosphorylation of a member of the NDR (nuclear Dbf2-related) protein-kinase family, the protein Cbk1. We observe that TORC1 alters the phosphorylation pattern of Cbk1 and we identify a residue within Cbk1 activation loop, T574, for which a phosphomimetic substitution makes Cbk1 catalytically inactive and, indeed, reproduces TORC1 control over cell separation. In addition, we identify the exocyst component Sec3 as a key substrate of Cbk1, since Sec3 activates the SNARE complex to promote membrane fusion. TORC1 activity ultimately compromises the interaction between Sec3 and a t-SNARE component. Our data indicate that TORC1 negatively regulates cell separation in budding yeast by participating in Cbk1 phosphorylation, which in turn controls the fusion of secretory vesicles transporting hydrolase at the site of division.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaphase
  • Cell Separation
  • Mechanistic Target of Rapamycin Complex 1
  • Phosphorylation
  • Saccharomycetales*

Substances

  • Mechanistic Target of Rapamycin Complex 1

Grants and funding

The Agencia Estatal de Investigación (AEI) of Ministerio de Ciencia e Innovación (MCIN) funded this work. Grants PID2019-106745GB-I00 funded by MCIN/AEI/10.13039/501100011033 to ASD, PID2019-109027GB-I00 funded by MCIN/AEI/10.13039/501100011033 to EQ. Moreover, ASD acknowledges a grant from the Consejería de Universidades, Investigación, Medio Ambiente y Política Social del Gobierno de Cantabria, and another grant from Sociedad para el Desarrollo de Cantabria (SODERCAN). EQ was funded by Generalitat Valenciana (CIDEGENT2020/41). ML acknowledges research support by grant RTI2018-097801-B-I00 funded by MCIN/AEI/ 10.13039/501100011033 and by “ERDF A way of making Europe” and grant PID2021-122611NB-100 funded by MCIN/AEI/ 10.13039/501100011033 and by “ESF Investing in your future”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.