Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation

Maureen Cetera, Guillermina R. Ramirez-San Juan, Patrick W. Oakes, Lindsay Lewellyn, Michael J. Fairchild, Guy Tanentzapf, Margaret L. Gardel, Sally Horne-Badovinac

Research output: Contribution to journalArticlepeer-review

117 Scopus citations

Abstract

Tissues use numerous mechanisms to change shape during development. The Drosophila egg chamber is an organ-like structure that elongates to form an elliptical egg. During elongation the follicular epithelial cells undergo a collective migration that causes the egg chamber to rotate within its surrounding basement membrane. Rotation coincides with the formation of a molecular corset, in which actin bundles in the epithelium and fibrils in the basement membrane are all aligned perpendicular to the elongation axis. Here we show that rotation plays a critical role in building the actin-based component of the corset. Rotation begins shortly after egg chamber formation and requires lamellipodial protrusions at each follicle cell s leading edge. During early stages, rotation is necessary for tissue-level actin bundle alignment, but it becomes dispensable after the basement membrane is polarized. This work highlights how collective cell migration can be used to build a polarized tissue organization for organ morphogenesis.

Original languageEnglish (US)
Article number5511
JournalNature communications
Volume5
DOIs
StatePublished - 2014
Externally publishedYes

Bibliographical note

Funding Information:
We thank C. Klämbt, T. Lecuit, B. McCartney, D. Montell, T. Schüpbach, E. Wieschaus and J. Zallen for generously providing reagents, and F. Robin and E. Munro for assistance with near-total internal reflection fluorescence microscopy. We are also grateful to E. Ferguson and members of the Horne-Badovinac lab for insightful comments on the manuscript and to N. Ellis for illustrations. This work was supported by NIH T32 GM007183 to M.C., a NSF Graduate Research Fellowship to G.R.R-SJ., an ACS Postdoctoral Fellowship (PF-12-135-01-CSM) and an award from the AHA to L.L., an NSERC Alexander Graham Bell Canada Graduate Scholarship to M.J.F., a Canadian Institutes of Health Research operating grant (MOP-272122) to G.T., a Burroughs Wellcome Career Award, American Asthma Early Excellence Award and funding from the Packard Foundation to M.L.G., and grants from the Edward Mallinckrodt, Jr Foundation and NIH (R01 GM094276) to S.H.-B.

Publisher Copyright:
© 2014 Macmillan Publishers Limited. All rights reserved.

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