PIG-1 MELK-dependent phosphorylation of nonmuscle myosin II promotes apoptosis through CES-1 Snail partitioning

PLoS Genet. 2020 Sep 18;16(9):e1008912. doi: 10.1371/journal.pgen.1008912. eCollection 2020 Sep.

Abstract

The mechanism(s) through which mammalian kinase MELK promotes tumorigenesis is not understood. We find that the C. elegans orthologue of MELK, PIG-1, promotes apoptosis by partitioning an anti-apoptotic factor. The C. elegans NSM neuroblast divides to produce a larger cell that differentiates into a neuron and a smaller cell that dies. We find that in this context, PIG-1 MELK is required for partitioning of CES-1 Snail, a transcriptional repressor of the pro-apoptotic gene egl-1 BH3-only. pig-1 MELK is controlled by both a ces-1 Snail- and par-4 LKB1-dependent pathway, and may act through phosphorylation and cortical enrichment of nonmuscle myosin II prior to neuroblast division. We propose that pig-1 MELK-induced local contractility of the actomyosin network plays a conserved role in the acquisition of the apoptotic fate. Our work also uncovers an auto-regulatory loop through which ces-1 Snail controls its own activity through the formation of a gradient of CES-1 Snail protein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actomyosin / metabolism
  • Animals
  • Animals, Genetically Modified
  • Apoptosis / physiology
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Death / physiology
  • Cell Polarity / physiology
  • Cytoskeletal Proteins / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Myosin Type II / metabolism
  • Neural Stem Cells / metabolism
  • Neurons / metabolism
  • Phosphorylation
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Snail Family Transcription Factors / genetics
  • Snail Family Transcription Factors / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • Snail Family Transcription Factors
  • Transcription Factors
  • ces-1 protein, C elegans
  • Actomyosin
  • PIG-1 protein, C elegans
  • Protein Serine-Threonine Kinases
  • Myosin Type II

Grants and funding

This work was supported by LMU Munich (https://www.uni-muenchen.de/index.html), the Deutsche Forschungsgemeinschaft (Center for Integrated Protein Science Munich – CIPSM, DFG EXC 114 to B.C., https://www.dfg.de/en/) and the European Research Council (https://erc.europa.eu/) under the European Union’s Horizon 2020 research and innovation programme (grant agreement 640553 – ACTOMYO to A.X.C.). H.W. was supported by a predoctoral fellowship from the China Scholarship Council (https://www.csc.edu.cn/). A.X.C. has a Principal Investigator position from the Fundação para a Ciência e Tecnologia (https://www.fct.pt/) (CEECIND/01967/2017). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.