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SMALP Publications and Patents

The following papers and patents have reported significant developments in the SMALP field.

2017

Pollock NL, Lee SC, Patel JH, Gulamhussein AA, Rothnie AJ. Structure and function of membrane proteins encapsulated in a polymer-bound lipid bilayer. Biochim Biophys Acta. in press.

Dörr JM, van Coevorden-Hameete MH, Hoogenraad CC, Antoinette Killian J. Solubilization of human cells by the styrene-maleic acid copolymer: Insights from fluorescence microscopy. Biochim Biophys Acta. in press.

Fiori MC, Jiang Y, Altenberg GA, Liang H. Polymer-encased nanodiscs with improved buffer compatibility. Sci Rep. 7(1):7432.

Swainsbury DJK, Scheidelaar S, Foster N, van Grondelle R, Killian JA, Jones MR. The effectiveness of styrene-maleic acid (SMA) copolymers for solubilisation of integral membrane proteins from SMA-accessible and SMA-resistant membranes. Biochim Biophys Acta. 1859(10):2133-2143.

Ravula T, Ramadugu SK, Di Mauro G, Ramamoorthy A. Bioinspired, Size-Tunable Self-Assembly of Polymer-Lipid Bilayer Nanodiscs. Angew Chem Int Ed Engl. 56(38):11466-11470.

Denisov IG, Sligar SG. Nanodiscs in Membrane Biochemistry and Biophysics. Chem Rev. 117(6):4669-4713.

Stetsenko A, Albert Guskov A. An Overview of the Top Ten Detergents Used for Membrane Protein Crystallization. Crystals 7, 197.

Huang J, Turner SR. Recent advances in alternating copolymers: The synthesis, modification, and applications of precision polymers. Polymer 116, 572-586.

Dowall JS, Ntai I, Hake J, Whitley PR, Mason JM, Pudney CR, Brown DR. Steady-State Kinetics of α-Synuclein Ferrireductase Activity Identifies the Catalytically Competent Species. Biochemistry. 56(19):2497-2505.

Hu Z, Ho JC, Nallani M. Synthetic (polymer) biology (membrane): functionalization of polymer scaffolds for membrane proteins. Curr Opin Biotechnol. 46:51-56.

Bos I, Bland KM, Tian L, Croce R, Frankel LK, van Amerongen H, Bricker TM, Wientjes E. Multiple LHCII antennae can transfer energy efficiently to a single Photosystem I. Biochim Biophys Acta. 1858(5):371-378.

Zoghbi ME, Altenberg GA. Membrane protein reconstitution in nanodiscs for luminescence spectroscopy studies. Nanotech Rev 6: 1

Penny WM, Steele HB, Ross JB, Palmer CP. Phospholipid bilayer affinities and solvation characteristics by electrokinetic chromatography with a nanodisc pseudostationary phase. Electrophoresis. 38(5):738-746.

Beales PA, Khan S, Muench SP, Jeuken LJ. Durable vesicles for reconstitution of membrane proteins in biotechnology. Biochem Soc Trans. 45(1):15-26.

Sahu ID, Zhang R, Dunagan MM, Craig AF, Lorigan GA. Characterization of KCNE1 inside Lipodisq Nanoparticles for EPR Spectroscopic Studies of Membrane Proteins. J Phys Chem B. 121(21):5312-5321.

Zhang R, Sahu ID, Bali AP, Dabney-Smith C, Lorigan GA. Characterization of the structure of lipodisq nanoparticles in the presence of KCNE1 by dynamic light scattering and transmission electron microscopy. Chem Phys Lipids. 203:19-23.

Cuevas Arenas R, Danielczak B, Martel A, Porcar L, Breyton C, Ebel C, Keller S. Fast Collisional Lipid Transfer Among Polymer-Bounded Nanodiscs. Sci Rep. 5;7:45875.

Puthenveetil R, Nguyen K, Vinogradova O. Nanodiscs and Solution NMR: preparation, application and challenges. Nanotechnol Rev. 6(1):111-126.

Rehan S, Paavilainen VO, Jaakola VP. Functional reconstitution of human equilibrative nucleoside transporter-1 into styrene maleic acid co-polymer lipid particles. Biochim Biophys Acta. 1859(5):1059-1065.

Bersch B, Dörr JM, Hessel A, Killian JA, Schanda P. Proton-Detected Solid-State NMR Spectroscopy of a Zinc Diffusion Facilitator Protein in Native Nanodiscs. Angew Chem Int Ed Engl. 56(9):2508-2512.

Oluwole AO, Danielczak B, Meister A, Babalola JO, Vargas C, Keller S. Solubilization of Membrane Proteins into Functional Lipid-Bilayer Nanodiscs Using a Diisobutylene / Maleic Acid Copolymer. Angew Chem Int Ed Engl. 6;56(7):1919-1924.

Broecker J, Eger BT, Ernst OP. Crystallogenesis of Membrane Proteins Mediated by Polymer-Bounded Lipid Nanodiscs. Structure 25, 1–9.

Dominguez Pardo JJ, Dörr JM, Iyer A, Cox RC, Scheidelaar S, Koorengevel MC, Subramaniam V, Killian JA. Solubilization of lipids and lipid phases by the styrene-maleic acid copolymer. Eur Biophys J. 46(1):91-101.

2016

Rawson S, Davies S, Lippiat JD, Muench SP. The changing landscape of membrane protein structural biology through developments in electron microscopy, Molecular Membrane Biology, 33:1-2, 12-22

Komar J, Alvira S, Schulze RJ, Martin R, Lycklama A Nijeholt JA, Lee SC, Dafforn TR, Deckers-Hebestreit G, Berger I, Schaffitzel C, Collinson I. Membrane protein insertion and assembly by the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. Biochem J. 473(19):3341-54.

Viegas A, Viennet T, Etzkorn M. The power, pitfalls and potential of the nanodisc system for NMR-based studies. Biol Chem. 397(12):1335-1354.

Grewal YS, Shiddiky MJ, Mahler SM, Cangelosi GA, Trau M. Nanoyeast and Other Cell Envelope Compositions for Protein Studies and Biosensor Applications. ACS Appl Mater Interfaces. 8(45):30649-30664.

Laursen T, Borch J, Knudsen C, Bavishi K, Torta F, Martens HJ, Silvestro D, Hatzakis NS, Wenk MR, Dafforn TR, Olsen CE, Motawia MS, Hamberger B, Møller BL, Bassard JE. Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum. Science. 354(6314):890-893.

Scheidelaar S, Koorengevel MC, van Walree CA, Dominguez JJ, Dörr JM, Killian JA. Effect of Polymer Composition and pH on Membrane Solubilization by Styrene-Maleic Acid Copolymers. Biophys J. 111(9):1974-1986.

Craig AF, Clark EE, Sahu ID, Zhang R, Frantz ND, Al-Abdul-Wahid MS, Dabney-Smith C, Konkolewicz D, Lorigan GA. Tuning the size of styrene-maleic acid copolymer-lipid nanoparticles (SMALPs) using RAFT polymerization for biophysical studies. Biochim Biophys Acta. 1858(11):2931-2939.

Parmar MJ, Lousa Cde M, Muench SP, Goldman A, Postis VL. Artificial membranes for membrane protein purification, functionality and structure studies. Biochem Soc Trans. 44(3):877-82.

Hazell G, Arnold T, Barker RD, Clifton LA, Steinke NJ, Tognoloni C, Edler KJ. Evidence of Lipid Exchange in Styrene Maleic Acid Lipid Particle (SMALP) Nanodisc Systems. Langmuir 15;32(45):11845-11853.

Morrison KA, Akram A, Mathews A, Khan ZA, Patel JH, Zhou C, Hardy DJ, Moore-Kelly C, Patel R, Odiba V, Knowles T, Javed MU, Chmel NP, Dafforn TR, Rothnie AJ. Membrane protein extraction and purification using styrene-maleic acid (SMA) co-polymer: Effect of variations in polymer structure. Biochem J 1;473(23):4349-4360.

Rajesh S, Overduin M, Bonev BB. NMR of Membrane Proteins: Beyond Crystals. Adv Exp Med Biol. 922:29-42.

Rothnie AJ. Detergent-Free Membrane Protein Purification. Methods Mol Biol. 1432:261-7.

Lee SC, Pollock NL. Membrane proteins: is the future disc shaped? Biochem Soc Trans. 44(4):1011-8.

Smirnova IA, Sjöstrand D, Li F, Björck M, Schäfer J, Östbye H, Högbom M, von Ballmoos C, Lander GC, Ädelroth P, Brzezinski P. Isolation of yeast complex IV in native lipid nanodiscs. Biochim Biophys Acta. 1858(12):2984-2992.

Cuevas Arenas R, Klingler J, Vargas C, Keller S. Influence of lipid bilayer properties on nanodisc formation mediated by styrene/maleic acid copolymers. Nanoscale. 8(32):15016-26.

Hardy D, Bill RM, Jawhari A, Rothnie AJ. Overcoming bottlenecks in the membrane protein structural biology pipeline. Biochem Soc Trans. 44(3):838-44.

Dafforn TR, Lee SC, Knowles TJ, Postis V, Jamshad M, Parslow R, Lin YP, Goldman A, Sridhar P, Overduin M, Muench SP. A Method for Detergent-free isolation of Membrane Protein with its Local Lipid Environment, Nature Protocols, 11(7), 1149-1162.

Lee SC, Khalid S, Pollock NL, Knowles TJ, Edler K, Rothnie AJ, Thomas ORT, Dafforn TR, Encapsulated Membrane Proteins: A Simplified System For Molecular Simulation, BBA - Biomembranes, 1858(10):2549-57.

Wheatley M, Charlton J, Jamshad M, Routledge SJ, Bailey S, La-Borde PJ, Azam MT, Logan RT, Bill RM, Dafforn TR, Poyner DR. GPCR-styrene maleic acid lipid particles (GPCR-SMALPs): their nature and potential. Biochem Soc Trans. 44:619-23.

Lindhoud S, Carvalho V, Pronk JW, Aubin-Tam ME, SMA-SH: Modified Styrene-Maleic Acid copolymer for functionalization of lipid nanodiscs. Biomacromolecules, 17(4):1516-22.

Routledge SJ, Mikaliunaite L, Patel A, Clare M, Cartwright SP, Bawa Z, Wilks MD, Low F, Hardy D, Rothnie AJ, Bill RM. The synthesis of recombinant membrane proteins in yeast for structural studies. Methods 95:26-37.

Dörr JM, Scheidelaar S, Koorengevel MC, Dominguez JJ, Schäfer M, van Walree CA, Killian JA. The styrene-maleic acid copolymer: a versatile tool in membrane research. Eur Biophys J 45:3-21.

Logez C, Damian M, Legros C, Dupré C, Guéry M, Mary S, Wagner R, M'Kadmi C, Nosjean O, Fould B, Marie J, Fehrentz JA, Martinez J, Ferry G, Boutin JA, Banères JL. Detergent-free Isolation of Functional G Protein-Coupled Receptors into Nanometric Lipid Particles. Biochemistry 55:38-48.

2015

Zhang R, Sahu ID, Liu L, Osatuke A, Comer RG, Dabney-Smith C, Lorigan GA. Characterizing the structure of lipodisq nanoparticles for membrane protein spectroscopic studies. Biochim Biophys Acta 1848:329-33. PMID: 24853657.

Postis V, Rawson S, Mitchell JK, Lee SC, Parslow RA, Dafforn TR, Baldwin SA, Muench SP. The use of SMALPs as a novel membrane protein scaffold for structure study by negative stain electron microscopy. Biochim Biophys Acta 1848:496-501. PMID: 25450810.

Vargas C, Arenas RC, Frotscher E, Keller S. Nanoparticle self-assembly in mixtures of phospholipids with styrene/maleic acid copolymers or fluorinated surfactants. Nanoscale 7:20685-96. PMID: 26599076.

Skaar K, Korza HJ, Tarry M, Sekyrova P, Högbom M. Expression and Subcellular Distribution of GFP-Tagged Human Tetraspanin Proteins in Saccharomyces cerevisiae. PLoS One 10(7):e0134041. PMID: 26218426.

Bell AJ, Frankel LK, Bricker TM. High Yield Non-detergent Isolation of Photosystem I-Light-harvesting Chlorophyll II Membranes from Spinach Thylakoids: IMPLICATIONS FOR THE ORGANIZATION OF THE PS I ANTENNAE IN HIGHER PLANTS. J Biol Chem 290(30):18429-37. PMID: 26055710.

Scheidelaar S, Koorengevel MC, Pardo JD, Meeldijk JD, Breukink E, Killian JA. Molecular Model for the Solubilization of Membranes into Nanodisks by Styrene Maleic Acid Copolymers. Biophys J 108, 279–290. PMC4302193.

Li D, Li J, Zhuang Y, Zhang L, Xiong Y, Shi P, Tian C. Nano-size uni-lamellar lipodisq improved in situ auto-phosphorylation analysis of E. coli tyrosine kinase using (19)F nuclear magnetic resonance. Protein Cell 6:229-33. PMID: 25564343.

Tanaka M, Hosotani A, Tachibana Y, Nakano M, Iwasaki K, Kawakami T, Mukai T. Preparation and Characterization of Reconstituted Lipid-Synthetic Polymer Discoidal Particles. Langmuir. 31(46):12719-26. PMID: 26531224.

Prabudiansyah I, Kusters I, Caforio A, Driessen AJ. Characterization of the annular lipid shell of the Sec translocon. Biochim Biophys Acta 1848:2050-6. PMID: 26129641.

Goddard AD, Dijkman PM, Adamson RJ, dos Reis RI, Watts A. Reconstitution of membrane proteins: a GPCR as an example. Methods Enzymol 556:405-24. PMID: 25857793.

Jamshad M, Charlton J, Lin YP, Routledge SJ, Bawa Z, Knowles TJ, Overduin M, Dekker N, Dafforn TR, Bill RM, Poyner DR, Wheatley M. G-protein coupled receptor solubilization and purification for biophysical analysis and functional studies, in the total absence of detergent. Biosci Rep 35 pii: e00188. PMID: 25720391.

2014

Jamshad M, Grimard V, Idini I, Knowles TJ, Dowle MR, Schofield N, Sridhar P, Lin YP, Finka R, Wheatley M, Thomas ORT, Palmer RE, Overduin M, Govaerts C, Ruysschaert JM, Edler KJ, Dafforn TR. Structural analysis of a nanoparticle containing a lipid bilayer used for detergent-free extraction of membrane proteins. Nano Research 8: 774-789.

Paulin S, Jamshad M, Dafforn TR, Garcia-Lara J, Foster SJ, Galley NF, Roper DI, Rosado H, Taylor PW. Surfactant-free purification of membrane protein complexes from bacteria: application to the staphylococcal penicillin-binding protein complex PBP2/PBP2a. Nanotechnology 25:285101. PMID: 24972373.

Swainsbury DJ, Scheidelaar S, van Grondelle R, Killian JA, Jones MR. Bacterial reaction centers purified with styrene maleic acid copolymer retain native membrane functional properties and display enhanced stability. Angew Chem Int Ed Engl 53(44):11803-7. PMID: 25212490.

Dörr JM, Koorengevel MC, Schäfer M, Prokofyev AV, Scheidelaar S, van der Cruijsen EA, Dafforn TR, Baldus M, Killian JA. Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: the power of native nanodiscs. Proc Natl Acad Sci USA 111(52):18607-12. PMID: 25512535.

Sahu ID, Kroncke BM, Zhang R, Dunagan MM, Smith HJ, Craig A, McCarrick RM, Sanders CR, Lorigan GA. Structural investigation of the transmembrane domain of KCNE1 in proteoliposomes. Biochemistry 53:6392-401. PMID: 25234231.

Malhotra K, Alder NN. Advances in the use of nanoscale bilayers to study membrane protein structure and functionStructural investigation of the transmembrane domain of KCNE1 in proteoliposomes. Biotechnol Genet Eng Rev 30:79-93. PMID: 25023464.

2013

Gulati S, Jamshad M, Knowles TJ, Morrison KA, Downing R, Cant N, Collins R, Koenderink JB, Ford RC, Overduin M, Kerr ID, Dafforn TR, Rothnie AJ. Detergent-free purification of ABC (ATP-binding-cassette) transporters. Biochem J 461:269-78. PMID: 24758594.

Sahu ID, McCarrick RM, Troxel KR, Zhang R, Smith HJ, Dunagan MM, Swartz MS, Rajan PV, Kroncke BM, Sanders CR, Lorigan GA. DEER EPR measurements for membrane protein structures via bifunctional spin labels and lipodisq nanoparticles. Biochemistry 52:6627-32. PMID: 23984855.

Long AR, O'Brien CC, Malhotra K, Schwall CT, Albert AD, Watts A, Alder NN. A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol 13:41. PMID: 23663692.

2012

Orwick MC, Judge PJ, Procek J, Lindholm L, Graziadei A, Engel A, Gröbner G, Watts A. Detergent-free formation and physicochemical characterization of nanosized lipid-polymer complexes: Lipodisq. Angew Chem Int Ed Engl 51:4653-7. PMID: 22473824.

Orwick-Rydmark M, Lovett JE, Graziadei A, Lindholm L, Hicks MR, Watts A. Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer Lipodisq particles for functional and biophysical studies. Nano Lett 12:4687-92. PMID: 22827450.

Banerjee S, Pal TK, Guha SK. Probing molecular interactions of poly(styrene-co-maleic acid) with lipid matrix models to interpret the therapeutic potential of the co-polymer. Biochim Biophys Acta. 1818(3):537-50. 22197504.

2011

Jamshad M, Lin YP, Knowles TJ, Parslow RA, Harris C, Wheatley M, Poyner DR, Bill RM, Thomas OR, Overduin M, Dafforn TR. Surfactant-free purification of membrane proteins with intact native membrane environment. Biochem Soc Trans 39:813-8. PMID: 21599653.

Rajesh S, Knowles T, Overduin M. Production of membrane proteins without cells or detergents. N Biotechnol 28:250-4. PMID: 20654746.

Dafforn TR, Thomas ORT. Protein extraction, Patent GB20110007737 20110509; WO2012GB00423 20120509.

2010

Overduin M, Jamshad M, Lin Y, Knowles T, Jazayeri A, Poyner D, Bill R, Wheatley M, Dafforn T. Amphipathic polymer-based nanoparticles for purifying and characterizing stable and active GPCRs without detergents. Keystone Symposium on G Protein-Coupled Receptors.

Overduin M, Knowles T, Dafforn T. Solubilisation of membrane proteins. Patent GB2010/001309; WO2011/004158.

2009

Knowles TJ, Finka R, Smith C, Lin YP, Dafforn T, Overduin M. Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J Am Chem Soc 131:7484-5. PMID: 19449872.

2006

Tonge S. Compositions comprising a lipid and copolymer of styrene and maleic acid (note that the membrane protein data included in this patent is from Knowles et. al., 2009). Patent PCT/GB2006/050134; WO2006/129127.

Overduin, M, Tonge S. Memtein: Providing Membrane Protein Solutions, Venturefest finalist at the Oxford University Business Plan Competition.

2005

Michael Overduin submits Nanodisks for Drug Screening to Birmingham Research and Development Ltd, and is awarded a Technology Transfer Fund Grant by the Central Technology Belt for commercial development of the SMALP system with Steve Tonge being a co-applicant.

2004

A Royal Society Wolfson Research Merit Award to Michael Overduin entitled Structural Biology of Membrane Spanning Proteins by NMR Spectroscopy is funded from 2004-2009.