Patterned gene expression directs bipolar planar polarity in Drosophila.
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.
Zallen
Jennifer A
JA
Department of Molecular Biology, Princeton University, Lewis Thomas Lab, Washington Road, Princeton, NJ 08544, USA. jzallen@molbio.princeton.edu
Wieschaus
Eric
E
D000818:Animals; D030801:Animals, Genetically Modified; D015703:Antigens, CD; D051186:Armadillo Domain Proteins; D019521:Body Patterning / Q000235:genetics / Q000502:physiology*; D002352:Carrier Proteins / Q000378:metabolism; D015815:Cell Adhesion Molecules / Q000378:metabolism; D002465:Cell Movement; D016764:Cell Polarity / Q000235:genetics / Q000502:physiology*; D004268:DNA-Binding Proteins / Q000378:metabolism; D004330:Drosophila / Q000502:physiology*; D029721:Drosophila Proteins / Q000378:metabolism; D004625:Embryo, Nonmammalian; D004627:Embryonic Induction; D005260:Female; D005786:Gene Expression Regulation / Q000502:physiology*; D017344:Genes, Insect / Q000235:genetics; D006023:Glycoproteins / Q000502:physiology*; D018398:Homeodomain Proteins / Q000378:metabolism; D007136:Immunoglobulins / Q000502:physiology*; D007150:Immunohistochemistry / Q000379:methods; D047908:Intracellular Signaling Peptides and Proteins; D008297:Male; D009154:Mutation; D024462:Myosin Type II / Q000378:metabolism; D009687:Nuclear Proteins; D011956:Receptors, Cell Surface; D000071177:Signaling Lymphocytic Activation Molecule Family Member 1; D015534:Trans-Activators / Q000378:metabolism; D014157:Transcription Factors / Q000378:metabolism
C495305:ARM protein, Drosophila; D015703:Antigens, CD; D051186:Armadillo Domain Proteins; D002352:Carrier Proteins; D015815:Cell Adhesion Molecules; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D006023:Glycoproteins; D018398:Homeodomain Proteins; D007136:Immunoglobulins; D047908:Intracellular Signaling Peptides and Proteins; D009687:Nuclear Proteins; D011956:Receptors, Cell Surface; D015534:Trans-Activators; D014157:Transcription Factors; C400774:baz protein, Drosophila; C052837:eve protein, Drosophila; C080833:run protein, Drosophila; D000071177:Signaling Lymphocytic Activation Molecule Family Member 1; D024462:Myosin Type II