The role of the membrane confinement in the surface area regulation of cells (original) (raw)

Mechanics of surface area regulation in cells examined with confined lipid membranes

Proceedings of The National Academy of Sciences, 2011

Cells are wrapped in inelastic membranes, yet they can sustain large mechanical strains by regulating their area. The area regulation in cells is achieved either by membrane folding or by membrane exo-and endocytosis. These processes involve complex morphological transformations of the cell membrane, i.e., invagination, vesicle fusion, and fission, whose precise mechanisms are still under debate. Here we provide mechanistic insights into the area regulation of cell membranes, based on the previously neglected role of membrane confinement, as well as on the strain-induced membrane tension. Commonly, the membranes of mammalian and plant cells are not isolated, but rather they are adhered to an extracellular matrix, the cytoskeleton, and to other cell membranes. Using a lipid bilayer, coupled to an elastic sheet, we are able to demonstrate that, upon straining, the confined membrane is able to regulate passively its area. In particular, by stretching the elastic support, the bilayer laterally expands without rupture by fusing adhered lipid vesicles; upon compression, lipid tubes grow out of the membrane plane, thus reducing its area. These transformations are reversible, as we show using cycles of expansion and compression, and closely reproduce membrane processes found in cells during area regulation. Moreover, we demonstrate a new mechanism for the formation of lipid tubes in cells, which is driven by the membrane lateral compression and may therefore explain the various membrane tubules observed in shrinking cells.

Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells

Biochimica et Biophysica Acta (BBA) - Biomembranes, 2008

Ternary lipid compositions in model membranes segregate into large-scale liquid-ordered (L o) and liquiddisordered (L d) phases. Here, we show μm-sized lipid domain separation leading to vesicle formation in unperturbed human HaCaT keratinocytes. Budding vesicles in the apical portion of the plasma membrane were predominantly labelled with L d markers 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate, 1,1′-dilinoleyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate, 1,1′-didodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate and weakly stained by L o marker fluorescein-labeled cholera toxin B subunit which labels ganglioside GM 1 enriched plasma membrane rafts. Cholesterol depletion with methylβ-cyclodextrin enhanced DiI vesiculation, GM 1 /DiI domain separation and was accompanied by a detachment of the subcortical cytoskeleton from the plasma membrane. Based on these observations we describe the energetic requirements for plasma membrane vesiculation. We propose that the decrease in total 'L o /L d ' boundary line tension arising from the coalescence of smaller L d-like domains makes it energetically favourable for L d-like domains to bend from flat μm-sized surfaces to cap-like budding vesicles. Thus living cells may utilize membrane line tension energies as a control mechanism of exocytic events.

Inflated Vesicles: A New Phase of Fluid Membranes

EPL (Europhysics Letters)

The conformation and scaling properties of self-avoiding fluid vesicles subject to an internal-pressure increment A p a 0 are studied using Monte Carlo methods and scaling arguments. We find that there is a firstader phase transition from a low-pressure, branched polymer phase to a high-pressure, inflated phase. Evidence is presented that the crossover exponent in the branched polymer phase is zero. The behavior in the inflated phase is analyzed using a generalization of de Gennes' <<blob* picture, and it is shown that the mean-square radius of gyration within the blobs scales with a new, independent exponent v = 0.787 5 0.020, where (R;) -N;, and Nb is the number of monomers in a blob.

Geometry and dynamics of lipid membranes

2019

The equations governing lipid membrane dynamics in planar, spherical, and cylindrical geometries are presented here. Unperturbed and first-order perturbed equations are determined and non-dimensionalized. A new dimensionless number, named the Scriven-Love number, and the wellknown Föppl-von Kármán number result from a non-dimensional analysis. The Scriven-Love number compares out-of-plane forces arising from the in-plane, intramembrane viscous stresses to the familiar elastic bending forces, while the Föppl-von Kármán number compares tension to bending forces. Both numbers are calculated in past experimental works, and span a wide range of values in various biological processes across different geometries. In situations with large Scriven-Love and Föppl-von Kármán numbers, the dynamical response of a perturbed membrane is dominated by out-of-plane viscous and surface tension forces-with bending forces playing a negligible role. Calculations of non-negligible Scriven-Love numbers in various biological processes and in vitro experiments show in-plane intramembrane fluidity cannot generally be ignored when analyzing lipid membrane behavior.

Osmotic Gradients Induce Bio-Reminiscent Morphological Transformations in Giant Unilamellar Vesicles

Frontiers in Physiology, 2012

We report observations of large-scale, in-plane and out-of-plane membrane deformations in giant uni-and multilamellar vesicles composed of binary and ternary lipid mixtures in the presence of net transvesicular osmotic gradients. The lipid mixtures we examined consisted of binary mixtures of DOPC and DPPC lipids and ternary mixtures comprising POPC, sphingomyelin and cholesterol over a range of compositions -both of which produce co-existing phases for selected ranges of compositions at room temperature under thermodynamic equilibrium. In the presence of net osmotic gradients, we find that the in-plane phase separation potential of these mixtures is non-trivially altered and a variety of out-of-plane morphological remodeling events occur. The repertoire of membrane deformations we observe display striking resemblance to their biological counterparts in live cells encompassing vesiculation, membrane fission and fusion, tubulation and pearling, as well as expulsion of entrapped vesicles from multicompartmental giant unilamellar vesicles through large, self-healing transient pores.These observations suggest that the forces introduced by simple osmotic gradients across membrane boundaries could act as a trigger for shape-dependent membrane and vesicle trafficking activities. We speculate that such coupling of osmotic gradients with membrane properties might have provided lipidmediated mechanisms to compensate for osmotic stress during the early evolution of membrane compartmentalization in the absence of osmoregulatory protein machinery.

The ins and outs in membrane dynamics: tubulation and vesiculation

Trends in plant science, 2005

Living cells constantly adjust the composition and size of their membrane systems to accommodate the demands for the housekeeping activities, to expand and reduce cell size, and to commit the cell for division. Although it is well known that vesicles are the vehicles to deliver and retrieve lipids and proteins to and from the membranes, the mechanisms allowing vesicles to pinch off from membranes or fuse into a flat lipid bilayer have been poorly understood, particularly in plants. Recent studies on dynamins and dynamin-related proteins in animals and plants now allow new concepts in membrane dynamics to be considered.