Differential activity of Drosophila Hox genes induces myosin expression and can maintain compartment boundaries

PLoS One. 2013;8(2):e57159. doi: 10.1371/journal.pone.0057159. Epub 2013 Feb 25.

Abstract

Compartments are units of cell lineage that subdivide territories with different developmental potential. In Drosophila, the wing and haltere discs are subdivided into anterior and posterior (A/P) compartments, which require the activity of Hedgehog, and into dorsal and ventral (D/V) compartments, needing Notch signaling. There is enrichment in actomyosin proteins at the compartment boundaries, suggesting a role for these proteins in their maintenance. Compartments also develop in the mouse hindbrain rhombomeres, which are characterized by the expression of different Hox genes, a group of genes specifying different structures along their main axis of bilaterians. We show here that the Drosophila Hox gene Ultrabithorax can maintain the A/P and D/V compartment boundaries when Hedgehog or Notch signaling is compromised, and that the interaction of cells with and without Ultrabithorax expression induces high levels of non-muscle myosin II. In the absence of Ultrabithorax there is occasional mixing of cells from different segments. We also show a similar role in cell segregation for the Abdominal-B Hox gene. Our results suggest that the juxtaposition of cells with different Hox gene expression leads to their sorting out, probably through the accumulation of non-muscle myosin II at the boundary of the different cell territories. The increase in myosin expression seems to be a general mechanism used by Hox genes or signaling pathways to maintain the segregation of different groups of cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / genetics*
  • Gene Expression Regulation / genetics
  • Genes, Homeobox*
  • Myosins / genetics*
  • Myosins / metabolism
  • Signal Transduction

Substances

  • Myosins

Grant support

The work was supported by grants from Ministerio de Ciencia e Innovación (numbers 2004-2OE172, BMC2005-04342 and BFU2008-00632), the Consolider Program (CSD2007-0008) and an institutional grant from the Ramon Areces Foundation. J. R. is supported by a CSIC-JAE fellowship and L. de N. was supported by a FPU fellowship, both from the Spanish Ministerio de Ciencia e Innovación. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.