Literature DB >> 20022244

Epithelial polarity proteins regulate Drosophila tracheal tube size in parallel to the luminal matrix pathway.

Patrick Laprise1, Sarah M Paul, Jim Boulanger, Renée M Robbins, Greg J Beitel, Ulrich Tepass.   

Abstract

Regulation of epithelial tube size is critical for organ function. However, the mechanisms of tube size control remain poorly understood. In the Drosophila trachea, tube dimensions are regulated by a luminal extracellular matrix (ECM). ECM organization requires apical (luminal) secretion of the protein Vermiform (Verm), which depends on the basolateral septate junction (SJ). Here, we show that apical and basolateral epithelial polarity proteins interact to control tracheal tube size independently of the Verm pathway. Mutations in yurt (yrt) and scribble (scrib), which encode SJ-associated polarity proteins, cause an expansion of tracheal tubes but do not disrupt Verm secretion. Reducing activity of the apical polarity protein Crumbs (Crb) suppresses the length defects in yrt but not scrib mutants, suggesting that Yrt acts by negatively regulating Crb. Conversely, Crb overexpression increases tracheal tube dimensions. Reducing crb dosage also rescues tracheal size defects caused by mutations in coracle (cora), which encodes an SJ-associated polarity protein. In addition, crb mutations suppress cora length defects without restoring Verm secretion. Together, these data indicate that Yrt, Cora, Crb, and Scrib operate independently of the Verm pathway. Our data support a model in which Cora and Yrt act through Crb to regulate epithelial tube size. Copyright 2010 Elsevier Ltd. All rights reserved.

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Year:  2010        PMID: 20022244      PMCID: PMC2821987          DOI: 10.1016/j.cub.2009.11.017

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  36 in total

Review 1.  Organization and function of septate junctions: an evolutionary perspective.

Authors:  Swati Banerjee; Aurea D Sousa; Manzoor A Bhat
Journal:  Cell Biochem Biophys       Date:  2006       Impact factor: 2.194

2.  Requirement for chitin biosynthesis in epithelial tube morphogenesis.

Authors:  W Patrick Devine; Barry Lubarsky; Ken Shaw; Stefan Luschnig; Lisa Messina; Mark A Krasnow
Journal:  Proc Natl Acad Sci U S A       Date:  2005-11-15       Impact factor: 11.205

3.  mummy/cystic encodes an enzyme required for chitin and glycan synthesis, involved in trachea, embryonic cuticle and CNS development--analysis of its role in Drosophila tracheal morphogenesis.

Authors:  Sofia J Araújo; Hanna Aslam; Guy Tear; Jordi Casanova
Journal:  Dev Biol       Date:  2005-11-08       Impact factor: 3.582

4.  Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea.

Authors:  Shenqiu Wang; Satish Arcot Jayaram; Johanna Hemphälä; Kirsten-André Senti; Vasilios Tsarouhas; Haining Jin; Christos Samakovlis
Journal:  Curr Biol       Date:  2006-01-24       Impact factor: 10.834

5.  The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size.

Authors:  Patrick Laprise; Slobodan Beronja; Nancy F Silva-Gagliardi; Milena Pellikka; Abbie M Jensen; C Jane McGlade; Ulrich Tepass
Journal:  Dev Cell       Date:  2006-09       Impact factor: 12.270

6.  Mosaic Eyes is a novel component of the Crumbs complex and negatively regulates photoreceptor apical size.

Authors:  Ya-Chu Hsu; John J Willoughby; Arne K Christensen; Abbie M Jensen
Journal:  Development       Date:  2006-11-08       Impact factor: 6.868

7.  serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila.

Authors:  Stefan Luschnig; Tilmann Bätz; Kristina Armbruster; Mark A Krasnow
Journal:  Curr Biol       Date:  2006-01-24       Impact factor: 10.834

Review 8.  The PAR proteins: fundamental players in animal cell polarization.

Authors:  Bob Goldstein; Ian G Macara
Journal:  Dev Cell       Date:  2007-11       Impact factor: 12.270

Review 9.  Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture.

Authors:  Markus Affolter; Emmanuel Caussinus
Journal:  Development       Date:  2008-05-14       Impact factor: 6.868

10.  Drosophila Varicose, a member of a new subgroup of basolateral MAGUKs, is required for septate junctions and tracheal morphogenesis.

Authors:  Victoria M Wu; Marcus H Yu; Raehum Paik; Swati Banerjee; Zhiguo Liang; Sarah M Paul; Manzoor A Bhat; Greg J Beitel
Journal:  Development       Date:  2007-01-31       Impact factor: 6.868

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  41 in total

Review 1.  Comparing peripheral glial cell differentiation in Drosophila and vertebrates.

Authors:  Floriano Rodrigues; Imke Schmidt; Christian Klämbt
Journal:  Cell Mol Life Sci       Date:  2010-09-04       Impact factor: 9.261

2.  Extracellular Mipp1 Activity Confers Migratory Advantage to Epithelial Cells during Collective Migration.

Authors:  Yim Ling Cheng; Deborah J Andrew
Journal:  Cell Rep       Date:  2015-11-25       Impact factor: 9.423

3.  QuBiT: a quantitative tool for analyzing epithelial tubes reveals unexpected patterns of organization in the Drosophila trachea.

Authors:  Ran Yang; Eric Li; Yong-Jae Kwon; Madhav Mani; Greg J Beitel
Journal:  Development       Date:  2019-05-16       Impact factor: 6.868

Review 4.  Tubulogenesis.

Authors:  M Luisa Iruela-Arispe; Greg J Beitel
Journal:  Development       Date:  2013-07       Impact factor: 6.868

5.  Seamless tube shape is constrained by endocytosis-dependent regulation of active Moesin.

Authors:  Jodi Schottenfeld-Roames; Jeffrey B Rosa; Amin S Ghabrial
Journal:  Curr Biol       Date:  2014-07-24       Impact factor: 10.834

Review 6.  The multiple roles of epidermal growth factor repeat O-glycans in animal development.

Authors:  Amanda R Haltom; Hamed Jafar-Nejad
Journal:  Glycobiology       Date:  2015-07-14       Impact factor: 4.313

Review 7.  Development and Function of the Drosophila Tracheal System.

Authors:  Shigeo Hayashi; Takefumi Kondo
Journal:  Genetics       Date:  2018-06       Impact factor: 4.562

8.  Morphogenesis of neurons and glia within an epithelium.

Authors:  Isabel I C Low; Claire R Williams; Megan K Chong; Ian G McLachlan; Bradley M Wierbowski; Irina Kolotuev; Maxwell G Heiman
Journal:  Development       Date:  2019-02-20       Impact factor: 6.868

Review 9.  Apicobasal polarity in the kidney.

Authors:  Marc A Schlüter; Ben Margolis
Journal:  Exp Cell Res       Date:  2012-03-06       Impact factor: 3.905

10.  Crumbs organizes the transport machinery by regulating apical levels of PI(4,5)P2 in Drosophila.

Authors:  Johanna Lattner; Weihua Leng; Elisabeth Knust; Marko Brankatschk; David Flores-Benitez
Journal:  Elife       Date:  2019-11-07       Impact factor: 8.140

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