Membrane Curvature and Tension Control the Formation and Collapse of Caveolar Superstructures

Gonen Golani, Nicholas Ariotti, Robert G. Parton*, Michael M. Kozlov

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

50 Scopus citations

Abstract

Caveolae, flask-shaped pits covered by caveolin-cavin coats, are abundant features of the plasma membrane of many cells. Besides appearing as single-membrane indentations, caveolae are organized as superstructures in the form of rosette-like clusters, whose mechanism of assembly and biological functions have been elusive. Here, we propose that clustering of caveolae in mature muscle cells is driven by forces originating from the elastic energy of membrane-bending deformations and membrane tension. We substantiate this mechanism by computational modeling, which recovers the unique shapes observed for the most ubiquitous caveolar clusters. We support the agreement between the calculated and observed configurations by electron tomography of caveolar clusters. The model predicts the experimentally assessable dependence of caveolar clustering on membrane tension and on the degree of the caveolar coat assembly. We reveal a difference in conformation and, possibly, in function and formation mechanism between caveolar clusters of muscle cells and of adipocytes.

Original languageEnglish
Pages (from-to)523-538.e4
JournalDevelopmental Cell
Volume48
Issue number4
DOIs
StatePublished - 25 Feb 2019

Funding

FundersFunder number
Centre of Excellence in Convergent Bio-Nano Science and TechnologyDP 150100505
EU consortium InCeM
Australian Research Council
National Health and Medical Research CouncilAPP1100771, APP1058565, APP1037320, APP569542, APP1045092
Israel Science Foundation1066/15
Erzincan Üniversitesi
Azərbaycan Respirator Cəmiyyəti

    Keywords

    • caveolae
    • caveolar clusters
    • mechano-protective function
    • membrane bending elasticity
    • membrane curvature
    • membrane tension
    • membrane-mediated interaction
    • modeling caveolae

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