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PMID: 15695629 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Coalescence of membrane tethers: experiments, theory, and applications.

Biophysical journal ·Vol. 88 ·No. 4 ·2005-04-00 ·Pages 2714-26

Cuvelier D, Derényi I, Bassereau P, Nassoy P

Abstract

Tethers are nanocylinders of lipid bilayer membrane, arising in situations ranging from micromanipulation experiments on synthetic vesicles to the formation of dynamic tubular networks in the Golgi apparatus. Relying on the extensive theoretical and experimental works aimed to understand the physics of individual tethers formation, we addressed the problem of the interaction between two nanotubes. By using a combination of micropipette manipulation and optical tweezers, we quantitatively studied the process of coalescence that occurred when the separation distance between both vesicle-tether junctions became smaller than a threshold length. Our experiments, which were supported by an original theoretical analysis, demonstrated that the measurements of the tether force and angle between tethers at coalescence directly yield the bending rigidity, kappa, and the membrane tension, sigma, of the vesicles. Contrary to other methods used to probe the bending rigidity of vesicles, the proposed approach permits a direct measurement of kappa without requiring any control of the membrane tension. Finally, after validation of the method and proposal of possible applications, we experimentally investigated the dynamics of the coalescence process.

MeSH Terms
Animals Biophysics/methods Calibration Cell Membrane/chemistry Chickens Cytoskeleton/metabolism Electrochemistry Lipid Bilayers/chemistry,metabolism Lipids/chemistry Membrane Fluidity Membranes/chemistry Membranes, Artificial Microscopy, Video Models, Biological Models, Statistical Models, Theoretical Phosphatidylcholines/chemistry Surface Properties Time Factors
Chemicals
Lipid Bilayers Lipids Membranes, Artificial Phosphatidylcholines
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Cuvelier Damien
Laboratoire de Physico-Chimie Curie, Institut Curie, F-75005 Paris, France.
Derényi Imre
Bassereau Patricia
Nassoy Pierre
References (38)
38 references, click to expand
  1. Mechanical tweezer action by self-tightening knots in surfactant nanotubes.
    Proc Natl Acad Sci U S A. 2004 May 25;101(21):7949-53 PMID: 15141081
  2. Membrane tube formation from giant vesicles by dynamic association of motor proteins.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15583-8 PMID: 14663143
  3. Effect of chain length and unsaturation on elasticity of lipid bilayers.
    Biophys J. 2000 Jul;79(1):328-39 PMID: 10866959
  4. Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique.
    Biophys J. 1973 Aug;13(8):747-62 PMID: 4726877
  5. Mechanical equilibrium of thick, hollow, liquid membrane cylinders.
    Biophys J. 1987 Sep;52(3):391-400 PMID: 3651558
  6. Entropy-driven tension and bending elasticity in condensed-fluid membranes.
    Phys Rev Lett. 1990 Apr 23;64(17):2094-2097 PMID: 10041575
  7. Formation and interaction of membrane tubes.
    Phys Rev Lett. 2002 Jun 10;88(23):238101 PMID: 12059401
  8. Thermoelasticity of red blood cell membrane.
    Biophys J. 1979 Apr;26(1):115-31 PMID: 262408
  9. Nanotube-vesicle networks with functionalized membranes and interiors.
    J Am Chem Soc. 2003 Jan 15;125(2):374-8 PMID: 12517148
  10. Adhesion energy of receptor-mediated interaction measured by elastic deformation.
    Biophys J. 1999 Mar;76(3):1632-8 PMID: 10049343
  11. Hidden dynamics of vesicle adhesion induced by specific stickers.
    Phys Rev Lett. 2004 Nov 26;93(22):228101 PMID: 15601119
  12. Formation of membrane networks in vitro by kinesin-driven microtubule movement.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2233-41 PMID: 3143735
  13. Membrane tether formation from blebbing cells.
    Biophys J. 1999 Dec;77(6):3363-70 PMID: 10585959
  14. Vesicle deformation by an axial load: from elongated shapes to tethered vesicles.
    Biophys J. 1999 Apr;76(4):2056-71 PMID: 10096901
  15. Theoretical analysis of the effect of the transbilayer movement of phospholipid molecules on the dynamic behavior of a microtube pulled out of an aspirated vesicle.
    Eur Biophys J. 1998;27(3):197-209 PMID: 9615393
  16. A piconewton force transducer and its application to measurement of the bending stiffness of phospholipid membranes.
    Ann Biomed Eng. 1996 Sep-Oct;24(5):595-605 PMID: 8886240
  17. Fluid-membrane tethers: minimal surfaces and elastic boundary layers.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2002 Apr;65(4 Pt 1):041901 PMID: 12005867
  18. All-optical measurements of the bending rigidity of lipid-vesicle membranes across structural phase transitions.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2001 Aug;64(2 Pt 1):020901 PMID: 11497555
  19. Force barriers for membrane tube formation.
    Phys Rev Lett. 2005 Feb 18;94(6):068101 PMID: 15783778
  20. Cell adhesion. Competition between nonspecific repulsion and specific bonding.
    Biophys J. 1984 Jun;45(6):1051-64 PMID: 6743742
  21. Cell control by membrane-cytoskeleton adhesion.
    Nat Rev Mol Cell Biol. 2001 May;2(5):392-6 PMID: 11331914
  22. Refined contour analysis of giant unilamellar vesicles.
    Eur Phys J E Soft Matter. 2004 Mar;13(3):277-90 PMID: 15103522
  23. Biomembrane templates for nanoscale conduits and networks.
    Science. 1996 Aug 16;273(5277):933-5 PMID: 8688071
  24. Role of curvature and phase transition in lipid sorting and fission of membrane tubules.
    EMBO J. 2005 Apr 20;24(8):1537-45 PMID: 15791208
  25. Unzipping DNA with optical tweezers: high sequence sensitivity and force flips.
    Biophys J. 2002 Mar;82(3):1537-53 PMID: 11867467
  26. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy.
    Nature. 1999 Jan 7;397(6714):50-3 PMID: 9892352
  27. A minimal system allowing tubulation with molecular motors pulling on giant liposomes.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5394-9 PMID: 11959994
  28. Pretransitional effects in dimyristoylphosphatidylcholine vesicle membranes: optical dynamometry study.
    Biophys J. 2000 Jul;79(1):340-56 PMID: 10866960
  29. Formation of geometrically complex lipid nanotube-vesicle networks of higher-order topologies.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11573-8 PMID: 12185244
  30. The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts.
    Cell. 1988 Jul 1;54(1):27-35 PMID: 3289756
  31. Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers.
    Biophys J. 1995 Mar;68(3):988-96 PMID: 7756561
  32. Nanotubular highways for intercellular organelle transport.
    Science. 2004 Feb 13;303(5660):1007-10 PMID: 14963329
  33. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts.
    Biophys J. 2003 Oct;85(4):2406-16 PMID: 14507704
  34. Microtubules and the endoplasmic reticulum are highly interdependent structures.
    J Cell Biol. 1986 Oct;103(4):1557-68 PMID: 3533956
  35. Nanofluidic networks based on surfactant membrane technology.
    Anal Chem. 2003 Jun 1;75(11):2529-37 PMID: 12948118
  36. Physical measurements of bilayer-skeletal separation forces.
    Ann Biomed Eng. 1995 May-Jun;23(3):308-21 PMID: 7631984
  37. Deformation and flow of membrane into tethers extracted from neuronal growth cones.
    Biophys J. 1996 Jan;70(1):358-69 PMID: 8770212
  38. Tension in tubulovesicular networks of Golgi and endoplasmic reticulum membranes.
    Biophys J. 2004 May;86(5):2923-8 PMID: 15111408
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2005-04-00
Epub
2005-00-04
Pages
2714-26
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1305367
Subset
IM
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