Patterned Gene Expression Directs Bipolar Planar Polarity in Drosophila

Dev Cell. 2004 Mar;6(3):343-55. doi: 10.1016/s1534-5807(04)00060-7.

Abstract

During convergent extension in Drosophila, polarized cell movements cause the germband to narrow along the dorsal-ventral (D-V) axis and more than double in length along the anterior-posterior (A-P) axis. This tissue remodeling requires the correct patterning of gene expression along the A-P axis, perpendicular to the direction of cell movement. Here, we demonstrate that A-P patterning information results in the polarized localization of cortical proteins in intercalating cells. In particular, cell fate differences conferred by striped expression of the even-skipped and runt pair-rule genes are both necessary and sufficient to orient planar polarity. This polarity consists of an enrichment of nonmuscle myosin II at A-P cell borders and Bazooka/PAR-3 protein at the reciprocal D-V cell borders. Moreover, bazooka mutants are defective for germband extension. These results indicate that spatial patterns of gene expression coordinate planar polarity across a multicellular population through the localized distribution of proteins required for cell movement.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Antigens, CD
  • Armadillo Domain Proteins
  • Body Patterning / genetics
  • Body Patterning / physiology*
  • Carrier Proteins / metabolism
  • Cell Adhesion Molecules / metabolism
  • Cell Movement
  • Cell Polarity / genetics
  • Cell Polarity / physiology*
  • DNA-Binding Proteins / metabolism
  • Drosophila / physiology*
  • Drosophila Proteins / metabolism
  • Embryo, Nonmammalian
  • Embryonic Induction
  • Female
  • Gene Expression Regulation / physiology*
  • Genes, Insect / genetics
  • Glycoproteins / physiology*
  • Homeodomain Proteins / metabolism
  • Immunoglobulins / physiology*
  • Immunohistochemistry / methods
  • Intracellular Signaling Peptides and Proteins*
  • Male
  • Mutation
  • Myosin Type II / metabolism
  • Nuclear Proteins
  • Receptors, Cell Surface
  • Signaling Lymphocytic Activation Molecule Family Member 1
  • Trans-Activators / metabolism
  • Transcription Factors / metabolism

Substances

  • ARM protein, Drosophila
  • Antigens, CD
  • Armadillo Domain Proteins
  • Carrier Proteins
  • Cell Adhesion Molecules
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Glycoproteins
  • Homeodomain Proteins
  • Immunoglobulins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Receptors, Cell Surface
  • Trans-Activators
  • Transcription Factors
  • baz protein, Drosophila
  • eve protein, Drosophila
  • run protein, Drosophila
  • Signaling Lymphocytic Activation Molecule Family Member 1
  • Myosin Type II