The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila

Harris, Tony J. C.; Peifer, Mark

doi:10.1083/jcb.200505127

The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila

Journal Article · Mon Aug 29 00:00:00 EDT 2005 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.200505127· OSTI ID:1625135

Harris, Tony J. C. ^[1]; Peifer, Mark ^[2]

Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology; DOE/OSTI
Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biology; Univ. of North Carolina, Chapel Hill, NC (United States). Lineberger Comprehensive Cancer Center

Cell polarity is critical for epithelial structure and function. Adherens junctions (AJs) often direct this polarity, but we previously found that Bazooka (Baz) acts upstream of AJs as epithelial polarity is first established in Drosophila. This prompted us to ask how Baz is positioned and how downstream polarity is elaborated. Surprisingly, we found that Baz localizes to an apical domain below its typical binding partners atypical protein kinase C (aPKC) and partitioning defective (PAR)-6 as the Drosophila epithelium first forms. In fact, Baz positioning is independent of aPKC and PAR-6 relying instead on cytoskeletal cues, including an apical scaffold and dynein-mediated basal-to-apical transport. AJ assembly is closely coupled to Baz positioning, whereas aPKC and PAR-6 are positioned separately. This forms a stratified apical domain with Baz and AJs localizing basal to aPKC and PAR-6, and we identify specific mechanisms that keep these proteins apart. These results reveal key steps in the assembly of the apical domain in Drosophila.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of North Carolina, Chapel Hill, NC (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

OSTI ID:: 1625135

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 5 Vol. 170; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Role for Traf4 in Polarizing Adherens Junctions as a Prerequisite for Efficient Cell Shape Changes Mathew, S. J.; Rembold, M.; Leptin, M. Molecular and Cellular Biology, Vol. 31, Issue 24 https://doi.org/10.1128/mcb.05542-11	journal	October 2011
The PAR proteins: from molecular circuits to dynamic self-stabilizing cell polarity Lang, Charles F.; Munro, Edwin Development, Vol. 144, Issue 19 https://doi.org/10.1242/dev.139063	journal	October 2017
FGF controls epithelial-mesenchymal transitions during gastrulation by regulating cell division and apicobasal polarity Sun, Jingjing; Stathopoulos, Angelike Development https://doi.org/10.1242/dev.161927	journal	January 2018
Scribble and discs-large direct initial assembly and positioning of adherens junctions during establishment of apical-basal polarity Bonello, Teresa T.; Choi, Wangsun; Peifer, Mark Development https://doi.org/10.1242/dev.180976	journal	January 2019
Development and dynamics of cell polarity at a glance Campanale, Joseph P.; Sun, Thomas Y.; Montell, Denise J. Journal of Cell Science, Vol. 130, Issue 7 https://doi.org/10.1242/jcs.188599	journal	April 2017
Shot and Patronin polarise microtubules to direct membrane traffic and biogenesis of microvilli in epithelia Khanal, Ichha; Elbediwy, Ahmed; Diaz de la Loza, Maria del Carmen Journal of Cell Science https://doi.org/10.1242/jcs.189076	journal	January 2016
Dynamics of cortical domains in early Drosophila development Schmidt, Anja; Grosshans, Jörg Journal of Cell Science, Vol. 131, Issue 7 https://doi.org/10.1242/jcs.212795	journal	April 2018
Troponin-I localizes selected apico-basal cell polarity signals Casas-Tintó, Sergio; Ferrús, Alberto Journal of Cell Science https://doi.org/10.1242/jcs.225243	journal	January 2019
An alternative mode of epithelial polarity in the Drosophila midgut Chen, Jia; Sayadian, Aram-Christopher; Lowe, Nick PLOS Biology, Vol. 16, Issue 10 https://doi.org/10.1371/journal.pbio.3000041	journal	October 2018
The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction Mark, Peifer,; J., Harris, Nathan; C., Slep, Kevin The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/ybyp-zs32	text	January 2009
An alternative mode of epithelial polarity in the Drosophila midgut Chen, Jia; Sayadian, Aram-Christopher; Lowe, Nick Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.35892	text	January 2019
Src Cooperates with Oncogenic Ras in Tumourigenesis via the JNK and PI3K Pathways in Drosophila epithelial Tissue Poon, Carole; Brumby, Anthony; Richardson, Helena La Trobe https://doi.org/10.26181/19306097	text	January 2022
The contractile vacuole complex of protists – New cues to function and biogenesis Plattner, Helmut Critical Reviews in Microbiology, Vol. 41, Issue 2 https://doi.org/10.3109/1040841x.2013.821650	journal	July 2013
Src Cooperates with Oncogenic Ras in Tumourigenesis via the JNK and PI3K Pathways in Drosophila epithelial Tissue Poon, Carole; Brumby, Anthony; Richardson, Helena International Journal of Molecular Sciences, Vol. 19, Issue 6 https://doi.org/10.3390/ijms19061585	journal	May 2018
Reconstruction of Par-dependent polarity in apolar cells reveals a dynamic process of cortical polarization Kono, Kalyn; Yoshiura, Shigeki; Fujita, Ikumi eLife, Vol. 8 https://doi.org/10.7554/elife.45559	journal	June 2019

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