Tuned polymerization of the transcription factor Yan limits off-DNA sequestration to confer context-specific repression

Elife. 2018 Nov 9:7:e37545. doi: 10.7554/eLife.37545.

Abstract

During development, transcriptional complexes at enhancers regulate gene expression in complex spatiotemporal patterns. To achieve robust expression without spurious activation, the affinity and specificity of transcription factor-DNA interactions must be precisely balanced. Protein-protein interactions among transcription factors are also critical, yet how their affinities impact enhancer output is not understood. The Drosophila transcription factor Yan provides a well-suited model to address this, as its function depends on the coordinated activities of two independent and essential domains: the DNA-binding ETS domain and the self-associating SAM domain. To explore how protein-protein affinity influences Yan function, we engineered mutants that increase SAM affinity over four orders of magnitude. This produced a dramatic subcellular redistribution of Yan into punctate structures, reduced repressive output and compromised survival. Cell-type specification and genetic interaction defects suggest distinct requirements for polymerization in different regulatory decisions. We conclude that tuned protein-protein interactions enable the dynamic spectrum of complexes that are required for proper regulation.

Keywords: D. melanogaster; ETS repressor; computational biology; developmental biology; eye development; mathematical modeling; photoreceptor; receptor tyrosine kinase signaling; systems biology.

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

  • Alleles
  • Animals
  • Cell Lineage
  • Cell Nucleus / metabolism
  • DNA / metabolism*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / metabolism*
  • Eye Proteins / metabolism*
  • Models, Biological
  • Mutagenesis / genetics
  • Mutation / genetics
  • Photoreceptor Cells, Invertebrate / cytology
  • Photoreceptor Cells, Invertebrate / metabolism
  • Polymerization*
  • Protein Aggregates
  • Protein Binding
  • Repressor Proteins / metabolism*
  • Signal Transduction
  • Transcription Factors / metabolism*
  • Transcription, Genetic

Substances

  • AOP protein, Drosophila
  • Drosophila Proteins
  • Eye Proteins
  • Protein Aggregates
  • Repressor Proteins
  • Transcription Factors
  • DNA