A positive role for Short gastrulation in modulating BMP signaling during dorsoventral patterning in the Drosophila embryo

Development. 2001 Oct;128(19):3831-41. doi: 10.1242/dev.128.19.3831.

Abstract

Positional information in the dorsoventral axis of the Drosophila embryo is encoded by a BMP activity gradient formed by synergistic signaling between the BMP family members Decapentaplegic (DPP) and Screw (SCW). short gastrulation (sog), which is functionally homologous to Xenopus Chordin, is expressed in the ventrolateral regions of the embryo and has been shown to act as a local antagonist of BMP signaling. Here we demonstrate that SOG has a second function, which is to promote BMP signaling on the dorsal side of the embryo. We show that a weak, homozygous-viable sog mutant is enhanced to lethality by reduction in the activities of the Smad family members Mad or Medea, and that the lethality is caused by defects in the molecular specification and subsequent cellular differentiation of the dorsal-most cell type, the amnioserosa. While previous data had suggested that the negative function of SOG is directed against SCW, we present data that suggests that the positive activity of SOG is directed towards DPP. We demonstrate that Chordin shares the same apparent ligand specificity as does SOG, preferentially inhibiting SCW but not DPP activity. However, in Drosophila assays Chordin does not have the same capacity to elevate BMP signaling as does SOG, identifying a functional difference in the otherwise well conserved process of dorsoventral pattern formation in arthropods and chordates.

Publication types

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

MeSH terms

  • Animals
  • Body Patterning / physiology*
  • Bone Morphogenetic Proteins / genetics
  • Bone Morphogenetic Proteins / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila / embryology*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Embryo, Nonmammalian / metabolism
  • Female
  • Fetal Death
  • Gastrula
  • Gene Dosage
  • Gene Expression Regulation, Developmental
  • Glycoproteins*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Insect Proteins / genetics
  • Insect Proteins / metabolism*
  • Intercellular Signaling Peptides and Proteins*
  • Male
  • Mutation
  • Proteins / genetics
  • Proteins / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Signal Transduction
  • Smad4 Protein
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors*
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Bone Morphogenetic Proteins
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Glycoproteins
  • Homeodomain Proteins
  • Insect Proteins
  • Intercellular Signaling Peptides and Proteins
  • MAD protein, Drosophila
  • Med protein, Drosophila
  • Proteins
  • Repressor Proteins
  • SCW protein, Drosophila
  • Smad4 Protein
  • TSG protein, Drosophila
  • Trans-Activators
  • Transcription Factors
  • Transforming Growth Factor beta
  • Zen protein, Drosophila
  • dpp protein, Drosophila
  • sog protein, Drosophila
  • chordin