Dynamic Tension Spectroscopy and Strength of Biomembranes

Abstract

Rupturing fluid membrane vesicles with a steady ramp of micropipette suction produces a distribution of breakage tensions governed by the kinetic process of membrane failure. When plotted as a function of log(tension loading rate), the locations of distribution peaks define a dynamic tension spectrum with distinct regimes that reflect passage of prominent energy barriers along the kinetic pathway. Using tests on five types of giant phosphatidylcholine lipid vesicles over loading rates(tension/time) from 0.01-100 mN/m/s, we show that the kinetic process of membrane breakage can be modeled by a causal sequence of two thermally-activated transitions. At fast loading rates, a steep linear regime appears in each spectrum which implies that membrane failure starts with nucleation of a rare precursor defect. The slope and projected intercept of this regime are set by defect size and frequency of spontaneous formation, respectively. But at slow loading rates, each spectrum crosses over to a shallow-curved regime where rupture tension changes weakly with rate. This regime is predicted by the classical cavitation theory for opening an unstable hole in a two-dimensional film within the lifetime of the defect state. Under slow loading, membrane edge energy and the frequency scale for thermal fluctuations in hole size are the principal factors that govern the level of tension at failure. To critically test the model and obtain the parameters governing the rates of transition under stress, distributions of rupture tension were computed and matched to the measured histograms through solution of the kinetic master (Markov) equations for defect formation and annihilation or evolution to an unstable hole under a ramp of tension. As key predictors of membrane strength, the results for spontaneous frequencies of defect formation and hole edge energies were found to correlate with membrane thicknesses and elastic bending moduli, respectively.

Mechanical Criterion for the Rupture of a Cell Membrane under Compression

“…2 is applicable to estimate the contact area, which leads to a compressive stress ranging from 17 to 43 kPa. This also is in reasonable agreement with our results, especially taking into account that incorporating peptides into lipid bilayers (hence getting a model somewhat closer to a cell membrane) makes them easier to break, according to micropipette aspiration (44) and AFM indentation (42) measurements. Kagiwada et al (45) reported that a typical force of 3 nN is required to insert a nanoneedle of 200 nm in diameter into a cell.…”

“…In another study using nanoneedle geometries, Xie et al (46,47) investigated the penetration of nanowires fixed to a substrate into cells that adhere to this substrate. They used a cell membrane rupture criterion based on activation energy theory and leading to a critical membrane tension to be reached before rupture (42,44). In the study of Xie et al, tensile forces of~1 nN are applied to the tips of nanowires of radius R ¼ 50 nm.…”

Lipid Domain Co-localization Induced by Membrane Undulations

“…What is perhaps more interesting is the observation that a significant (i.e., a 10-fold) decrease of L fluct relative to L fluct;free is obtained only when ðs' 2 =4p 2 k 0 ÞT1 or ða 2 ' 4 =ð16p 4 k 0 ÞÞT1. In the former case, sTðð4p 2 k 0 Þ=' 2 Þ $ 20 k B T= nm 2 , a value comparable to reported values of the membrane rupture tension (28). In the latter case, a 2 Tðð16p 4 k 0 Þ=' 4 Þ, or, upon introducing the root mean-square (RMS) height fluctuation, w 2 hhh 2 i 0 ¼ ðpk B T=ða 2 ' 2 ÞÞ, the condition becomes ðw='Þ(½k B T=16p 3 k 0 1=2 $ 10 À2 , where we have employed k 0 z20 k B T, appropriate for the Ld phase (21).…”

Molecular Structure Influences the Stability of Membrane Penetrating Biointerfaces.

“…Unfunctionalized probes were first measured to determine E 0 and γ for the situation where penetration of the underlying bilayer is the rate-limiting step, rather than bilayer adhesion to the band. The energy barrier height of 13.0±1.6k b T for the unfunctionalized case is in excellent agreement with the previously reported 16 energy barrier for defect formation and failure in SOPC bilayers of ~13.6k b T.…”