Literature DB >> 30015616

Radially patterned cell behaviours during tube budding from an epithelium.

Yara E Sanchez-Corrales1, Guy B Blanchard2, Katja Röper1.   

Abstract

The budding of tubular organs from flat epithelial sheets is a vital morphogenetic process. Cell behaviours that drive such processes are only starting to be unraveled. Using live-imaging and novel morphometric methods, we show that in addition to apical constriction, radially oriented directional intercalation of cells plays a major contribution to early stages of invagination of the salivary gland tube in the Drosophila embryo. Extending analyses in 3D, we find that near the pit of invagination, isotropic apical constriction leads to strong cell-wedging. Further from the pit cells interleave circumferentially, suggesting apically driven behaviours. Supporting this, junctional myosin is enriched in, and neighbour exchanges are biased towards the circumferential orientation. In a mutant failing pit specification, neither are biased due to an inactive pit. Thus, tube budding involves radially patterned pools of apical myosin, medial as well as junctional, and radially patterned 3D-cell behaviours, with a close mechanical interplay between invagination and intercalation.
© 2018, Sanchez-Corrales et al.

Entities:  

Keywords:  D. melanogaster; cell biology; cell shape; developmental biology; epithelia; morphogenesis; organogenesis; quantitative analysis; radial polarity

Mesh:

Substances:

Year:  2018        PMID: 30015616      PMCID: PMC6089598          DOI: 10.7554/eLife.35717

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  52 in total

1.  Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane.

Authors:  Monn Monn Myat; Deborah J Andrew
Journal:  Cell       Date:  2002-12-13       Impact factor: 41.582

2.  Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts.

Authors:  A Wodarz; A Ramrath; U Kuchinke; E Knust
Journal:  Nature       Date:  1999-12-02       Impact factor: 49.962

3.  Regulation and function of Scr, exd, and hth in the Drosophila salivary gland.

Authors:  K D Henderson; D J Andrew
Journal:  Dev Biol       Date:  2000-01-15       Impact factor: 3.582

4.  Salivary gland determination in Drosophila: a salivary-specific, fork head enhancer integrates spatial pattern and allows fork head autoregulation.

Authors:  B Zhou; A Bagri; S K Beckendorf
Journal:  Dev Biol       Date:  2001-09-01       Impact factor: 3.582

5.  Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos.

Authors:  Anne Royou; Christine Field; John C Sisson; William Sullivan; Roger Karess
Journal:  Mol Biol Cell       Date:  2003-12-02       Impact factor: 4.138

6.  Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation.

Authors:  Claire Bertet; Lawrence Sulak; Thomas Lecuit
Journal:  Nature       Date:  2004-06-10       Impact factor: 49.962

7.  Patterned gene expression directs bipolar planar polarity in Drosophila.

Authors:  Jennifer A Zallen; Eric Wieschaus
Journal:  Dev Cell       Date:  2004-03       Impact factor: 12.270

8.  Organ shape in the Drosophila salivary gland is controlled by regulated, sequential internalization of the primordia.

Authors:  M M Myat; D J Andrew
Journal:  Development       Date:  2000-02       Impact factor: 6.868

9.  Fork head prevents apoptosis and promotes cell shape change during formation of the Drosophila salivary glands.

Authors:  M M Myat; D J Andrew
Journal:  Development       Date:  2000-10       Impact factor: 6.868

10.  Organogenesis in Drosophila melanogaster: embryonic salivary gland determination is controlled by homeotic and dorsoventral patterning genes.

Authors:  S Panzer; D Weigel; S K Beckendorf
Journal:  Development       Date:  1992-01       Impact factor: 6.868

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  22 in total

1.  A 3D cell shape that enables tube formation.

Authors:  Guy Blanchard
Journal:  Nature       Date:  2018-09       Impact factor: 49.962

Review 2.  Cell intercalation in a simple epithelium.

Authors:  Matteo Rauzi
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-24       Impact factor: 6.237

3.  Theoretical tool bridging cell polarities with development of robust morphologies.

Authors:  Silas Boye Nissen; Steven Rønhild; Ala Trusina; Kim Sneppen
Journal:  Elife       Date:  2018-11-27       Impact factor: 8.140

Review 4.  Orchestrating morphogenesis: building the body plan by cell shape changes and movements.

Authors:  Kia Z Perez-Vale; Mark Peifer
Journal:  Development       Date:  2020-09-11       Impact factor: 6.868

5.  Secrets of secretion-How studies of the Drosophila salivary gland have informed our understanding of the cellular networks underlying secretory organ form and function.

Authors:  Rajprasad Loganathan; Ji Hoon Kim; Michael B Wells; Deborah J Andrew
Journal:  Curr Top Dev Biol       Date:  2020-11-19       Impact factor: 4.897

6.  Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis.

Authors:  Akankshi Munjal; Edouard Hannezo; Tony Y-C Tsai; Timothy J Mitchison; Sean G Megason
Journal:  Cell       Date:  2021-12-22       Impact factor: 41.582

7.  Topological defects of integer charge in cell monolayers.

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Journal:  Soft Matter       Date:  2021-03-12       Impact factor: 3.679

8.  Origami: Single-cell 3D shape dynamics oriented along the apico-basal axis of folding epithelia from fluorescence microscopy data.

Authors:  Tania Mendonca; Ana A Jones; Jose M Pozo; Sarah Baxendale; Tanya T Whitfield; Alejandro F Frangi
Journal:  PLoS Comput Biol       Date:  2021-11-01       Impact factor: 4.475

9.  Correct regionalization of a tissue primordium is essential for coordinated morphogenesis.

Authors:  Yara E Sánchez-Corrales; Guy B Blanchard; Katja Röper
Journal:  Elife       Date:  2021-11-01       Impact factor: 8.140

10.  A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding.

Authors:  Ghislain Gillard; Gemma Girdler; Katja Röper
Journal:  Nat Commun       Date:  2021-07-02       Impact factor: 14.919

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