CYK-4 functions independently of its centralspindlin partner ZEN-4 to cellularize oocytes in germline syncytia

Elife. 2018 Jul 10:7:e36919. doi: 10.7554/eLife.36919.

Abstract

Throughout metazoans, germ cells undergo incomplete cytokinesis to form syncytia connected by intercellular bridges. Gamete formation ultimately requires bridge closure, yet how bridges are reactivated to close is not known. The most conserved bridge component is centralspindlin, a complex of the Rho family GTPase-activating protein (GAP) CYK-4/MgcRacGAP and the microtubule motor ZEN-4/kinesin-6. Here, we show that oocyte production by the syncytial Caenorhabditis elegans germline requires CYK-4 but not ZEN-4, which contrasts with cytokinesis, where both are essential. Longitudinal imaging after conditional inactivation revealed that CYK-4 activity is important for oocyte cellularization, but not for the cytokinesis-like events that generate syncytial compartments. CYK-4's lipid-binding C1 domain and the GTPase-binding interface of its GAP domain were both required to target CYK-4 to intercellular bridges and to cellularize oocytes. These results suggest that the conserved C1-GAP region of CYK-4 constitutes a targeting module required for closure of intercellular bridges in germline syncytia.

Keywords: C. elegans; Kinesin-6; MgcRacGAP; cell biology; centralspindlin; germline syncytia; intercellular bridge; ring canal.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cells, Cultured
  • Cytokinesis
  • GTPase-Activating Proteins / metabolism
  • Germ Cells / cytology*
  • Germ Cells / physiology
  • Giant Cells / cytology*
  • Giant Cells / physiology
  • Kinesins / genetics
  • Kinesins / metabolism*
  • Morphogenesis
  • Oocytes / cytology*
  • Oocytes / physiology
  • Protein Binding
  • Spindle Apparatus / physiology*
  • rho GTP-Binding Proteins / metabolism

Substances

  • CYK-4 protein, C elegans
  • Caenorhabditis elegans Proteins
  • GTPase-Activating Proteins
  • ZEN-4 protein, C elegans
  • Kinesins
  • rho GTP-Binding Proteins