» Articles » PMID: 24316147

The Plasma Membrane Flattens out to Fuel Cell-surface Growth During Drosophila Cellularization

Overview
Journal Dev Cell
Publisher Cell Press
Date 2013 Dec 10
PMID 24316147
Citations 34
Authors
Affiliations
Soon will be listed here.
Abstract

Cell-shape change demands cell-surface growth, but how growth is fueled and choreographed is still debated. Here we use cellularization, the first complete cytokinetic event in Drosophila embryos, to show that cleavage furrow ingression is kinetically coupled to the loss of surface microvilli. We modulate furrow kinetics with RNAi against the Rho1-GTPase regulator slam and show that furrow ingression controls the rate of microvillar depletion. Finally, we directly track the microvillar membrane and see it move along the cell surface and into ingressing furrows, independent of endocytosis. Together, our results demonstrate that the kinetics of the ingressing furrow regulate the utilization of a microvillar membrane reservoir. Because membranes of the furrow and microvilli are contiguous, we suggest that ingression drives unfolding of the microvilli and incorporation of microvillar membrane into the furrow. We conclude that plasma membrane folding/unfolding can contribute to the cell-shape changes that promote embryonic morphogenesis.

Citing Articles

Differential regulation of the proteome and phosphoproteome along the dorso-ventral axis of the early embryo.

Gomez J, Nolte H, Vogelsang E, Dey B, Takeda M, Giudice G Elife. 2024; 13.

PMID: 39221782 PMC: 11466282. DOI: 10.7554/eLife.99263.


Centrosome-organized plasma membrane infoldings linked to growth of a cortical actin domain.

Tam R, Harris T J Cell Biol. 2024; 223(10).

PMID: 38935075 PMC: 11215285. DOI: 10.1083/jcb.202403115.


Reshaping the Syncytial Drosophila Embryo with Cortical Actin Networks: Four Main Steps of Early Development.

Tam R, Harris T Results Probl Cell Differ. 2023; 71:67-90.

PMID: 37996673 DOI: 10.1007/978-3-031-37936-9_4.


A comprehensive model of epithelium reveals the role of embryo geometry and cell topology in mechanical responses.

Cheikh M, Tchoufag J, Osterfield M, Dean K, Bhaduri S, Zhang C Elife. 2023; 12.

PMID: 37782009 PMC: 10584372. DOI: 10.7554/eLife.85569.


Consumption of a polarized membrane reservoir drives asymmetric membrane expansion during the unequal divisions of neural stem cells.

LaFoya B, Prehoda K Dev Cell. 2023; 58(11):993-1003.e3.

PMID: 37116487 PMC: 10247545. DOI: 10.1016/j.devcel.2023.04.006.


References
1.
Masters T, Pontes B, Viasnoff V, Li Y, Gauthier N . Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis. Proc Natl Acad Sci U S A. 2013; 110(29):11875-80. PMC: 3718161. DOI: 10.1073/pnas.1301766110. View

2.
Grosshans J, Wenzl C, Herz H, Bartoszewski S, Schnorrer F, Vogt N . RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development. 2005; 132(5):1009-20. DOI: 10.1242/dev.01669. View

3.
Murthy M, Teodoro R, Miller T, Schwarz T . Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization. Development. 2010; 137(16):2773-83. PMC: 2910387. DOI: 10.1242/dev.048330. View

4.
Schweitzer J, Burke E, Goodson H, DSouza-Schorey C . Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem. 2005; 280(50):41628-35. DOI: 10.1074/jbc.M504497200. View

5.
Keren K, Pincus Z, Allen G, Barnhart E, Marriott G, Mogilner A . Mechanism of shape determination in motile cells. Nature. 2008; 453(7194):475-80. PMC: 2877812. DOI: 10.1038/nature06952. View