Socs36E attenuates STAT signaling to optimize motile cell specification in the Drosophila ovary

Dev Biol. 2013 Jul 15;379(2):152-66. doi: 10.1016/j.ydbio.2013.03.022. Epub 2013 Apr 10.

Abstract

The Janus kinase/Signal transducers and activators of transcription (JAK/STAT) pathway determines cell fates by regulating gene expression. One example is the specification of the motile cells called border cells during Drosophila oogenesis. It has been established that too much or too little STAT activity disrupts follicle cell identity and cell motility, which suggests the signaling must be precisely regulated. Here, we find that Suppressor of cytokine signaling at 36E (Socs36E) is a necessary negative regulator of JAK/STAT signaling during border cell specification. We find when STAT signaling is too low to induce migration in the presumptive border cell population, nearby follicle cells uncharacteristically become invasive to enable efficient migration of the cluster. We generated a genetic null allele that reveals Socs36E is required in the anterior follicle cells to limit invasive behavior to an optimal number of cells. We further show Socs36E genetically interacts with the required STAT feedback inhibitor apontic (apt) and APT's downstream target, mir-279, and provide evidence that suggests APT directly regulates Socs36E transcriptionally. Our work shows Socs36E plays a critical role in a genetic circuit that establishes a boundary between the motile border cell cluster and its non-invasive epithelial neighbors through STAT attenuation.

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
  • Cell Differentiation / physiology*
  • Cell Movement / physiology
  • DNA Primers / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology*
  • Electrophoretic Mobility Shift Assay
  • Female
  • Fluorescent Antibody Technique
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology*
  • Ovarian Follicle / cytology
  • Ovarian Follicle / physiology
  • Ovary / cytology
  • Ovary / embryology*
  • STAT Transcription Factors / metabolism*
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Suppressor of Cytokine Signaling Proteins / metabolism*
  • Transcription Factors / metabolism

Substances

  • DNA Primers
  • DNA-Binding Proteins
  • Drosophila Proteins
  • STAT Transcription Factors
  • Socs36E protein, Drosophila
  • Suppressor of Cytokine Signaling Proteins
  • Transcription Factors
  • apt protein, Drosophila