Fractal avalanche ruptures in biological membranes

Abstract

Bilayer membranes envelope cells as well as organelles, and constitute the most ubiquitous biological material found in all branches of the phylogenetic tree. Cell membrane rupture is an important biological process, and substantial rupture rates are found in skeletal and cardiac muscle cells under a mechanical load. Rupture can also be induced by processes such as cell death, and active cell membrane repair mechanisms are essential to preserve cell integrity. Pore formation in cell membranes is also at the heart of many biomedical applications such as in drug, gene and short interfering RNA delivery. Membrane rupture dynamics has been studied in bilayer vesicles under tensile stress, which consistently produce circular pores. We observed very different rupture mechanics in bilayer membranes spreading on solid supports: in one instance fingering instabilities were seen resulting in floral-like pores and in another, the rupture proceeded in a series of rapid avalanches causing fractal membrane fragmentation. The intermittent character of rupture evolution and the broad distribution in avalanche sizes is consistent with crackling-noise dynamics. Such noisy dynamics appear in fracture of solid disordered materials, in dislocation avalanches in plastic deformations and domain wall magnetization avalanches. We also observed similar fractal rupture mechanics in spreading cell membranes.

Imaging the dynamics of individual electropores

“…We note that the rupture patterns we observe (Fig. 5A, lower row) are similar to the floral instability patterns seen in rupturing multilamellar vesicles (41).…”

Peridynamic Modeling of Ruptures in Biomembranes

“…Lipid film precursors, buffered solutions, and high energy surfaces were prepared as described earlier[1]. As shown in Fig 1, Multilamellar (or onion shell) lipid vesicles were manually deposited on a silicon oxide surface, where self-spreading occurred spontaneously, forming a circular double bilayer patch (Fig 1A) with a fixed proximal (lower) and mobile distal (upper) bilayer (Fig 1B).…”

“…It was recently shown that a double phospholipid bilayer membrane, forming spontaneously from a lipid source on a solid support, can form both floral and fractal ruptures[1]. In double bilayer membranes, the two individual stacked bilayers are in close proximity, separated by a nanoscopically thin water layer.…”

Mechanism of Lipid Nanodrop Spreading in a Case of Asymmetric Wetting

“…Lipid films on a hydrophilic substrate in water correspond to the so-called symmetric wetting situation [16,17], where the number of monolayer leaflets in the supported film is even, due to the preferential affinity of both the solid and the liquid with the polar head of the molecules. In this case, spreading has been described as the rolling of the front bilayer creeping on the solid surface [18][19][20][21]. The same mechanism does not transpose to the asymmetric wetting situation [16,[22][23][24], where the solid and the free surface prefer to be in contact with opposite parts of the molecule (hydrophilic versus hydrophobic).…”