Antagonism versus cooperativity with TALE cofactors at the base of the functional diversification of Hox protein function

PLoS Genet. 2013;9(2):e1003252. doi: 10.1371/journal.pgen.1003252. Epub 2013 Feb 7.

Abstract

Extradenticle (Exd) and Homothorax (Hth) function as positive transcriptional cofactors of Hox proteins, helping them to bind specifically their direct targets. The posterior Hox protein Abdominal-B (Abd-B) does not require Exd/Hth to bind DNA; and, during embryogenesis, Abd-B represses hth and exd transcription. Here we show that this repression is necessary for Abd-B function, as maintained Exd/Hth expression results in transformations similar to those observed in loss-of-function Abd-B mutants. We characterize the cis regulatory module directly regulated by Abd-B in the empty spiracles gene and show that the Exd/Hth complex interferes with Abd-B binding to this enhancer. Our results suggest that this novel Exd/Hth function does not require the complex to bind DNA and may be mediated by direct Exd/Hth binding to the Abd-B homeodomain. Thus, in some instances, the main positive cofactor complex for anterior Hox proteins can act as a negative factor for the posterior Hox protein Abd-B. This antagonistic interaction uncovers an alternative way in which MEIS and PBC cofactors can modulate Abd-B like posterior Hox genes during development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Binding Sites
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / growth & development
  • Embryonic Development / genetics*
  • Gene Expression Regulation, Developmental
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Regulatory Sequences, Nucleic Acid
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Abd-B proteins, Drosophila
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Homeodomain Proteins
  • Transcription Factors
  • exd protein, Drosophila
  • hth protein, Drosophila

Grants and funding

This work was supported by the Programa Consolider, MICINN, European Regional Development Fund (FEDER), and Junta de Andalucía to JC-GH and by an EMBO short-term fellowship to MLR. YG was supported by the CNRS, Université de la Méditerranée, and grants from CEFIPRA, ANR, FRM, and ARC, and by a fellowship from MRT CEFIPRA to NS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.