Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir

Lauren Figard, Mengyu Wang, Liuliu Zheng, Ido Golding, Anna Marie Sokac

Research output: Contribution to journalArticle

Abstract

Cells store membrane in surface reservoirs of pits and protrusions. These membrane reservoirs facilitate cell shape change and buffer mechanical stress, but we do not know how reservoir dynamics are regulated. During cellularization, the first cytokinesis in Drosophila embryos, a reservoir of microvilli unfolds to fuel cleavage furrow ingression. We find that regulated exocytosis adds membrane to the reservoir before and during unfolding. Dynamic F-actin deforms exocytosed membrane into microvilli. Single microvilli extend and retract in ~20 s, while the overall reservoir is depleted in sync with furrow ingression over 60-70 min. Using pharmacological and genetic perturbations, we show that exocytosis promotes microvillar F-actin assembly, while furrow ingression controls microvillar F-actin disassembly. Thus, reservoir F-actin and, consequently, reservoir dynamics are regulated by membrane supply from exocytosis and membrane demand from furrow ingression.

Original languageEnglish (US)
Pages (from-to)267-278
Number of pages12
JournalDevelopmental cell
Volume37
Issue number3
DOIs
StatePublished - May 9 2016
Externally publishedYes

Fingerprint

Actins
Membranes
Exocytosis
Microvilli
Mechanical Stress
Cytokinesis
Cell Shape
Drosophila
Buffers
Embryonic Structures
Cell Membrane
Pharmacology

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir. / Figard, Lauren; Wang, Mengyu; Zheng, Liuliu; Golding, Ido; Sokac, Anna Marie.

In: Developmental cell, Vol. 37, No. 3, 09.05.2016, p. 267-278.

Research output: Contribution to journalArticle

Figard, Lauren ; Wang, Mengyu ; Zheng, Liuliu ; Golding, Ido ; Sokac, Anna Marie. / Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir. In: Developmental cell. 2016 ; Vol. 37, No. 3. pp. 267-278.
@article{c4d01a1108564e4a8b90bbb0774dea42,
title = "Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir",
abstract = "Cells store membrane in surface reservoirs of pits and protrusions. These membrane reservoirs facilitate cell shape change and buffer mechanical stress, but we do not know how reservoir dynamics are regulated. During cellularization, the first cytokinesis in Drosophila embryos, a reservoir of microvilli unfolds to fuel cleavage furrow ingression. We find that regulated exocytosis adds membrane to the reservoir before and during unfolding. Dynamic F-actin deforms exocytosed membrane into microvilli. Single microvilli extend and retract in ~20 s, while the overall reservoir is depleted in sync with furrow ingression over 60-70 min. Using pharmacological and genetic perturbations, we show that exocytosis promotes microvillar F-actin assembly, while furrow ingression controls microvillar F-actin disassembly. Thus, reservoir F-actin and, consequently, reservoir dynamics are regulated by membrane supply from exocytosis and membrane demand from furrow ingression.",
author = "Lauren Figard and Mengyu Wang and Liuliu Zheng and Ido Golding and Sokac, {Anna Marie}",
year = "2016",
month = "5",
day = "9",
doi = "10.1016/j.devcel.2016.04.010",
language = "English (US)",
volume = "37",
pages = "267--278",
journal = "Developmental Cell",
issn = "1534-5807",
publisher = "Cell Press",
number = "3",

}

TY - JOUR

T1 - Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir

AU - Figard, Lauren

AU - Wang, Mengyu

AU - Zheng, Liuliu

AU - Golding, Ido

AU - Sokac, Anna Marie

PY - 2016/5/9

Y1 - 2016/5/9

N2 - Cells store membrane in surface reservoirs of pits and protrusions. These membrane reservoirs facilitate cell shape change and buffer mechanical stress, but we do not know how reservoir dynamics are regulated. During cellularization, the first cytokinesis in Drosophila embryos, a reservoir of microvilli unfolds to fuel cleavage furrow ingression. We find that regulated exocytosis adds membrane to the reservoir before and during unfolding. Dynamic F-actin deforms exocytosed membrane into microvilli. Single microvilli extend and retract in ~20 s, while the overall reservoir is depleted in sync with furrow ingression over 60-70 min. Using pharmacological and genetic perturbations, we show that exocytosis promotes microvillar F-actin assembly, while furrow ingression controls microvillar F-actin disassembly. Thus, reservoir F-actin and, consequently, reservoir dynamics are regulated by membrane supply from exocytosis and membrane demand from furrow ingression.

AB - Cells store membrane in surface reservoirs of pits and protrusions. These membrane reservoirs facilitate cell shape change and buffer mechanical stress, but we do not know how reservoir dynamics are regulated. During cellularization, the first cytokinesis in Drosophila embryos, a reservoir of microvilli unfolds to fuel cleavage furrow ingression. We find that regulated exocytosis adds membrane to the reservoir before and during unfolding. Dynamic F-actin deforms exocytosed membrane into microvilli. Single microvilli extend and retract in ~20 s, while the overall reservoir is depleted in sync with furrow ingression over 60-70 min. Using pharmacological and genetic perturbations, we show that exocytosis promotes microvillar F-actin assembly, while furrow ingression controls microvillar F-actin disassembly. Thus, reservoir F-actin and, consequently, reservoir dynamics are regulated by membrane supply from exocytosis and membrane demand from furrow ingression.

UR - http://www.scopus.com/inward/record.url?scp=84975028922&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84975028922&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2016.04.010

DO - 10.1016/j.devcel.2016.04.010

M3 - Article

C2 - 27165556

AN - SCOPUS:84975028922

VL - 37

SP - 267

EP - 278

JO - Developmental Cell

JF - Developmental Cell

SN - 1534-5807

IS - 3

ER -