Method for measuring the unbinding energy of strongly-bound membrane-associated proteins

La Bauve, Elisa; Vernon, Briana C.; Ye, Dongmei; Rogers, David M.; Siegrist, Cathryn M.; Carson, Bryan D.; Rempe, Susan B.; Zheng, Aihua; Kielian, Margaret; Shreve, Andrew P.; Kent, Michael S.

doi:10.1016/j.bbamem.2016.07.004

Title: Method for measuring the unbinding energy of strongly-bound membrane-associated proteins

Journal Article · Tue Nov 01 00:00:00 EDT 2016 · Biochimica et Biophysica Acta. Biomembranes

DOI:https://doi.org/10.1016/j.bbamem.2016.07.004· OSTI ID:1406383

La Bauve, Elisa; Vernon, Briana C.; Ye, Dongmei; Rogers, David M.; Siegrist, Cathryn M.; Carson, Bryan D.; Rempe, Susan B.; Zheng, Aihua; Kielian, Margaret; Shreve, Andrew P.; Kent, Michael S.

Here, we describe a new method to measure the activation energy for unbinding (enthalpy ΔH*_u and free energy ΔG*_u) of a strongly-bound membrane-associated protein from a lipid membrane. It is based on measuring the rate of release of a liposome-bound protein during centrifugation on a sucrose gradient as a function of time and temperature. The method is used to determine ΔH*u and ΔG*u for the soluble dengue virus envelope protein (sE) strongly bound to 80:20 POPC:POPG liposomes at pH 5.5. ΔH*u is determined from the Arrhenius equation whereas ΔG*u is determined by fitting the data to a model based on mean first passage time for escape from a potential well. The binding free energy ΔG_b of sE was also measured at the same pH for the initial, predominantly reversible, phase of binding to a 70:30 PC:PG lipid bilayer. The unbinding free energy (20 ± 3 kcal/mol, 20% PG) was found to be roughly three times the binding energy per monomer, (7.8 ± 0.3 kcal/mol for 30% PG, or est. 7.0 kcal/mol for 20% PG). This is consistent with data showing that free sE is a monomer at pH 5.5, but assembles into trimers after associating with membranes. Furthermore, this new method to determine unbinding energies should be useful to understand better the complex interactions of integral monotopic proteins and strongly-bound peripheral membrane proteins with lipid membranes.

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Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1406383

Alternate ID(s):: OSTI ID: 1397547; OSTI ID: 1411226

Report Number(s):: SAND2017-11814J; S0005273616302474; PII: S0005273616302474

Journal Information:: Biochimica et Biophysica Acta. Biomembranes, Journal Name: Biochimica et Biophysica Acta. Biomembranes Vol. 1858 Journal Issue: 11; ISSN 0005-2736

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 1 work

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References (58)

Quantitative Characterization of Membrane Binding of Peripheral Proteins by Spin-Label EPR Spectroscopy Tatulian, Suren A. The Journal of Physical Chemistry B, Vol. 106, Issue 34 https://doi.org/10.1021/jp026052n	journal	August 2002
Strength of Integration of Transmembrane α-Helical Peptides in Lipid Bilayers As Determined by Atomic Force Spectroscopy ^† Ganchev, Dragomir N.; Rijkers, Dirk T. S.; Snel, Margot M. E. Biochemistry, Vol. 43, Issue 47 https://doi.org/10.1021/bi048372y	journal	November 2004
C2 Domain of Protein Kinase Cα: Elucidation of the Membrane Docking Surface by Site-Directed Fluorescence and Spin Labeling ^† Kohout, Susy C.; Corbalán-García, Senena; Gómez-Fernández, Juan C. Biochemistry, Vol. 42, Issue 5 https://doi.org/10.1021/bi026596f	journal	February 2003
Optimizing the Interfacial Binding and Activity of a Bacterial Phosphatidylinositol-specific Phospholipase C Feng, Jianwen; Bradley, William D.; Roberts, Mary F. Journal of Biological Chemistry, Vol. 278, Issue 27 https://doi.org/10.1074/jbc.M301207200	journal	July 2003
Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins Resh, Marilyn D. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1451, Issue 1 https://doi.org/10.1016/S0167-4889(99)00075-0	journal	August 1999
Trp ²⁰⁶³ and Trp ²⁰⁶⁴ in the Factor Va C2 Domain Are Required for High-Affinity Binding to Phospholipid Membranes but Not for Assembly of the Prothrombinase Complex ^† Peng, Weimin; Quinn-Allen, Mary Ann; Kim, Suhng Wook Biochemistry, Vol. 43, Issue 14 https://doi.org/10.1021/bi035763o	journal	April 2004
Mapping the Interfacial Binding Surface of Human Secretory Group IIa Phospholipase A ₂ ^† Snitko, Yana; Koduri, Rao S.; Han, Sang K. Biochemistry, Vol. 36, Issue 47 https://doi.org/10.1021/bi971200z	journal	November 1997
Differential Association of the Pleckstrin Homology Domains of Phospholipases C-β ₁ , C-β ₂ , and C-δ ₁ with Lipid Bilayers and the βγ Subunits of Heterotrimeric G Proteins ^† Wang, Tieli; Pentyala, Srinivas; Rebecchi, Mario J. Biochemistry, Vol. 38, Issue 5 https://doi.org/10.1021/bi982008f	journal	February 1999
Kinetics and Thermodynamics of Annexin A1 Binding to Solid-Supported Membranes: A QCM Study ^† Kastl, Katja; Ross, Michaela; Gerke, Volker Biochemistry, Vol. 41, Issue 31 https://doi.org/10.1021/bi025951z	journal	August 2002
Anisotropic Solvent Model of the Lipid Bilayer. 2. Energetics of Insertion of Small Molecules, Peptides, and Proteins in Membranes Lomize, Andrei L.; Pogozheva, Irina D.; Mosberg, Henry I. Journal of Chemical Information and Modeling, Vol. 51, Issue 4 https://doi.org/10.1021/ci200020k	journal	March 2011
A Stable Prefusion Intermediate of the Alphavirus Fusion Protein Reveals Critical Features of Class II Membrane Fusion Sánchez-San Martín, Claudia; Sosa, Hernando; Kielian, Margaret Cell Host & Microbe, Vol. 4, Issue 6 https://doi.org/10.1016/j.chom.2008.10.012	journal	December 2008
Some mean first-passage time approximations for the Ornstein-Uhlenbeck process Thomas, Marlin U. Journal of Applied Probability, Vol. 12, Issue 3 https://doi.org/10.2307/3212877	journal	September 1975
Mechanism of Actin Filament Turnover by Severing and Nucleation at Different Concentrations of ADF/Cofilin Andrianantoandro, Ernesto; Pollard, Thomas D. Molecular Cell, Vol. 24, Issue 1 https://doi.org/10.1016/j.molcel.2006.08.006	journal	October 2006
Structure of the dengue virus envelope protein after membrane fusion Modis, Yorgo; Ogata, Steven; Clements, David Nature, Vol. 427, Issue 6972 https://doi.org/10.1038/nature02165	journal	January 2004
Studies on the membrane interactions of the cyclotides kalata B1 and kalata B6 on model membrane systems by surface plasmon resonance Kamimori, Hiroshi; Hall, Kristopher; Craik, David J. Analytical Biochemistry, Vol. 337, Issue 1 https://doi.org/10.1016/j.ab.2004.10.028	journal	February 2005
Molecular basis of endosomal-membrane association for the dengue virus envelope protein Rogers, David M.; Kent, Michael S.; Rempe, Susan B. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1848, Issue 4 https://doi.org/10.1016/j.bbamem.2014.12.018	journal	April 2015
Investigation of Membrane Disruption in the Reaction Catalyzed by Cholesterol Oxidase ^† Ghoshroy, Kajal Bose; Zhu, Weiqun; Sampson, Nicole S. Biochemistry, Vol. 36, Issue 20 https://doi.org/10.1021/bi962190p	journal	May 1997
In Vitro and In Vivo Studies Identify Important Features of Dengue Virus pr-E Protein Interactions Zheng, Aihua; Umashankar, Mahadevaiah; Kielian, Margaret PLoS Pathogens, Vol. 6, Issue 10 https://doi.org/10.1371/journal.ppat.1001157	journal	October 2010
Two-step Membrane Binding by Equinatoxin II, a Pore-forming Toxin from the Sea Anemone, Involves an Exposed Aromatic Cluster and a Flexible Helix Hong, Qi; Gutiérrez-Aguirre, Ion; Barlič, Ariana Journal of Biological Chemistry, Vol. 277, Issue 44 https://doi.org/10.1074/jbc.M204625200	journal	August 2002
On the Binding Preference of Human Groups IIA and X Phospholipases A2 for Membranes with Anionic Phospholipids Bezzine, Sofiane; Bollinger, James G.; Singer, Alan G. Journal of Biological Chemistry, Vol. 277, Issue 50 https://doi.org/10.1074/jbc.M203137200	journal	December 2002
Interfacial Binding of Bee Venom Secreted Phospholipase A ₂ to Membranes Occurs Predominantly by a Nonelectrostatic Mechanism ^† Bollinger, James G.; Diraviyam, Karthikeyan; Ghomashchi, Farideh Biochemistry, Vol. 43, Issue 42 https://doi.org/10.1021/bi049390i	journal	October 2004
The Molecular Basis of the Differential Subcellular Localization of FYVE Domains Blatner, Nichole R.; Stahelin, Robert V.; Diraviyam, Karthikeyan Journal of Biological Chemistry, Vol. 279, Issue 51 https://doi.org/10.1074/jbc.M408408200	journal	December 2004
Quartz crystal microbalance with dissipation monitoring of supported lipid bilayers on various substrates Cho, Nam-Joon; Frank, Curtis W.; Kasemo, Bengt Nature Protocols, Vol. 5, Issue 6 https://doi.org/10.1038/nprot.2010.65	journal	May 2010
Membrane Fusion Activity of Semliki Forest Virus in a Liposomal Model System: Specific Inhibition by Zn2+Ions Corver, Jeroen; Bron, Romke; Snippe, Harm Virology, Vol. 238, Issue 1 https://doi.org/10.1006/viro.1997.8799	journal	November 1997
Interaction of cytochrome c and its precursor apocytochrome c with various phospholipids Rietveld, A.; Sijens, P.; Verkleij, A. J. The EMBO Journal, Vol. 2, Issue 6 https://doi.org/10.1002/j.1460-2075.1983.tb01520.x	journal	June 1983
Characterization of a Structural Intermediate of Flavivirus Membrane Fusion Stiasny, Karin; Kössl, Christian; Lepault, Jean PLoS Pathogens, Vol. 3, Issue 2 https://doi.org/10.1371/journal.ppat.0030020	journal	February 2007
Insights from the X-ray Crystal Structure of Coral 8R-Lipoxygenase Oldham, Michael L.; Brash, Alan R.; Newcomer, Marcia E. Journal of Biological Chemistry, Vol. 280, Issue 47 https://doi.org/10.1074/jbc.M506675200	journal	November 2005
Arf1-GTP-induced Tubule Formation Suggests a Function of Arf Family Proteins in Curvature Acquisition at Sites of Vesicle Budding Krauss, Michael; Jia, Jun-Yong; Roux, Aurélien Journal of Biological Chemistry, Vol. 283, Issue 41 https://doi.org/10.1074/jbc.M804528200	journal	October 2008
A simple guide to biochemical approaches for analyzing protein–lipid interactions Zhao, Hongxia; Lappalainen, Pekka Molecular Biology of the Cell, Vol. 23, Issue 15 https://doi.org/10.1091/mbc.e11-07-0645	journal	August 2012
Exponential trends of Ornstein–Uhlenbeck first-passage-time densities Nobile, A. G.; Ricciardi, L. M.; Sacerdote, L. Journal of Applied Probability, Vol. 22, Issue 2 https://doi.org/10.2307/3213779	journal	June 1985
Cholesterol Oxidase Senses Subtle Changes in Lipid Bilayer Structure ^† Ahn, Kwang-wook; Sampson, Nicole S. Biochemistry, Vol. 43, Issue 3 https://doi.org/10.1021/bi035697q	journal	January 2004
Introductory Lecture Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy Evans, Evan Faraday Discussions, Vol. 111 https://doi.org/10.1039/a809884k	journal	January 1999
N-Terminal Hydrophobic Residues of the G-Protein ADP-Ribosylation Factor-1 Insert into Membrane Phospholipids upon GDP to GTP Exchange ^† Antonny, Bruno; Beraud-Dufour, Sophie; Chardin, Pierre Biochemistry, Vol. 36, Issue 15 https://doi.org/10.1021/bi962252b	journal	April 1997
Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles Ben-Tal, N.; Honig, B.; Miller, C. Biophysical Journal, Vol. 73, Issue 4 https://doi.org/10.1016/S0006-3495(97)78203-1	journal	October 1997
In Vitro Reconstitution Reveals Key Intermediate States of Trimer Formation by the Dengue Virus Membrane Fusion Protein Liao, M.; Martin, C. S. S.; Zheng, A. Journal of Virology, Vol. 84, Issue 11 https://doi.org/10.1128/JVI.00170-10	journal	March 2010
Viral membrane fusion Harrison, Stephen C. Nature Structural & Molecular Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nsmb.1456	journal	July 2008
Characterization of Supported Lipid Bilayer Disruption By Chrysophsin-3 Using QCM-D Wang, Kathleen F.; Nagarajan, Ramanathan; Mello, Charlene M. The Journal of Physical Chemistry B, Vol. 115, Issue 51 https://doi.org/10.1021/jp209658y	journal	December 2011
Differential Cholesterol Binding by Class II Fusion Proteins Determines Membrane Fusion Properties Umashankar, M.; Sánchez-San Martín, Claudia; Liao, Maofu Journal of Virology, Vol. 82, Issue 18 https://doi.org/10.1128/JVI.00975-08	journal	July 2008
Penetration of a cardiotoxin into cardiolipin model membranes and its implications on lipid organization Batenburg, A. M.; Bougis, P. E.; Rochat, H. Biochemistry, Vol. 24, Issue 25 https://doi.org/10.1021/bi00346a013	journal	December 1985
Contrasting Membrane Interaction Mechanisms of AP180 N-terminal Homology (ANTH) and Epsin N-terminal Homology (ENTH) Domains Stahelin, Robert V.; Long, Fei; Peter, Brian J. Journal of Biological Chemistry, Vol. 278, Issue 31 https://doi.org/10.1074/jbc.M302865200	journal	August 2003
A Structure-Function Study of the C2 Domain of Cytosolic Phospholipase A ₂ : IDENTIFICATION OF ESSENTIAL CALCIUM LIGANDS AND HYDROPHOBIC MEMBRANE BINDING RESIDUES Bittova, Lenka; Sumandea, Marius; Cho, Wonhwa Journal of Biological Chemistry, Vol. 274, Issue 14 https://doi.org/10.1074/jbc.274.14.9665	journal	April 1999
Membrane-binding and activation mechanism of PTEN Das, S.; Dixon, J. E.; Cho, W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13 https://doi.org/10.1073/pnas.0932835100	journal	June 2003
Phospholipase A2 at the bilayer interface Ramirez, Fausto; Jain, Mahendra Kumar Proteins: Structure, Function, and Genetics, Vol. 9, Issue 4 https://doi.org/10.1002/prot.340090402	journal	April 1991
Transient Convection, Diffusion, and Adsorption in Surface-Based Biosensors Hansen, Rasmus; Bruus, Henrik; Callisen, Thomas H. Langmuir, Vol. 28, Issue 19 https://doi.org/10.1021/la3000763	journal	May 2012
Solution Structure and Lipid Membrane Partitioning of VSTx1, an Inhibitor of the KvAP Potassium Channel ^† ^, ^‡ Jung, Hoi Jong; Lee, Ju Yeon; Kim, Su Hwan Biochemistry, Vol. 44, Issue 16 https://doi.org/10.1021/bi0477034	journal	April 2005
Evaluation of liposome populations using a sucrose density gradient centrifugation approach coupled to a continuous flow system Sánchez-López, V.; Fernández-Romero, J. M.; Gómez-Hens, A. Analytica Chimica Acta, Vol. 645, Issue 1-2 https://doi.org/10.1016/j.aca.2009.04.045	journal	July 2009
Use of the Parallax-Quench Method to Determine the Position of the Active-Site Loop of Cholesterol Oxidase in Lipid Bilayers ^† Chen, Xiaoyu; Wolfgang, David E.; Sampson, Nicole S. Biochemistry, Vol. 39, Issue 44 https://doi.org/10.1021/bi001407j	journal	November 2000
Membrane Fluidity Is a Key Modulator of Membrane Binding, Insertion, and Activity of 5-Lipoxygenase Pande, Abhay H.; Qin, Shan; Tatulian, Suren A. Biophysical Journal, Vol. 88, Issue 6 https://doi.org/10.1529/biophysj.104.056788	journal	June 2005
Trafficking and signaling by fatty-acylated and prenylated proteins Resh, Marilyn D. Nature Chemical Biology, Vol. 2, Issue 11 https://doi.org/10.1038/nchembio834	journal	October 2006
Dengue Virus Ensures Its Fusion in Late Endosomes Using Compartment-Specific Lipids Zaitseva, Elena; Yang, Sung-Tae; Melikov, Kamran PLoS Pathogens, Vol. 6, Issue 10 https://doi.org/10.1371/journal.ppat.1001131	journal	October 2010
Viscoelastic Acoustic Response of Layered Polymer Films at Fluid-Solid Interfaces: Continuum Mechanics Approach Voinova, M. V.; Rodahl, M.; Jonson, M. Physica Scripta, Vol. 59, Issue 5 https://doi.org/10.1238/Physica.Regular.059a00391	journal	May 1999
Amphitropic proteins: regulation by reversible membrane interactions (Review) Johnson, Joanne E.; Cornell, Rosemary B. Molecular Membrane Biology, Vol. 16, Issue 3 https://doi.org/10.1080/096876899294544	journal	January 1999
Structural Basis for Endosomal Targeting by FYVE Domains Hayakawa, Akira; Hayes, Susan J.; Lawe, Deirdre C. Journal of Biological Chemistry, Vol. 279, Issue 7 https://doi.org/10.1074/jbc.M310503200	journal	February 2004
Membrane-bending proteins Prinz, William A.; Hinshaw, Jenny E. Critical Reviews in Biochemistry and Molecular Biology, Vol. 44, Issue 5 https://doi.org/10.1080/10409230903183472	journal	July 2009
Binding of acylated peptides and fatty acids to phospholipid vesicles: Pertinence to myristoylated proteins Peitzsch, Robert M.; McLaughlin, Stuart Biochemistry, Vol. 32, Issue 39 https://doi.org/10.1021/bi00090a020	journal	October 1993
Dealing with low pH: entry and exit of alphaviruses and flaviviruses Martín, Claudia Sánchez-San; Liu, Catherine Y.; Kielian, Margaret Trends in Microbiology, Vol. 17, Issue 11 https://doi.org/10.1016/j.tim.2009.08.002	journal	November 2009
Membrane Interactions of the Tick-Borne Encephalitis Virus Fusion Protein E at Low pH Stiasny, Karin; Allison, Steven L.; Schalich, Juliane Journal of Virology, Vol. 76, Issue 8 https://doi.org/10.1128/JVI.76.8.3784-3790.2002	journal	April 2002
Differential Roles of Ionic, Aliphatic, and Aromatic Residues in Membrane−Protein Interactions: A Surface Plasmon Resonance Study on Phospholipases A ₂ ^† Stahelin, Robert V.; Cho, Wonhwa Biochemistry, Vol. 40, Issue 15 https://doi.org/10.1021/bi0020325	journal	April 2001

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