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Published March 15, 2004 | public
Journal Article

bullwinkle is required for epithelial morphogenesis during Drosophila oogenesis

Abstract

Many organs, such as the liver, neural tube, and lung, form by the precise remodeling of flat epithelial sheets into tubes. Here we investigate epithelial tubulogenesis in Drosophila melanogaster by examining the development of the dorsal respiratory appendages of the eggshell. We employ a culture system that permits confocal analysis of stage 10–14 egg chambers. Time-lapse imaging of GFP-Moesin-expressing egg chambers reveals three phases of morphogenesis: tube formation, anterior extension, and paddle maturation. The dorsal-appendage-forming cells, previously thought to represent a single cell fate, consist of two subpopulations, those forming the tube roof and those forming the tube floor. These two cell types exhibit distinct morphological and molecular features. Roof-forming cells constrict apically and express high levels of Broad protein. Floor cells lack Broad, express the rhomboid-lacZ marker, and form the floor by directed cell elongation. We examine the morphogenetic phenotype of the bullwinkle (bwk) mutant and identify defects in both roof and floor formation. Dorsal appendage formation is an excellent system in which cell biological, molecular, and genetic tools facilitate the study of epithelial morphogenesis.

Additional Information

© 2003 Elsevier Inc. Received for publication 29 July 2003, revised 4 October 2003, accepted 7 October 2003. Thanks to Tadashi Uemura, Hiroki Oda, Greg Guild, and Hannele Ruohola-Baker for antibodies; Tony Ip, Hannele Ruohola-Baker, and Trudi Schu¨pbach for flies; Marianne Bronner-Fraser and Kai Zinn for lab space and encouragement; and Paulette Brunner, Andy Ewald, and Steve Potter for microscopy help. Thanks to Dave Ehlert, Jake Dorman, and Mark Terayama for heroic help creating Figure 1. Thanks to Ellen Ward for sharing unpublished data and, concerning Figure 1, for suggesting that we hire an illustrator who perfected the drawings. Thanks to Dave Tran for the bwk image in Figure 8H and to members of the Berg lab for constructive criticism of this manuscript. This work was supported by National Institutes of Health grant RO1-GM-45248 and National Science Foundation grant IBN-9983207 to C.A.B., the Beckman Institute and N.I.H. grant HD37105 to S.E.F., and N.I.H. grant GM33830 to D.P.K. J.B.D. also was supported by the Molecular and Cellular Biology and A.R.C.S. programs at the University of Washington and a Howard Hughes Medical Institute Predoctoral Fellowship.

Additional details

Created:
August 19, 2023
Modified:
October 17, 2023