Literature DB >> 21750259

A novel function for the PAR complex in subcellular morphogenesis of tracheal terminal cells in Drosophila melanogaster.

Tiffani A Jones1, Mark M Metzstein.   

Abstract

The processes that generate cellular morphology are not well understood. To investigate this problem, we use Drosophila melanogaster tracheal terminal cells, which undergo two distinct morphogenetic processes: subcellular branching morphogenesis and subcellular apical lumen formation. Here we show these processes are regulated by components of the PAR-polarity complex. This complex, composed of the proteins Par-6, Bazooka (Par-3), aPKC, and Cdc42, is best known for roles in asymmetric cell division and apical/basal polarity. We find Par-6, Bazooka, and aPKC, as well as known interactions between them, are required for subcellular branch initiation, but not for branch outgrowth. By analysis of single and double mutants, and isolation of two novel alleles of Par-6, one of which specifically truncates the Par-6 PDZ domain, we conclude that dynamic interactions between apical PAR-complex members control the branching pattern of terminal cells. These data suggest that canonical apical PAR-complex activity is required for subcellular branching morphogenesis. In addition, we find the PAR proteins are downstream of the FGF pathway that controls terminal cell branching. In contrast, we find that while Par-6 and aPKC are both required for subcellular lumen formation, neither Bazooka nor a direct interaction between Par-6 and aPKC is needed for this process. Thus a novel, noncanonical role for the polarity proteins Par-6 and aPKC is used in formation of this subcellular apical compartment. Our results demonstrate that proteins from the PAR complex can be deployed independently within a single cell to control two different morphogenetic processes.

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Year:  2011        PMID: 21750259      PMCID: PMC3176136          DOI: 10.1534/genetics.111.130351

Source DB:  PubMed          Journal:  Genetics        ISSN: 0016-6731            Impact factor:   4.562


  52 in total

1.  DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila.

Authors:  M Petronczki; J A Knoblich
Journal:  Nat Cell Biol       Date:  2001-01       Impact factor: 28.824

2.  PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex.

Authors:  T Yamanaka; Y Horikoshi; A Suzuki; Y Sugiyama; K Kitamura; R Maniwa; Y Nagai; A Yamashita; T Hirose; H Ishikawa; S Ohno
Journal:  Genes Cells       Date:  2001-08       Impact factor: 1.891

Review 3.  Dendritic cells: a specialized complex system of antigen presenting cells.

Authors:  Levi H C Makala; Hideyuki Nagasawa
Journal:  J Vet Med Sci       Date:  2002-03       Impact factor: 1.267

4.  Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.

Authors:  Markus Babst; David J Katzmann; Eden J Estepa-Sabal; Timo Meerloo; Scott D Emr
Journal:  Dev Cell       Date:  2002-08       Impact factor: 12.270

5.  Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells.

Authors:  Yoko Nagai-Tamai; Keiko Mizuno; Tomonori Hirose; Atsushi Suzuki; Shigeo Ohno
Journal:  Genes Cells       Date:  2002-11       Impact factor: 1.891

Review 6.  Elaborating polarity: PAR proteins and the cytoskeleton.

Authors:  Jeremy Nance; Jennifer A Zallen
Journal:  Development       Date:  2011-03       Impact factor: 6.868

7.  Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF.

Authors:  J Jarecki; E Johnson; M A Krasnow
Journal:  Cell       Date:  1999-10-15       Impact factor: 41.582

8.  Bazooka and atypical protein kinase C are required to regulate oocyte differentiation in the Drosophila ovary.

Authors:  D N Cox; S A Seyfried; L Y Jan; Y N Jan
Journal:  Proc Natl Acad Sci U S A       Date:  2001-12-04       Impact factor: 11.205

Review 9.  Branching morphogenesis of the Drosophila tracheal system.

Authors:  Amin Ghabrial; Stefan Luschnig; Mark M Metzstein; Mark A Krasnow
Journal:  Annu Rev Cell Dev Biol       Date:  2003       Impact factor: 13.827

10.  Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts.

Authors:  A Wodarz; A Ramrath; A Grimm; E Knust
Journal:  J Cell Biol       Date:  2000-09-18       Impact factor: 10.539

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  16 in total

1.  Transient junction anisotropies orient annular cell polarization in the Drosophila airway tubes.

Authors:  Chie Hosono; Ryo Matsuda; Boris Adryan; Christos Samakovlis
Journal:  Nat Cell Biol       Date:  2015-11-09       Impact factor: 28.824

2.  Examination of Drosophila larval tracheal terminal cells by light microscopy.

Authors:  Tiffani A Jones; Mark M Metzstein
Journal:  J Vis Exp       Date:  2013-07-09       Impact factor: 1.355

Review 3.  Molecular mechanisms of de novo lumen formation.

Authors:  Sara Sigurbjörnsdóttir; Renjith Mathew; Maria Leptin
Journal:  Nat Rev Mol Cell Biol       Date:  2014-09-04       Impact factor: 94.444

4.  Exocyst-mediated membrane trafficking is required for branch outgrowth in Drosophila tracheal terminal cells.

Authors:  Tiffani A Jones; Linda S Nikolova; Ani Schjelderup; Mark M Metzstein
Journal:  Dev Biol       Date:  2014-03-04       Impact factor: 3.582

Review 5.  Polarized protein transport and lumen formation during epithelial tissue morphogenesis.

Authors:  Alex J Blasky; Anthony Mangan; Rytis Prekeris
Journal:  Annu Rev Cell Dev Biol       Date:  2015-09-10       Impact factor: 13.827

Review 6.  Insane in the apical membrane: Trafficking events mediating apicobasal epithelial polarity during tube morphogenesis.

Authors:  Cayla E Jewett; Rytis Prekeris
Journal:  Traffic       Date:  2018-05-16       Impact factor: 6.215

7.  Polarized exocyst-mediated vesicle fusion directs intracellular lumenogenesis within the C. elegans excretory cell.

Authors:  Stephen T Armenti; Emily Chan; Jeremy Nance
Journal:  Dev Biol       Date:  2014-08-04       Impact factor: 3.582

8.  Drosophila Zpr1 (Zinc finger protein 1) is required downstream of both EGFR and FGFR signaling in tracheal subcellular lumen formation.

Authors:  Oscar E Ruiz; Linda S Nikolova; Mark M Metzstein
Journal:  PLoS One       Date:  2012-09-18       Impact factor: 3.240

9.  Bazooka/PAR3 is dispensable for polarity in Drosophila follicular epithelial cells.

Authors:  Jaffer Shahab; Manu D Tiwari; Mona Honemann-Capito; Michael P Krahn; Andreas Wodarz
Journal:  Biol Open       Date:  2015-03-13       Impact factor: 2.422

10.  Cropped, Drosophila transcription factor AP-4, controls tracheal terminal branching and cell growth.

Authors:  Matthew Man-Kin Wong; Ming-Fai Liu; Sung Kay Chiu
Journal:  BMC Dev Biol       Date:  2015-04-15       Impact factor: 1.978

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