INF2- And FHOD-related Formins Promote Ovulation in the Somatic Gonad of C. Elegans

Cytoskeleton (Hoboken). 2016 Dec;73(12):712-728. doi: 10.1002/cm.21341. Epub 2016 Nov 9.

Abstract

Formins are regulators of actin filament dynamics. We demonstrate here that two formins, FHOD-1 and EXC-6, are important in the nematode Caenorhabditis elegans for ovulation, during which actomyosin contractions push a maturing oocyte from the gonad arm into a distensible bag-like organ, the spermatheca. EXC-6, a homolog of the disease-associated mammalian formin INF2, is highly expressed in the spermatheca, where it localizes to cell-cell junctions and to circumferential actin filament bundles. Loss of EXC-6 does not noticeably affect the organization the actin filament bundles, and causes only a very modest increase in the population of junction-associated actin filaments. Despite absence of a strong cytoskeletal phenotype, approximately half of ovulations in exc-6 mutants exhibit extreme defects, including failure of the oocyte to enter the spermatheca, or breakage of the oocyte as the distal spermatheca entrance constricts during ovulation. Loss of FHOD-1 alone has little effect, and we cannot detect FHOD-1 in the spermatheca. However, combined loss of these formins in double fhod-1;exc-6 mutants results in profound ovulation defects, with significant slowing of the entry of oocytes into the spermatheca, and failure of nearly 80% of ovulations. We suggest that EXC-6 plays a role directly in the spermatheca, perhaps by modulating the ability of the spermatheca wall to rapidly accommodate an incoming oocyte, while FHOD-1 may play an indirect role relating to its known importance in the growth and function of the egg-laying muscles. © 2016 The Authors. Cytoskeleton Published by Wiley Periodicals, Inc.

Keywords: EXC-6; FHOD-1; actin; cell-cell junctions; reproductive defects; spermatheca.

MeSH terms

  • Actin Cytoskeleton / immunology
  • Actin Cytoskeleton / metabolism*
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Female
  • Formins
  • Male
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Oocytes / metabolism*
  • Ovulation / genetics
  • Ovulation / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • EXC-6 protein, C elegans
  • Formins
  • Microfilament Proteins
  • fhod-1 proteins, C elegans