A quantitative model for the caveolae under cell membrane stretch

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ORIGINAL PAPER

A quantitative model for the caveolae under cell membrane stretch Meng Zhang1,2   · Anqi Chen2 Received: 26 January 2020 / Accepted: 20 June 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract In this paper, we proposed a two-state model to quantitatively illustrate the working mechanism of caveolae structure in the regulation of cell membrane stretch. First, we derived the free energy compositions of one caveola in an arbitrary state. This model predicts two local minima for the free energy of one caveola at the completely open and completely closed states at the bottom of a relatively deep curve of free energy at different shape coefficients. The behavior of one caveola is generalized to large number of caveolae in cell membranes using the central limit theory. The dynamic stretching behavior of membrane during a constant-speed tether-pulling experiment is also investigated by making a hypothesis of transition rate between the closed and open states. Keywords  Caveolae modeling · Cell membrane · Dynamic stretch

1 Introduction Cells are regarded as the elementary units to carry out various activities in living organisms. A significant characteristic of cells in these activities is that they constantly undergo shape deformations (Zhu et al. 2000; Skalak and Branemark 1969; Zarda et al. 1977; Wells and Schmid-Schonbein 1969). Accompanying this shape deformation is the capability of increasing cell membrane area within a short period of time. Experiments have found that muscle cells can increase surface area by 30% within 5 min of osmotic shock (Sinha et al. 2011). Endothelial cells that spread at the bottom of culture flasks can double their surface area within half an hour (Guo et al. 2017). Lipid bilayers are the backbone structures of cell membranes. However, they can only resist 3% to 5% enthalpic area expansion that originates from increasing space between neighboring lipids (Ho et al. 2016). Although cell membranes are flexible, with a bending rigidity of 50 kBT Meng Zhang and Anqi Chen have contributed equally to this work. * Meng Zhang [email protected] 1



Precision Medicine Institute, The First Affiliated Hospital of Sun Yat‑Sen University, Sun Yat-Sen University, Guangzhou 510080, China



School of Engineering and Applied Science, Harvard University, Cambridge 02138, USA

2

(Phillips et al. 2012), the entropy-driven elasticity is not significant enough to provide an expansion of membrane area of more than 15% (Helfrich and Servuss 1984). These facts point to the existence of membrane reservoirs that store large portion of lipid membrane somewhere other than on its projected area. These structures were first identified in the early 1950s through the development of electron microscopy (Palade 1953) and were named caveolae. Later, caveolae is also found to have a function in receptor regulation by fluid shear stress (Shin et al. 2019). These cup-shaped invaginations that are particularly abundant in muscle cells, adiopocytes and endothelial cells are t