MPK-1 ERK controls membrane organization in C. elegans oogenesis via a sex-determination module

Dev Cell. 2011 May 17;20(5):677-88. doi: 10.1016/j.devcel.2011.04.009.

Abstract

Tissues that generate specialized cell types in a production line must coordinate developmental mechanisms with physiological demand, although how this occurs is largely unknown. In the Caenorhabditis elegans hermaphrodite, the developmental sex-determination cascade specifies gamete sex in the distal germline, while physiological sperm signaling activates MPK-1/ERK in the proximal germline to control plasma membrane biogenesis and organization during oogenesis. We discovered repeated utilization of a self-contained negative regulatory module, consisting of NOS-3 translational repressor, FEM-CUL-2 (E3 ubiquitin ligase), and TRA-1 (Gli transcriptional repressor), which acts both in sex determination and in physiological demand control of oogenesis, coordinating these processes. In the distal germline, where MPK-1 is not activated, TRA-1 represses the male fate as NOS-3 functions in translational repression leading to inactivation of the FEM-CUL-2 ubiquitin ligase. In the proximal germline, sperm-dependent physiological MPK-1 activation results in phosphorylation-based inactivation of NOS-3, FEM-CUL-2-mediated degradation of TRA-1 and the promotion of membrane organization during oogenesis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Membrane / genetics
  • Cell Membrane / metabolism
  • DNA-Binding Proteins / metabolism
  • Germ Cells / metabolism
  • Male
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Sex Determination Analysis / methods*
  • Signal Transduction
  • Spermatozoa / metabolism
  • Transcription Factors / metabolism
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • Nos-3 protein, C elegans
  • Transcription Factors
  • tra-1 protein, C elegans
  • Ubiquitin-Protein Ligases
  • Mitogen-Activated Protein Kinase 1
  • mpk-1 protein, C elegans