Incorporation of Membrane Proteins Into Bicontinuous Microemulsions Through Winsor‐III System‐Based Extraction

Hayes, Douglas G.; Anunciado, Divina B.; Ye, Ran; Williams, Rachel N. D.; O'Neill, Hugh M.; Pingali, Sai Venkatesh; Urban, Volker S.

doi:10.1002/jsde.12500

Title: Incorporation of Membrane Proteins Into Bicontinuous Microemulsions Through Winsor‐III System‐Based Extraction

Journal Article · Sun Mar 14 00:00:00 EST 2021 · Journal of Surfactants and Detergents

DOI:https://doi.org/10.1002/jsde.12500· OSTI ID:1786536

^[1];

^[2];

^[1]; Williams, Rachel N. D. ^[3];

^[3];

^[3]

Department of Biosystems Engineering and Soil Science University of Tennessee Knoxville TN 37996 USA
Neutron Scattering Division Oak Ridge National Laboratory 1 Bethel Valley Road Oak Ridge TN 37831 USA, Pfizer, Purification Process Development Andover MA 01810 USA
Neutron Scattering Division Oak Ridge National Laboratory 1 Bethel Valley Road Oak Ridge TN 37831 USA

Abstract The membrane proteins (MP) α‐synuclein (ASYN) and bacteriorhodopsin (BR) were readily incorporated into bicontinuous microemulsions (BμEs) formed by two microemulsion systems: water/heptane/Aerosol‐OT (AOT)/CK‐2,13 and water/dodecane/sodium dodecyl sulfate (SDS)/1‐pentanol. (CK‐2,13 is an alkyl ethoxylate possessing two alkyl tail groups of carbon chain length 2 and 13 and an average degree of ethoxylation of 5.6.) MP were encapsulated in BμEs through preparation of Winsor‐III systems at optimal salinity, with the anionic surfactants AOT and SDS providing the driving force for extraction. Dissolution of ASYN in BμEs greatly increased the former's α‐helicity, similar to ASYN's behavior in the presence of biomembranes, while BμE‐ and vesicle‐encapsulated BR possessed similar secondary structure. Small‐angle neutron scattering (SANS) results clearly demonstrated the direct interaction of MP with the surfactants, resulting in a decrease of surface area per volume for surfactant monolayers due to decreased surfactant efficiency. The SANS signal for ASYN was isolated through the use of neutron contrast matching for the surfactants through partial deuteration of water and oil, one of the first reports of contrast matching for BμEs in the literature. The SANS results of the contrast‐matched sample reflected similar aggregation for ASYN in BμEs as was reported previously for vesicles and SDS solution. This study demonstrates the potential use of BμEs as MP host systems for conducting biochemical reactions such as the conversion of sunlight into adenosine triphosphate by BR and studying the fundamental behavior of MP, such as the role of ASYN dysfunction in Parkinson's disease, as well as for isolation and purification of MP via Winsor‐III‐based extraction.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1786536

Journal Information:: Journal of Surfactants and Detergents, Journal Name: Journal of Surfactants and Detergents Vol. 24 Journal Issue: 4; ISSN 1097-3958

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United States

Language:: English

References (54)

α-Synuclein – Regulator of Exocytosis, Endocytosis, or Both? Lautenschläger, Janin; Kaminski, Clemens F.; Kaminski Schierle, Gabriele S. Trends in Cell Biology, Vol. 27, Issue 7 https://doi.org/10.1016/j.tcb.2017.02.002	journal	July 2017
Biomimetic hybrid membranes: incorporation of transport proteins/peptides into polymer supports Puiggalí-Jou, Anna; del Valle, Luis J.; Alemán, Carlos Soft Matter, Vol. 15, Issue 13 https://doi.org/10.1039/C8SM02513D	journal	January 2019
Purification and biochemical characterization of photo-active membrane protein bacteriorhodopsin from Haloarcula marismortui, an extreme halophile from the Dead Sea Alsafadi, Diya; Khalili, Fawwaz I.; Juwhari, Hassan International Journal of Biological Macromolecules, Vol. 118 https://doi.org/10.1016/j.ijbiomac.2018.07.045	journal	October 2018
Synergism in binary mixtures of surfactants Hua, Xi Yuan; Rosen, Milton J. Journal of Colloid and Interface Science, Vol. 90, Issue 1 https://doi.org/10.1016/0021-9797(82)90414-3	journal	November 1982
Dynamic structural flexibility of α-synuclein Mor, Danielle E.; Ugras, Scott E.; Daniels, Malcolm J. Neurobiology of Disease, Vol. 88 https://doi.org/10.1016/j.nbd.2015.12.018	journal	April 2016
Effect of multiple scattering on SANS spectra from bicontinuous microemulsions Silas, James A.; Kaler, Eric W. Journal of Colloid and Interface Science, Vol. 257, Issue 2 https://doi.org/10.1016/S0021-9797(02)00059-0	journal	January 2003
Protein extraction by Winsor-III microemulsion systems Gomez del Rio, Javier A.; Hayes, Douglas G. Biotechnology Progress, Vol. 27, Issue 4 https://doi.org/10.1002/btpr.611	journal	June 2011
The human transmembrane proteome Dobson, László; Reményi, István; Tusnády, Gábor E. Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0061-x	journal	May 2015
Molecular mechanism of vectorial proton translocation by bacteriorhodopsin Subramaniam, Sriram; Henderson, Richard Nature, Vol. 406, Issue 6796 https://doi.org/10.1038/35020614	journal	August 2000
Structure, viscoelasticity, and interfacial dynamics of a model polymeric bicontinuous microemulsion Hickey, Robert J.; Gillard, Timothy M.; Irwin, Matthew T. Soft Matter, Vol. 12, Issue 1 https://doi.org/10.1039/C5SM02009C	journal	January 2016
Synergism in binary mixtures of surfactants: II. Some experimental data Rosen, M. J.; Hua, X. Y. Journal of the American Oil Chemists' Society, Vol. 59, Issue 12 https://doi.org/10.1007/BF02636329	journal	December 1982
Removal of non-ionic organic pollutants from water via liquid–liquid extraction López-Montilla, Juan C.; Pandey, Samir; Shah, Dinesh O. Water Research, Vol. 39, Issue 9 https://doi.org/10.1016/j.watres.2005.02.018	journal	May 2005
Effect of Protein Incorporation on the Nanostructure of the Bicontinuous Microemulsion Phase of Winsor-III Systems: A Small-Angle Neutron Scattering Study Hayes, Douglas G.; Gomez del Rio, Javier A.; Ye, Ran Langmuir, Vol. 31, Issue 6 https://doi.org/10.1021/la504606x	journal	February 2015
How to Use the Normalized Hydrophilic-Lipophilic Deviation (HLDN) Concept for the Formulation of Equilibrated and Emulsified Surfactant-Oil-Water Systems for Cosmetics and Pharmaceutical Products Salager, Jean-Louis; Antón, Raquel; Bullón, Johnny Cosmetics, Vol. 7, Issue 3 https://doi.org/10.3390/cosmetics7030057	journal	July 2020
Mass fractal dimension and the compactness of proteins Enright, Matthew B.; Leitner, David M. Physical Review E, Vol. 71, Issue 1 https://doi.org/10.1103/PhysRevE.71.011912	journal	January 2005
Partitioning behavior of an acid-cleavable, 1,3-dioxolane alkyl ethoxylate, surfactant in single and binary surfactant mixtures for 2- and 3-phase microemulsion systems according to ethoxylate head group size Rio, Javier Gomez del; Hayes, Douglas G.; Urban, Volker S. Journal of Colloid and Interface Science, Vol. 352, Issue 2 https://doi.org/10.1016/j.jcis.2010.08.076	journal	December 2010
Activity of squalene-hopene cyclases in bicontinuous microemulsions Steudle, Anne K.; Nestl, Bettina M.; Hauer, Bernhard Colloids and Surfaces B: Biointerfaces, Vol. 135 https://doi.org/10.1016/j.colsurfb.2015.08.034	journal	November 2015
The critical micelle concentration of sodium dodecyl sulfate-bivalent metal dodecyl sulfate mixtures in aqueous solutions Moroi, Yoshikiyo; Motomura, Kinsi; Matuura, Ryohei Journal of Colloid and Interface Science, Vol. 46, Issue 1 https://doi.org/10.1016/0021-9797(74)90030-7	journal	January 1974
Current problems and future avenues in proteoliposome research Amati, Andrea Marco; Graf, Simone; Deutschmann, Sabina Biochemical Society Transactions, Vol. 48, Issue 4 https://doi.org/10.1042/BST20190966	journal	August 2020
Electrochemistry in bicontinuous microemulsions based on control of dynamic solution structures on electrode surfaces Kunitake, Masashi; Kuraya, Eisuke; Kato, Dai Current Opinion in Colloid & Interface Science, Vol. 25 https://doi.org/10.1016/j.cocis.2016.05.004	journal	October 2016
Large scale preparation of homogeneous bacteriorhodopsin Lorber, Bernard; DeLucas, Larry J. FEBS Letters, Vol. 261, Issue 1 https://doi.org/10.1016/0014-5793(90)80625-S	journal	February 1990
A new method for purification of recombinant human α-synuclein in Escherichia coli Huang, Chunjuan; Ren, Guoping; Zhou, Hui Protein Expression and Purification, Vol. 42, Issue 1 https://doi.org/10.1016/j.pep.2005.02.014	journal	July 2005
Production of membrane proteins in industry: The example of GPCRs Errey, James C.; Fiez-Vandal, Cédric Protein Expression and Purification, Vol. 169 https://doi.org/10.1016/j.pep.2020.105569	journal	May 2020
Synthesis of pH-Degradable Nonionic Surfactants and Their Applications in Microemulsions Iyer, Maithili; Hayes, Douglas G.; Harris, J. Milton Langmuir, Vol. 17, Issue 22 https://doi.org/10.1021/la010494t	journal	October 2001
Purification of a Membrane Protein with Conjugated Engineered Micelles Patchornik, Guy; Danino, Dganit; Kesselman, Ellina Bioconjugate Chemistry, Vol. 24, Issue 7 https://doi.org/10.1021/bc400069w	journal	June 2013
Confinement Effects in Block Copolymer Modified Bicontinuous Microemulsions Maccarrone, Simona; Byelov, Dmytro V.; Auth, Thorsten The Journal of Physical Chemistry B, Vol. 117, Issue 18 https://doi.org/10.1021/jp402825d	journal	April 2013
Scattering intensity of bicontinuous microemulsions and sponge phases Peltomäki, Matti; Gompper, Gerhard; Kroll, Daniel M. The Journal of Chemical Physics, Vol. 136, Issue 13 https://doi.org/10.1063/1.3701265	journal	April 2012
Bicontinuous microemulsions as a biomembrane mimetic system for melittin Hayes, Douglas G.; Ye, Ran; Dunlap, Rachel N. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 2 https://doi.org/10.1016/j.bbamem.2017.11.005	journal	February 2018
Small‐angle neutron scattering from microemulsions near the disorder line in water/formamide–octane‐C _i E _j systems Schubert, K. ‐V.; Strey, R. The Journal of Chemical Physics, Vol. 95, Issue 11 https://doi.org/10.1063/1.461282	journal	December 1991
One-step purification of delipidated Bacteriorhodopsin by aqueous-three-phase system from purple membrane of Halobacterium Shiu, Pei-Jiun; Chen, Hsiu-Mei; Lee, Cheng-Kang Food and Bioproducts Processing, Vol. 92, Issue 2 https://doi.org/10.1016/j.fbp.2014.01.003	journal	April 2014
Small-angle neutron scattering reveals the assembly of alpha-synuclein in lipid membranes Anunciado, Divina; Rai, Durgesh K.; Qian, Shuo Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 12 https://doi.org/10.1016/j.bbapap.2015.08.009	journal	December 2015
Approximations Leading to a Unified Exponential/Power-Law Approach to Small-Angle Scattering Beaucage, G. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895005292	journal	December 1995
Available Know-how in Transforming an Emulsified Drilling Fluid To Be Removed from an Unwanted Location into a Low-Viscosity Single-Phase System Salager, Jean-Louis; Forgiarini, Ana María; Antón, Raquel Elena Energy & Fuels, Vol. 26, Issue 7 https://doi.org/10.1021/ef300260v	journal	April 2012
Measuring bending rigidity and spatial renormalization in bicontinuous microemulsions Gompper, G.; Endo, H.; Mihailescu, M. Europhysics Letters (EPL), Vol. 56, Issue 5 https://doi.org/10.1209/epl/i2001-00574-3	journal	December 2001
α-synuclein toxicity in neurodegeneration: mechanism and therapeutic strategies Wong, Yvette C.; Krainc, Dimitri Nature Medicine, Vol. 23, Issue 2 https://doi.org/10.1038/nm.4269	journal	February 2017
Triacylglycerol microemulsions stabilized by alkyl ethoxylate surfactants—A basic study Engelskirchen, S.; Elsner, N.; Sottmann, T. Journal of Colloid and Interface Science, Vol. 312, Issue 1 https://doi.org/10.1016/j.jcis.2006.09.022	journal	August 2007
Current strategies for protein production and purification enabling membrane protein structural biology Pandey, Aditya; Shin, Kyungsoo; Patterson, Robin E. Biochemistry and Cell Biology, Vol. 94, Issue 6 https://doi.org/10.1139/bcb-2015-0143	journal	December 2016
Experimental determination of bending rigidity and saddle splay modulus in bicontinuous microemulsions Holderer, Olaf; Frielinghaus, Henrich; Monkenbusch, Michael Soft Matter, Vol. 9, Issue 7 https://doi.org/10.1039/c2sm27449c	journal	January 2013
Temperature dependence of the surfactant film bending elasticity in a bicontinuous sugar surfactant based microemulsion: a quasielastic scattering study Wellert, Stefan; Karg, Matthias; Holderer, Olaf Phys. Chem. Chem. Phys., Vol. 13, Issue 8 https://doi.org/10.1039/C0CP02044C	journal	January 2011
Silicone Microemulsion Structures Are Maintained During Polymerization with Reactive Surfactants Whinton, Marlena; Hughes, Timothy C.; Peng, Shuhua Langmuir, Vol. 34, Issue 14 https://doi.org/10.1021/acs.langmuir.8b00240	journal	March 2018
Reduction and analysis of SANS and USANS data using IGOR Pro Kline, Steven R. Journal of Applied Crystallography, Vol. 39, Issue 6, p. 895-900 https://doi.org/10.1107/S0021889806035059	journal	November 2006
Protein extraction into the bicontinuous microemulsion phase of a Water/SDS/pentanol/dodecane winsor-III system: Effect on nanostructure and protein conformation Hayes, Douglas G.; Ye, Ran; Dunlap, Rachel N. Colloids and Surfaces B: Biointerfaces, Vol. 160 https://doi.org/10.1016/j.colsurfb.2017.09.005	journal	December 2017
Reconstitution of Membrane Proteins into Model Membranes: Seeking Better Ways to Retain Protein Activities Shen, Hsin-Hui; Lithgow, Trevor; Martin, Lisa International Journal of Molecular Sciences, Vol. 14, Issue 1 https://doi.org/10.3390/ijms14011589	journal	January 2013
Membrane protein nanoparticles: the shape of things to come Simon, Kailene S.; Pollock, Naomi L.; Lee, Sarah C. Biochemical Society Transactions, Vol. 46, Issue 6 https://doi.org/10.1042/BST20180139	journal	November 2018
UV-LED induced bicontinuous microemulsions polymerisation for surface modification of commercial membranes – Enhancing the antifouling properties Galiano, Francesco; André Schmidt, Stefan; Ye, Xiaoyun Separation and Purification Technology, Vol. 194 https://doi.org/10.1016/j.seppur.2017.10.063	journal	April 2018
Small angle neutron scattering near Lifshitz lines: Transition from weakly structured mixtures to microemulsions Schubert, K. ‐V.; Strey, R.; Kline, S. R. The Journal of Chemical Physics, Vol. 101, Issue 6 https://doi.org/10.1063/1.467387	journal	September 1994
Protein Data Bank: the single global archive for 3D macromolecular structure data Burley, Stephen K.; Berman, Helen M.; Bhikadiya, Charmi Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky949	journal	October 2018
The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory Heller, William T.; Urban, Volker S.; Lynn, Gary W. Journal of Applied Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S1600576714011285	journal	June 2014
Segregation of Amphiphilic Polymer-Coated Nanoparticles to Bicontinuous Oil/Water Microemulsion Phases Qi, Luqing; ShamsiJazeyi, Hadi; Ruan, Gedeng Energy & Fuels, Vol. 31, Issue 2 https://doi.org/10.1021/acs.energyfuels.6b02687	journal	February 2017
Lecithin-Linker Microemulsion Gelatin Gels for Extended Drug Delivery Xuan, Xiao-Yue; Cheng, Yu-Ling; Acosta, Edgar Pharmaceutics, Vol. 4, Issue 1 https://doi.org/10.3390/pharmaceutics4010104	journal	January 2012
Using self-cleavable ternary fusion pattern for efficient preparation of Bacteriorhodopsin Huang, Haihong; Yang, Bin; Ge, Baosheng Process Biochemistry, Vol. 64 https://doi.org/10.1016/j.procbio.2017.09.024	journal	January 2018
Effect of amphiphilic block copolymers on the structure and phase behavior of oil–water-surfactant mixtures Endo, H.; Mihailescu, M.; Monkenbusch, M. The Journal of Chemical Physics, Vol. 115, Issue 1 https://doi.org/10.1063/1.1377881	journal	July 2001
Bio-nano hybrid materials based on bacteriorhodopsin: Potential applications and future strategies Mahyad, Baharak; Janfaza, Sajjad; Hosseini, Elaheh Sadat Advances in Colloid and Interface Science, Vol. 225 https://doi.org/10.1016/j.cis.2015.09.006	journal	November 2015
Biomimetic Membranes with Transmembrane Proteins: State-of-the-Art in Transmembrane Protein Applications Ryu, Hyunil; Fuwad, Ahmed; Yoon, Sunhee International Journal of Molecular Sciences, Vol. 20, Issue 6 https://doi.org/10.3390/ijms20061437	journal	March 2019

Similar Records

Observation of a structural gradient in Winsor-III microemulsion systems

Journal Article · Mon May 21 00:00:00 EDT 2018 · Soft Matter · OSTI ID:1786536

Hayes, Douglas G.; Pingali, Sai Venkatesh; O’Neill, Hugh M.; +2 more

Effect of Protein Incorporation on the Nanostructure of the Bicontinuous Microemulsion Phase of Winsor-III Systems: A Small-Angle Neutron Scattering Study

Journal Article · Tue Jan 20 00:00:00 EST 2015 · Langmuir · OSTI ID:1786536

Hayes, Douglas G.; Gomez del Rio, Javier A.; Ye, Ran; +3 more

Protein extraction into the bicontinuous microemulsion phase of a Water/SDS/pentanol/dodecane winsor-III system: Effect on nanostructure and protein conformation

Journal Article · Thu Sep 07 00:00:00 EDT 2017 · Colloids and Surfaces. B, Biointerfaces · OSTI ID:1786536

Hayes, Douglas G.; Ye, Ran; Dunlap, Rachel N.; +4 more

Title: Incorporation of Membrane Proteins Into Bicontinuous Microemulsions Through Winsor‐III System‐Based Extraction

Citation Formats

References (54)

Similar Records

Related Subjects