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The Mechanics and Thermodynamics of Tubule Formation in Biological Membranes

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Abstract

Membrane tubulation is a ubiquitous process that occurs both at the plasma membrane and on the membranes of intracellular organelles. These tubulation events are known to be mediated by forces applied on the membrane either due to motor proteins, by polymerization of the cytoskeleton, or due to the interactions between membrane proteins binding onto the membrane. The numerous experimental observations of tube formation have been amply supported by mathematical modeling of the associated membrane mechanics and have provided insights into the force-displacement relationships of membrane tubes. Recent advances in quantitative biophysical measurements of membrane-protein interactions and tubule formation have necessitated the need for advances in modeling that will account for the interplay of multiple aspects of physics that occur simultaneously. Here, we present a comprehensive review of experimental observations of tubule formation and provide context from the framework of continuum modeling. Finally, we explore the scope for future research in this area with an emphasis on iterative modeling and experimental measurements that will enable us to expand our mechanistic understanding of tubulation processes in cells.

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Abbreviations

AC:

Anterograde carriers

BAR:

Bin/Amphiphysin/Rvs

BDP:

BAR domain protein

BFA:

Brefeldin A

BIN1:

Bridging Integrator 1

CICR:

Calcium-induced calcium release

ER:

Endoplasmic reticulum

ERES:

ER exit site

ERGIC:

ER-Golgi intermediate compartment

GFP:

Green Fluorescent Protein

GUV:

Giant unilamellar vesicle

iPALM:

Interferometric photoactivated localization microscopy

LTCC:

yL-type calcium channel

PEC:

Protrusion, engorgement, and consolidation

RyRs:

Ryanodine receptors

SR:

Sarcoplasmic reticulum

TC:

Transport carrier

T-tubules:

Transverse tubules

wtENTH:

Wild-type epsin N-terminal homology

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Acknowledgements

The authors would like to thank their many collaborators in the field of membrane mechanics for discussing ideas and the organizers of the International Symposium on Cell Surface Macromolecules 2020 for engaging discussions. They would also like to acknowledge Haleh Alimohamadi, Prof. Ali Behzadan, Miriam Bell, and Jennifer Fromm for providing their critical comments and feedback for the manuscript. This work was supported by NIH R01GM132106 to P.R.

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  1. A. Mahapatra and C. Uysalel have contributed equally to this work.

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  1. Department of Mechanical and Aerospace Engineering, University of California San Diego, 9500 Gilman Dr, La Jolla, CA, 92093, USA

    Arijit Mahapatra, Can Uysalel & Padmini Rangamani

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  1. Arijit Mahapatra
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  3. Padmini Rangamani
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Mahapatra, A., Uysalel, C. & Rangamani, P. The Mechanics and Thermodynamics of Tubule Formation in Biological Membranes. J Membrane Biol 254, 273–291 (2021). https://doi.org/10.1007/s00232-020-00164-9

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