Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion

doi:https://doi.org/10.1038/ncomms8238

Title: Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion

Abstract

Membrane fusion is the core process in membrane trafficking and is essential for cellular transport of proteins and other biomacromolecules. During protein-mediated membrane fusion, membrane proteins are often excluded from the membrane–membrane contact, indicating that local structural transformations in lipid domains play a major role. However, the rearrangements of lipid domains during fusion have not been thoroughly examined. Here using a newly developed Fluorescence Surface Forces Apparatus (FL-SFA), migration of liquid-disordered clusters and depletion of liquid-ordered domains at the membrane–membrane contact are imaged in real time during hemifusion of model lipid membranes, together with simultaneous force–distance and lipid membrane thickness measurements. The load and contact time-dependent hemifusion results show that the domain rearrangements decrease the energy barrier to fusion, illustrating the significance of dynamic domain transformations in membrane fusion processes. Importantly, the FL-SFA can unambiguously correlate interaction forces and in situ imaging in many dynamic interfacial systems.

Authors:

Lee, Dong Woog ^[1]; Kristiansen, Kai ^[1]; Donaldson, Stephen H. ^[1]; Cadirov, Nicholas ^[1]; Banquy, Xavier ^[2]; Israelachvili, Jacob N. ^[3]

Univ. of California, Santa Barbara, CA (United States). Dept. of Chemical Engineering
Univ. of Montreal, QC (Canada). Canada Research Chair in Bio-inspired Materials and Interfaces. Faculty of Pharmacy
Univ. of California, Santa Barbara, CA (United States). Dept. of Chemical Engineering. Dept. of Materials

Publication Date:: 2015-05-26

Research Org.:: Univ. of California, Santa Barbara, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1623977

Grant/Contract Number:: FG02-87ER45331

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Nature Communications

Additional Journal Information:: Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 36 MATERIALS SCIENCE; Membrane lipids; Membrane fusion; Membrane biophysics

Citation Formats


                    Lee, Dong Woog, Kristiansen, Kai, Donaldson, Stephen H., Cadirov, Nicholas, Banquy, Xavier, and Israelachvili, Jacob N. Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion.  United States: N. p., 2015. 
        Web.  doi:10.1038/ncomms8238.

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                    Lee, Dong Woog, Kristiansen, Kai, Donaldson, Stephen H., Cadirov, Nicholas, Banquy, Xavier, & Israelachvili, Jacob N. Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion.  United States.  https://doi.org/10.1038/ncomms8238

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                    Lee, Dong Woog, Kristiansen, Kai, Donaldson, Stephen H., Cadirov, Nicholas, Banquy, Xavier, and Israelachvili, Jacob N. Tue .  
        "Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion".  United States.  https://doi.org/10.1038/ncomms8238.  https://www.osti.gov/servlets/purl/1623977.

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@article{osti_1623977,

  title        = {Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion},

  author       = {Lee, Dong Woog and Kristiansen, Kai and Donaldson, Stephen H. and Cadirov, Nicholas and Banquy, Xavier and Israelachvili, Jacob N.},

  abstractNote = {Membrane fusion is the core process in membrane trafficking and is essential for cellular transport of proteins and other biomacromolecules. During protein-mediated membrane fusion, membrane proteins are often excluded from the membrane–membrane contact, indicating that local structural transformations in lipid domains play a major role. However, the rearrangements of lipid domains during fusion have not been thoroughly examined. Here using a newly developed Fluorescence Surface Forces Apparatus (FL-SFA), migration of liquid-disordered clusters and depletion of liquid-ordered domains at the membrane–membrane contact are imaged in real time during hemifusion of model lipid membranes, together with simultaneous force–distance and lipid membrane thickness measurements. The load and contact time-dependent hemifusion results show that the domain rearrangements decrease the energy barrier to fusion, illustrating the significance of dynamic domain transformations in membrane fusion processes. Importantly, the FL-SFA can unambiguously correlate interaction forces and in situ imaging in many dynamic interfacial systems.},

  doi          = {10.1038/ncomms8238},

  url          = {https://www.osti.gov/biblio/1623977},
  journal      = {Nature Communications},

  issn         = {2041-1723},

  number       = 1,

  volume       = 6,

  place        = {United States},

  year         = {2015},

  month        = {5}

}

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Works referenced in this record:

Lipid Rafts As a Membrane-Organizing Principle
journal, December 2009

Lingwood, D.; Simons, K.
Science, Vol. 327, Issue 5961
https://doi.org/10.1126/science.1174621

SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis
journal, May 2001

Chamberlain, L. H.; Burgoyne, R. D.; Gould, G. W.
Proceedings of the National Academy of Sciences, Vol. 98, Issue 10
https://doi.org/10.1073/pnas.091502398

Lipid Raft Association of SNARE Proteins Regulates Exocytosis in PC12 Cells
journal, March 2005

Salaün, Christine; Gould, Gwyn W.; Chamberlain, Luke H.
Journal of Biological Chemistry, Vol. 280, Issue 20
https://doi.org/10.1074/jbc.M501923200

Membrane Fusion
journal, February 2003

Jahn, Reinhard; Lang, Thorsten; Südhof, Thomas C.
Cell, Vol. 112, Issue 4
https://doi.org/10.1016/S0092-8674(03)00112-0

Roles of lipid rafts in membrane transport
journal, August 2001

Ikonen, Elina
Current Opinion in Cell Biology, Vol. 13, Issue 4
https://doi.org/10.1016/S0955-0674(00)00238-6

Lipid rafts and signal transduction
journal, October 2000

Simons, Kai; Toomre, Derek
Nature Reviews Molecular Cell Biology, Vol. 1, Issue 1
https://doi.org/10.1038/35036052

Localization of Ion Channels to Lipid Raft Domains within the Cardiovascular System
journal, February 2004

O'Connell, K.
Trends in Cardiovascular Medicine, Vol. 14, Issue 2
https://doi.org/10.1016/j.tcm.2003.10.002

Identification of a Common Sphingolipid-binding Domain in Alzheimer, Prion, and HIV-1 Proteins
journal, January 2002

Mahfoud, Radhia; Garmy, Nicolas; Maresca, Marc
Journal of Biological Chemistry, Vol. 277, Issue 13
https://doi.org/10.1074/jbc.M111679200

SNARE proteins and ‘membrane rafts’: SNARE proteins and ‘membrane rafts’
journal, December 2007

Lang, Thorsten
The Journal of Physiology, Vol. 585, Issue 3
https://doi.org/10.1113/jphysiol.2007.134346

SNAREpins: Minimal Machinery for Membrane Fusion
journal, March 1998

Weber, Thomas; Zemelman, Boris V.; McNew, James A.
Cell, Vol. 92, Issue 6
https://doi.org/10.1016/S0092-8674(00)81404-X

Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells
journal, October 2009

Mukai, Atsushi; Kurisaki, Tomohiro; Sato, Satoshi B.
Experimental Cell Research, Vol. 315, Issue 17
https://doi.org/10.1016/j.yexcr.2009.07.010

Mechanisms of membrane fusion: disparate players and common principles
journal, May 2008

Martens, Sascha; McMahon, Harvey T.
Nature Reviews Molecular Cell Biology, Vol. 9, Issue 7
https://doi.org/10.1038/nrm2417

General hydrophobic interaction potential for surfactant/lipid bilayers from direct force measurements between light-modulated bilayers
journal, September 2011

Donaldson, S. H.; Lee, C. T.; Chmelka, B. F.
Proceedings of the National Academy of Sciences, Vol. 108, Issue 38
https://doi.org/10.1073/pnas.1112411108

Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers
journal, November 1989

Helm, C.; Israelachvili, J.; McGuiggan, P.
Science, Vol. 246, Issue 4932
https://doi.org/10.1126/science.2814514

Energetics of stalk intermediates in membrane fusion are controlled by lipid composition
journal, May 2012

Aeffner, S.; Reusch, T.; Weinhausen, B.
Proceedings of the National Academy of Sciences, Vol. 109, Issue 25
https://doi.org/10.1073/pnas.1119442109

Relating domain size distribution to line tension and molecular dipole density in model cytoplasmic myelin lipid monolayers
journal, May 2011

Lee, D. W.; Min, Y.; Dhar, P.
Proceedings of the National Academy of Sciences, Vol. 108, Issue 23
https://doi.org/10.1073/pnas.1106368108

Lipid domains control myelin basic protein adsorption and membrane interactions between model myelin lipid bilayers
journal, February 2014

Lee, D. W.; Banquy, X.; Kristiansen, K.
Proceedings of the National Academy of Sciences, Vol. 111, Issue 8
https://doi.org/10.1073/pnas.1401165111

Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension
journal, October 2003

Baumgart, Tobias; Hess, Samuel T.; Webb, Watt W.
Nature, Vol. 425, Issue 6960
https://doi.org/10.1038/nature02013

Lipid Rafts Reconstituted in Model Membranes
journal, March 2001

Dietrich, C.; Bagatolli, L. A.; Volovyk, Z. N.
Biophysical Journal, Vol. 80, Issue 3
https://doi.org/10.1016/S0006-3495(01)76114-0

Nonequilibrium Behavior in Supported Lipid Membranes Containing Cholesterol
journal, May 2004

Stottrup, Benjamin L.; Veatch, Sarah L.; Keller, Sarah L.
Biophysical Journal, Vol. 86, Issue 5
https://doi.org/10.1016/S0006-3495(04)74345-3

Separation of Liquid Phases in Giant Vesicles of Ternary Mixtures of Phospholipids and Cholesterol
journal, November 2003

Veatch, Sarah L.; Keller, Sarah L.
Biophysical Journal, Vol. 85, Issue 5
https://doi.org/10.1016/S0006-3495(03)74726-2

Role of calcium in the adhesion and fusion of bilayers
journal, February 1993

Leckband, D. E.; Helm, C. A.; Israelachvili, J.
Biochemistry, Vol. 32, Issue 4
https://doi.org/10.1021/bi00055a019

Adhesion and hemifusion of cytoplasmic myelin lipid membranes are highly dependent on the lipid composition
journal, March 2012

Banquy, Xavier; Kristiansen, Kai; Lee, Dong Woog
Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 3
https://doi.org/10.1016/j.bbamem.2011.10.015

Surface Energy and the Contact of Elastic Solids
journal, September 1971

Johnson, K. L.; Kendall, K.; Roberts, A. D.
Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 324, Issue 1558
https://doi.org/10.1098/rspa.1971.0141

Recent progress in understanding hydrophobic interactions
journal, October 2006

Meyer, E. E.; Rosenberg, K. J.; Israelachvili, J.
Proceedings of the National Academy of Sciences, Vol. 103, Issue 43
https://doi.org/10.1073/pnas.0606422103

Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins
journal, March 2009

Sorre, B.; Callan-Jones, A.; Manneville, J. -B.
Proceedings of the National Academy of Sciences, Vol. 106, Issue 14
https://doi.org/10.1073/pnas.0811243106

Recent advances in the surface forces apparatus (SFA) technique
journal, January 2010

Israelachvili, J.; Min, Y.; Akbulut, M.
Reports on Progress in Physics, Vol. 73, Issue 3
https://doi.org/10.1088/0034-4885/73/3/036601

Langmuir-Blodgett films
journal, March 1994

Zasadzinski, J.; Viswanathan, R.; Madsen, L.
Science, Vol. 263, Issue 5154
https://doi.org/10.1126/science.8134836

Works referencing / citing this record:

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation
journal, August 2019

Sugiyama, Ryosuke; Nakatani, Takahiro; Nishimura, Shinichi
Angewandte Chemie, Vol. 131, Issue 38
https://doi.org/10.1002/ange.201905970

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation
journal, September 2019

Sugiyama, Ryosuke; Nakatani, Takahiro; Nishimura, Shinichi
Angewandte Chemie International Edition, Vol. 58, Issue 38
https://doi.org/10.1002/anie.201905970

Additive interfacial chiral interaction in multilayers for stabilization of small individual skyrmions at room temperature
journal, January 2016

Moreau-Luchaire, C.; Moutafis, C.; Reyren, N.
Nature Nanotechnology, Vol. 11, Issue 5
https://doi.org/10.1038/nnano.2015.313

Optimizing multiple beam interferometry in the surface forces apparatus: Novel optics, reflection mode modeling, metal layer thicknesses, birefringence, and rotation of anisotropic layers
journal, April 2019

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Review of Scientific Instruments, Vol. 90, Issue 4
https://doi.org/10.1063/1.5085210

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Title: Real-time intermembrane force measurements and imaging of lipid domain morphology during hemifusion

Abstract

Citation Formats

Lipid Rafts As a Membrane-Organizing Principle journal, December 2009

SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis journal, May 2001

Lipid Raft Association of SNARE Proteins Regulates Exocytosis in PC12 Cells journal, March 2005

Membrane Fusion journal, February 2003

Roles of lipid rafts in membrane transport journal, August 2001

Lipid rafts and signal transduction journal, October 2000

Localization of Ion Channels to Lipid Raft Domains within the Cardiovascular System journal, February 2004

Identification of a Common Sphingolipid-binding Domain in Alzheimer, Prion, and HIV-1 Proteins journal, January 2002

SNARE proteins and ‘membrane rafts’: SNARE proteins and ‘membrane rafts’ journal, December 2007

SNAREpins: Minimal Machinery for Membrane Fusion journal, March 1998

Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells journal, October 2009

Mechanisms of membrane fusion: disparate players and common principles journal, May 2008

General hydrophobic interaction potential for surfactant/lipid bilayers from direct force measurements between light-modulated bilayers journal, September 2011

Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers journal, November 1989

Energetics of stalk intermediates in membrane fusion are controlled by lipid composition journal, May 2012

Relating domain size distribution to line tension and molecular dipole density in model cytoplasmic myelin lipid monolayers journal, May 2011

Lipid domains control myelin basic protein adsorption and membrane interactions between model myelin lipid bilayers journal, February 2014

Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension journal, October 2003

Lipid Rafts Reconstituted in Model Membranes journal, March 2001

Nonequilibrium Behavior in Supported Lipid Membranes Containing Cholesterol journal, May 2004

Separation of Liquid Phases in Giant Vesicles of Ternary Mixtures of Phospholipids and Cholesterol journal, November 2003

Role of calcium in the adhesion and fusion of bilayers journal, February 1993

Adhesion and hemifusion of cytoplasmic myelin lipid membranes are highly dependent on the lipid composition journal, March 2012

Surface Energy and the Contact of Elastic Solids journal, September 1971

Recent progress in understanding hydrophobic interactions journal, October 2006

Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins journal, March 2009

Recent advances in the surface forces apparatus (SFA) technique journal, January 2010

Langmuir-Blodgett films journal, March 1994

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation journal, August 2019

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation journal, September 2019

Additive interfacial chiral interaction in multilayers for stabilization of small individual skyrmions at room temperature journal, January 2016

Optimizing multiple beam interferometry in the surface forces apparatus: Novel optics, reflection mode modeling, metal layer thicknesses, birefringence, and rotation of anisotropic layers journal, April 2019

Lipid Rafts As a Membrane-Organizing Principle
journal, December 2009

SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis
journal, May 2001

Lipid Raft Association of SNARE Proteins Regulates Exocytosis in PC12 Cells
journal, March 2005

Membrane Fusion
journal, February 2003

Roles of lipid rafts in membrane transport
journal, August 2001

Lipid rafts and signal transduction
journal, October 2000

Localization of Ion Channels to Lipid Raft Domains within the Cardiovascular System
journal, February 2004

Identification of a Common Sphingolipid-binding Domain in Alzheimer, Prion, and HIV-1 Proteins
journal, January 2002

SNARE proteins and ‘membrane rafts’: SNARE proteins and ‘membrane rafts’
journal, December 2007

SNAREpins: Minimal Machinery for Membrane Fusion
journal, March 1998

Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells
journal, October 2009

Mechanisms of membrane fusion: disparate players and common principles
journal, May 2008

General hydrophobic interaction potential for surfactant/lipid bilayers from direct force measurements between light-modulated bilayers
journal, September 2011

Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers
journal, November 1989

Energetics of stalk intermediates in membrane fusion are controlled by lipid composition
journal, May 2012

Relating domain size distribution to line tension and molecular dipole density in model cytoplasmic myelin lipid monolayers
journal, May 2011

Lipid domains control myelin basic protein adsorption and membrane interactions between model myelin lipid bilayers
journal, February 2014

Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension
journal, October 2003

Lipid Rafts Reconstituted in Model Membranes
journal, March 2001

Nonequilibrium Behavior in Supported Lipid Membranes Containing Cholesterol
journal, May 2004

Separation of Liquid Phases in Giant Vesicles of Ternary Mixtures of Phospholipids and Cholesterol
journal, November 2003

Role of calcium in the adhesion and fusion of bilayers
journal, February 1993

Adhesion and hemifusion of cytoplasmic myelin lipid membranes are highly dependent on the lipid composition
journal, March 2012

Surface Energy and the Contact of Elastic Solids
journal, September 1971

Recent progress in understanding hydrophobic interactions
journal, October 2006

Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins
journal, March 2009

Recent advances in the surface forces apparatus (SFA) technique
journal, January 2010

Langmuir-Blodgett films
journal, March 1994

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation
journal, August 2019

Chemical Interactions of Cryptic Actinomycete Metabolite 5‐Alkyl‐1,2,3,4‐tetrahydroquinolines through Aggregate Formation
journal, September 2019

Additive interfacial chiral interaction in multilayers for stabilization of small individual skyrmions at room temperature
journal, January 2016

Optimizing multiple beam interferometry in the surface forces apparatus: Novel optics, reflection mode modeling, metal layer thicknesses, birefringence, and rotation of anisotropic layers
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