The product of the split ends gene is required for the maintenance of positional information during Drosophila development

BMC Dev Biol. 2004 Dec 13;4:15. doi: 10.1186/1471-213X-4-15.

Abstract

Background: The Drosophila split ends (spen) gene encodes a large nuclear protein containing three RNP-type RNA binding motifs, and a conserved transcriptional co-repressor-interacting domain at the C-terminus. Genetic analyses indicate that spen interacts with pathways that regulate the function of Hox proteins, the response to various signaling cascades and cell cycle control. Although spen mutants affect only a small subset of morphological structures in embryos, it has been difficult to find a common theme in spen mutant structural alterations, or in the interactions of spen with known signaling pathways.

Results: By generating clones of spen mutant cells in wing imaginal discs, we show that spen function is required for the correct formation and positioning of veins and mechanosensory bristles both on the anterior wing margin and on the notum, and for the maintenance of planar polarity. Wing vein phenotypic alterations are enhanced by mutations in the crinkled (ck) gene, encoding a non-conventional myosin, and correlate with an abnormal spatial expression of Delta, an early marker of vein formation in third instar wing imaginal discs. Positioning defects were also evident in the organization of the embryonic peripheral nervous system, accompanied by abnormal E-Cadherin expression in the epidermis.

Conclusions: The data presented indicate that the role of spen is necessary to maintain the correct positioning of cells within a pre-specified domain throughout development. Its requirement for epithelial planar polarity, its interaction with ck, and the abnormal E-Cadherin expression associated with spen mutations suggest that spen exerts its function by interacting with basic cellular mechanisms required to maintain multicellular organization in metazoans. This role for spen may explain why mutations in this gene interact with the outcome of multiple signaling pathways.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Body Patterning*
  • Cadherins / metabolism
  • Clone Cells / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development*
  • Drosophila melanogaster / metabolism*
  • Embryo, Nonmammalian / metabolism
  • Epidermis / metabolism
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins / metabolism
  • Mutation / genetics
  • Nerve Tissue Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Peripheral Nervous System / embryology
  • Peripheral Nervous System / metabolism
  • Phenotype
  • RNA-Binding Proteins
  • Signal Transduction
  • Transcription Factors
  • Veins / metabolism
  • Wings, Animal / blood supply
  • Wings, Animal / cytology
  • Wings, Animal / growth & development
  • Wings, Animal / metabolism

Substances

  • Cadherins
  • Drosophila Proteins
  • Homeodomain Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Spen protein, Drosophila
  • Transcription Factors
  • ck protein, Drosophila
  • ct protein, Drosophila
  • delta protein