Sulfation of eggshell components by Pipe defines dorsal-ventral polarity in the Drosophila embryo.
Drosophila embryonic dorsal-ventral (DV) polarity is controlled by a group of sequentially acting serine proteases located in the fluid-filled perivitelline space between the embryonic membrane and the eggshell, which generate the ligand for the Toll receptor on the ventral side of the embryo. Spatial control of the protease cascade relies on the Pipe sulfotransferase, a fly homolog of vertebrate glycosaminoglycan-modifying enzymes, which is expressed in ventral cells of the follicular epithelium surrounding the developing oocyte. Here we show that the vitelline membrane-like (VML) protein undergoes Pipe-dependent sulfation and, consistent with a role in conveying positional information from the egg chamber to the embryo, becomes incorporated into the eggshell at a position corresponding to the location of the follicle cells from which it was secreted. Although VML influences embryonic DV pattern in a sensitized genetic background, VML is not essential for DV axis formation, suggesting that there is redundancy in the composition of the Pipe enzymatic target. Correspondingly, we find that additional structural components of the vitelline membrane undergo Pipe-dependent sulfation. In identifying the elusive targets of Pipe, this work points to the vitelline membrane as the source of signals that generate the Drosophila DV axis.
Zhang
Zhenyu
Z
Section of Molecular Cell and Developmental Biology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX 78712, USA.
Stevens
Leslie M
LM
Stein
David
D
D000818:Animals; D019521:Body Patterning / Q000502:physiology*; D016764:Cell Polarity / Q000502:physiology*; D004330:Drosophila / Q000196:embryology*; D029721:Drosophila Proteins / Q000378:metabolism*; D004527:Egg Proteins / Q000235:genetics / Q000378:metabolism*; D004591:Electrophoresis, Polyacrylamide Gel; D017403:In Situ Hybridization; D013058:Mass Spectrometry; D009841:Oligonucleotides / Q000235:genetics; D016133:Polymerase Chain Reaction; D015238:Sulfotransferases / Q000378:metabolism*; D014817:Vitelline Membrane / Q000378:metabolism*
D029721:Drosophila Proteins; D004527:Egg Proteins; D009841:Oligonucleotides; C035651:vitelline membrane proteins; D015238:Sulfotransferases; C115847:pip protein, Drosophila