Force Barriers for Membrane Tube Formation

Koster, Gerbrand; Cacciuto, Angelo; Derényi, Imre; Frenkel, Daan; Dogterom, Marileen

doi:10.1103/physrevlett.94.068101

Cited by 143 publications

(175 citation statements)

References 35 publications

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“…4A) show lipid-tether formation as typically observed with hydrophilic probes, characterized by the multiple step-like failure events with zero-withdrawal force plateaus on withdrawal (25,26). These thin membrane tubules nonspecifically bind to the probe and are extruded from the main bilayer with low resistance, often extending tens of microns in length (27). As each tether either snaps or breaks free of the probe, rapid jumps in tip deflection occur.…”

Section: Resultsmentioning

confidence: 99%

Fusion of biomimetic stealth probes into lipid bilayer cores

Almquist

Melosh

2010

Proc. Natl. Acad. Sci. U.S.A.

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Many biomaterials are designed to regulate the interactions between artificial and natural surfaces. However, when materials are inserted through the cell membrane itself the interface formed between the interior edge of the membrane and the material surface is not well understood and poorly controlled. Here we demonstrate that by replicating the nanometer-scale hydrophilichydrophobic-hydrophilic architecture of transmembrane proteins, artificial "stealth" probes spontaneously insert and anchor within the lipid bilayer core, forming a high-strength interface. These nanometer-scale hydrophobic bands are readily fabricated on metallic probes by functionalizing the exposed sidewall of an ultrathin evaporated Au metal layer rather than by lithography. Penetration and adhesion forces for butanethiol and dodecanethiol functionalized probes were directly measured using atomic force microscopy (AFM) on thick stacks of lipid bilayers to eliminate substrate effects. The penetration dynamics were starkly different for hydrophobic versus hydrophilic probes. Both 5-and 10 nm thick hydrophobically functionalized probes naturally resided within the lipid core, while hydrophilic probes remained in the aqueous region. Surprisingly, the barrier to probe penetration with short butanethiol chains (E o;5 nm ¼ 21.8k b T , E o;10 nm ¼ 15.3k b T ) was dramatically higher than longer dodecanethiol chains (E o;5 nm ¼ 14.0k b T , E o;10 nm ¼ 10.9k b T ), indicating that molecular mobility and orientation also play a role in addition to hydrophobicity in determining interface stability. These results highlight a new strategy for designing artificial cell interfaces that can nondestructively penetrate the lipid bilayer.atomic force microscopy | biophysics | membranes | proteins

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Section: Resultsmentioning

confidence: 99%

Fusion of biomimetic stealth probes into lipid bilayer cores

Almquist

Melosh

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…If the membrane is attached to a surface by a small adhesion patch, tube extrusion can be obtained when a f low is applied to the system (44). The diameter of the zone over which the force is applied is a crucial parameter, because it determines directly the force overshoot necessary to form a tube (45). If the adhesion patch is too large, the pulling system may not be able to extract a tube, although the force to extend the tube, once formed, is perfectly accessible.…”

Section: Discussionmentioning

confidence: 99%

Vesicles surfing on a lipid bilayer: Self-induced haptotactic motion

Solon

Streicher

Richter

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Haptotaxis is a mechanism proposed at the end of the 1960s to explain cell motility. It describes cell movement induced by an adhesion gradient. In this work, we present evidence for selfinduced haptotaxis using negatively charged giant vesicles interacting with positively charged supported lipid bilayers, which has not been previously described. Depending on the charge of the vesicle, we observed different behaviors. At low charge, no adhesion occurs. At high charge, the vesicle adheres but does not move. In a restricted range of intermediate charge densities, we found that the vesicle moves spontaneously with velocities of the order of a few micrometers per second over distances of >100 m. We show that a local lipid transfer between the giant vesicle and the supported lipid bilayer takes place during the adhesion, breaking the symmetry and inducing a lateral charge gradient. This charge gradient polarizes the giant vesicle and induces its motion. To explain our observations, we propose a scaling model that relates the adhesion energy to the velocity of vesicle motion and to the characteristic lipid transfer time. Our measurements indicate that the effective adhesion energy is strongly reduced by counterions, which are dynamically trapped between the vesicle and the supported bilayer.adhesion ͉ electrostatic interaction ͉ giant unilamellar vesicles ͉ haptotaxis ͉ lipid membrane

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“…For phospholipid vesicles, theory [16][17][18][19] provides an accurate, experimentally tested account of tether formation in terms of membrane tension and bending rigidity [15,20,21]. The situation with living cells is more complicated [22,23].…”

Section: Introductionmentioning

confidence: 99%

Eukaryotic membrane tethers revisited using magnetic tweezers

et al. 2007

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Membrane nanotubes, under physiological conditions, typically form en masse. We employed magnetic tweezers (MTW) to extract tethers from human brain tumor cells and compared their biophysical properties with tethers extracted after disruption of the cytoskeleton and from a strongly differing cell type, Chinese hamster ovary cells. In this method, the constant force produced with the MTW is transduced to cells through super-paramagnetic beads attached to the cell membrane. Multiple sudden jumps in bead velocity were manifest in the recorded bead displacement-time profiles. These discrete events were interpreted as successive ruptures of individual tethers. Observation with scanning electron microscopy supported the simultaneous existence of multiple tethers. The physical characteristics, in particular, the number and viscoelastic properties of the extracted tethers were determined from the analytic fit to bead trajectories, provided by a standard model of viscoelasticity. Comparison of tethers formed with MTW and atomic force microscopy (AFM), a technique where the cantilever-force transducer is moved at constant velocity, revealed significant differences in the two methods of tether formation. Our findings imply that extreme care must be used to interpret the outcome of tether pulling experiments performed with single molecular techniques (MTW, AFM, optical tweezers, etc). First, the different methods may be testing distinct membrane structures with distinct properties. Second, as soon as a true cell membrane (as opposed to that of a vesicle) can attach to a substrate, upon pulling on it, multiple nonspecific membrane tethers may be generated. Therefore, under physiological conditions, distinguishing between tethers formed through specific and nonspecific interactions is highly nontrivial if at all possible.

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Force Barriers for Membrane Tube Formation

Cited by 143 publications

References 35 publications

Fusion of biomimetic stealth probes into lipid bilayer cores

Fusion of biomimetic stealth probes into lipid bilayer cores

Vesicles surfing on a lipid bilayer: Self-induced haptotactic motion

Eukaryotic membrane tethers revisited using magnetic tweezers

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