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 load1. Rupture can also be induced by processes such as cell death2, and active cell membrane repair mechanisms are essential to preserve cell integrity3. Pore formation in cell membranes is also at the heart of many biomedical applications such as in drug, gene and short interfering RNA delivery4. Membrane rupture dynamics has been studied in bilayer vesicles under tensile stress5,6,7,8, which consistently produce circular pores5,6. 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 dynamics9. Such noisy dynamics appear in fracture of solid disordered materials10, in dislocation avalanches in plastic deformations11 and domain wall magnetization avalanches12. We also observed similar fractal rupture mechanics in spreading cell membranes.

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Figure 1: Increase in wetted surface area in growing flat unilamellar vesicles undergoing floral and fractal membrane rupture.
Figure 2: Propagation of a lipid bilayer rupture as a viscous fingering-like instability.
Figure 3: Propagation of a lipid bilayer rupture in fractal patterns.
Figure 4: Propagation of a lipid bilayer rupture in fractal patterns in two different CHO cells.

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Acknowledgements

This work was made possible through financial support obtained from the European Research Council (ERC Advanced Grant), The Swedish Research Council (VR) and the Knut and Alice Wallenberg Foundation.

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O.O. and T.L. conceived the original concept. I.G. carried out the microscopy experiments. P.D. developed the theoretical framework. I.C. and P.D. carried out data treatment and analysis of the fractal ruptures. A.J. carried out image analysis of pore edge regions. All authors contributed to writing the manuscript.

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Correspondence to Owe Orwar.

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The authors declare no competing financial interests.

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Gözen, I., Dommersnes, P., Czolkos, I. et al. Fractal avalanche ruptures in biological membranes. Nature Mater 9, 908–912 (2010). https://doi.org/10.1038/nmat2854

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