Amphiphilic polymers are increasingly applied in the detergent-free isolation and functional studies of membrane proteins. However, the carboxylate group present in the structure of many popular variants, such as styrene-maleic acid (SMA) copolymers, brings limitations in terms of polymer sensitivity to precipitation at acidic pH or in the presence of divalent metal cations. Herein, we addressed this problem by replacing carboxylate with the more acidic sulfonate groups. To this end, we synthesized a library of amphiphilic poly[styrene-co-(sodium 4-styrene sulfonate)] copolymers (termed SSS), differing in their molecular weight and overall polarity. Using model cell membranes (Jurkat), we identified two copolymer compositions (SSS-L30 and SSS-L36) that solubilized membranes to an extent similar to SMA. Interestingly, the density gradient ultracentrifugation/SDS-PAGE/Western blotting analysis of cell lysates revealed a distribution of studied membrane proteins in the gradient fractions that was different than for SMA-solubilized membranes. Importantly, unlike SMA, the SSS copolymers remained soluble at low pH and in the presence of Mg2+ ions. Additionally, the solubilization of DMPC liposomes by the lead materials was studied by turbidimetry, DLS, SEC, and high-resolution NMR, revealing, for SSS-L36, the formation of stable particles (nanodiscs), facilitated by the direct hydrophobic interaction of the copolymer phenyls with lipid acyl chains.

Biophysics Program Department of Chemistry Macromolecular Science and Engineering Biomedical Engineering Michigan Neuroscience Institute The University of Michigan Ann Arbor MI 48109 1055 USA

Institute of Macromolecular Chemistry Czech Academy of Sciences Heyrovského nám 2 162 06 Prague 6 Czech Republic

Institute of Molecular Genetics of the Czech Academy of Sciences Vídeňská 1083 142 20 Prague 4 Czech Republic

Zobrazit více v PubMed

Overington JP, Al-Lazikani B, Hopkins AL, How many drug targets are there?, Nat. Rev. Drug Discovery 5 (12) (2006) 993–996. 10.1038/nrd2199. PubMed DOI

Sligar SG, Denisov IG, Nanodiscs: A toolkit for membrane protein science, Protein Science 30 (2) (2021) 297–315. 10.1002/pro.3994. PubMed DOI PMC

Overduin M, Esmaili M, Memtein: The fundamental unit of membrane-protein structure and function, Chem. Phys. Lipids 218 (2019) 73–84. 10.1016/j.chemphyslip.2018.11.008. PubMed DOI

Ravula T, Hardin NZ, Ramamoorthy A, Polymer nanodiscs: Advantages and limitations, Chem. Phys. Lipids 219 (2019) 45–49. 10.1016/j.chemphyslip.2019.01.010. PubMed DOI PMC

Zoonens M, Comer J, Masscheleyn S, Pebay-Peyroula E, Chipot C, Miroux B, Dehez F, Dangerous Liaisons between Detergents and Membrane Proteins. The Case of Mitochondrial Uncoupling Protein 2, J. Am. Chem. Soc 135 (40) (2013) 15174–15182. 10.1021/ja407424v. PubMed DOI

Knowles TJ, Finka R, Smith C, Lin Y-P, Dafforn T, Overduin M, Membrane Proteins Solubilized Intact in Lipid Containing Nanoparticles Bounded by Styrene Maleic Acid Copolymer, J. Am. Chem. Soc 131 (22) (2009) 7484–7485. 10.1021/ja810046q. PubMed DOI

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 (1) (2016) 3–21. 10.1007/s00249-015-1093-y. PubMed DOI PMC

Barniol-Xicota M, Verhelst SHL, Stable and Functional Rhomboid Proteases in Lipid Nanodiscs by Using Diisobutylene/Maleic Acid Copolymers, J. Am. Chem. Soc 140 (44) (2018) 14557–14561. 10.1021/jacs.8b08441. PubMed DOI

Sun C, Benlekbir S, Venkatakrishnan P, Wang Y, Hong S, Hosier J, Tajkhorshid E, Rubinstein JL, Gennis RB, Structure of the alternative complex III in a supercomplex with cytochrome oxidase, Nature 557 (7703) (2018) 123–126. 10.1038/s41586-018-0061-y. PubMed DOI PMC

Swainsbury DJK, 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 53 (44) (2014) 11803–11807. 10.1002/anie.201406412. PubMed DOI PMC

Bada Juarez JF, Harper AJ, Judge PJ, Tonge SR, Watts A, From polymer chemistry to structural biology: The development of SMA and related amphipathic polymers for membrane protein extraction and solubilisation, Chem. Phys. Lipids 221 (2019) 167–175. 10.1016/j.chemphyslip.2019.03.008. PubMed DOI

Krishnarjuna B, Im S-C, Ravula T, Marte J, Auchus RJ, Ramamoorthy A, Non-Ionic Inulin-Based Polymer Nanodiscs Enable Functional Reconstitution of a Redox Complex Composed of Oppositely Charged CYP450 and CPR in a Lipid Bilayer Membrane, Anal. Chem 94 (34) (2022) 11908–11915. 10.1021/acs.analchem.2c02489. PubMed DOI PMC

Krishnarjuna B, Ravula T, Ramamoorthy A, Detergent-free isolation of CYP450-reductase’s FMN-binding domain in E. coli lipid-nanodiscs using a charge-free polymer, Chem. Commun 58 (31) (2022) 4913–4916. 10.1039/D1CC07193A. PubMed DOI PMC

Shu S, Mi W, Regulatory mechanisms of lipopolysaccharide synthesis in Escherichia coli, Nat. Commun 13 (1) (2022) 4576. 10.1038/s41467-022-32277-1. PubMed DOI PMC

Swainsbury DJK, Hawkings FR, Martin EC, Musiat S, Salisbury JH, Jackson PJ, Farmer DA, Johnson MP, Siebert CA, Hitchcock A, Hunter CN, Cryo-EM structure of the four-subunit Rhodobacter sphaeroides cytochrome bc(1) complex in styrene maleic acid nanodiscs, Proc. Natl. Acad. Sci. U. S. A 120 (12) (2023) e2217922120. 10.1073/pnas.2217922120. PubMed DOI PMC

Harant K, Čajka T, Angelisová P, Pokorná J, Hořejší V, Composition of raft-like cell membrane microdomains resistant to styrene-maleic acid copolymer (SMA) solubilization, Biophys. Chem 296 (2023) 106989. 10.1016/j.bpc.2023.106989. PubMed DOI

Krishnarjuna B, Ramamoorthy A, Detergent-Free Isolation of Membrane Proteins and Strategies to Study Them in a Near-Native Membrane Environment, Biomolecules 12 (8) (2022) 1076. 10.3390/biom12081076. PubMed DOI PMC

Noh I, Guo Z, Zhou J, Gao W, Fang RH, Zhang L, Cellular Nanodiscs Made from Bacterial Outer Membrane as a Platform for Antibacterial Vaccination, ACS Nano 17 (2) (2023) 1120–1127. 10.1021/acsnano.2c08360. PubMed DOI PMC

Sun L, Wang D, Noh I, Fang RH, Gao W, Zhang L, Synthesis of Erythrocyte Nanodiscs for Bacterial Toxin Neutralization, Angew. Chem. Int. Ed n/a (n/a) (2023) e202301566. 10.1002/anie.202301566. PubMed DOI

Klumperman B, Mechanistic considerations on styrene–maleic anhydride copolymerization reactions, Polym. Chem 1 (5) (2010) 558–562. 10.1039/B9PY00341J. DOI

Smith AAA, Autzen HE, Laursen T, Wu V, Yen M, Hall A, Hansen SD, Cheng Y, Xu T, Controlling Styrene Maleic Acid Lipid Particles through RAFT, Biomacromolecules 18 (11) (2017) 3706–3713. 10.1021/acs.biomac.7b01136. PubMed DOI

Stroud Z, Hall SCL, Dafforn TR, Purification of membrane proteins free from conventional detergents: SMA, new polymers, new opportunities and new insights, Methods 147 (2018) 106–117. 10.1016/j.ymeth.2018.03.011. PubMed DOI

Smith AAA, Autzen HE, Faust B, Mann JL, Muir BW, Howard S, Postma A, Spakowitz AJ, Cheng Y, Appel EA, Lipid Nanodiscs via Ordered Copolymers, Chem 6 (10) (2020) 2782–2795. 10.1016/j.chempr.2020.08.004. DOI

Sawczyc H, Heit S, Watts A, A comparative characterisation of commercially available lipid-polymer nanoparticles formed from model membranes, Eur. Biophys. J 52 (1) (2023) 39–51. 10.1007/s00249-023-01632-5. PubMed DOI PMC

Bariwal J, Ma H, Altenberg GA, Liang H, Nanodiscs: a versatile nanocarrier platform for cancer diagnosis and treatment, Chem. Soc. Rev 51 (5) (2022) 1702–1728. 10.1039/D1CS01074C. PubMed DOI

Cunningham RD, Kopf AH, Elenbaas BOW, Staal BBP, Pfukwa R, Killian JA, Klumperman B, Iterative RAFT-Mediated Copolymerization of Styrene and Maleic Anhydride toward Sequence- and Length-Controlled Copolymers and Their Applications for Solubilizing Lipid Membranes, Biomacromolecules 21 (8) (2020) 3287–3300. 10.1021/acs.biomac.0c00736. PubMed DOI

Domínguez Pardo JJ, Koorengevel MC, Uwugiaren N, Weijers J, Kopf AH, Jahn H, van Walree CA, van Steenbergen MJ, Killian JA, Membrane Solubilization by Styrene-Maleic Acid Copolymers: Delineating the Role of Polymer Length, Biophys. J 115 (1) (2018) 129–138. 10.1016/j.bpj.2018.05.032. PubMed DOI PMC

Hall SCL, Tognoloni C, Price GJ, Klumperman B, Edler KJ, Dafforn TR, Arnold T, Influence of Poly(styrene-co-maleic acid) Copolymer Structure on the Properties and Self-Assembly of SMALP Nanodiscs, Biomacromolecules 19 (3) (2018) 761–772. 10.1021/acs.biomac.7b01539. PubMed DOI

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, Biomembr 1858 (11) (2016) 2931–2939. 10.1016/j.bbamem.2016.08.004. PubMed DOI

Ravula T, Hardin NZ, Ramadugu SK, Cox SJ, Ramamoorthy A, Formation of pH-Resistant Monodispersed Polymer–Lipid Nanodiscs, Angew. Chem. Int. Ed 57 (5) (2018) 1342–1345. 10.1002/anie.201712017. PubMed DOI PMC

Fiori MC, Jiang Y, Altenberg GA, Liang H, Polymer-encased nanodiscs with improved buffer compatibility, Sci. Rep 7 (1) (2017) 7432. 10.1038/s41598-017-07110-1. PubMed DOI PMC

Ravula T, Hardin NZ, Ramadugu SK, Ramamoorthy A, pH Tunable and Divalent Metal Ion Tolerant Polymer Lipid Nanodiscs, Langmuir 33 (40) (2017) 10655–10662. 10.1021/acs.langmuir.7b02887. PubMed DOI

Ravula T, Ramadugu SK, Di Mauro G, Ramamoorthy A, Bioinspired, Size-Tunable Self-Assembly of Polymer–Lipid Bilayer Nanodiscs, Angew. Chem. Int. Ed 56 (38) (2017) 11466–11470. 10.1002/anie.201705569. PubMed DOI PMC

Lindhoud S, Carvalho V, Pronk JW, Aubin-Tam M-E, SMA-SH: Modified Styrene–Maleic Acid Copolymer for Functionalization of Lipid Nanodiscs, Biomacromolecules 17 (4) (2016) 1516–1522. 10.1021/acs.biomac.6b00140. PubMed DOI

Hall SCL, Tognoloni C, Charlton J, Bragginton ÉC, Rothnie AJ, Sridhar P, Wheatley M, Knowles TJ, Arnold T, Edler KJ, Dafforn TR, An acid-compatible co-polymer for the solubilization of membranes and proteins into lipid bilayer-containing nanoparticles, Nanoscale 10 (22) (2018) 10609–10619. 10.1039/C8NR01322E. PubMed DOI PMC

Neville GM, Edler KJ, Price GJ, Fluorescent styrene maleic acid copolymers to facilitate membrane protein studies in lipid nanodiscs, Nanoscale 14 (15) (2022) 5689–5693. 10.1039/D1NR07230G. PubMed DOI

Krishnarjuna B, Ravula T, Ramamoorthy A, Detergent-free extraction, reconstitution and characterization of membrane-anchored cytochrome-b5 in native lipids, Chem. Commun 56 (48) (2020) 6511–6514. 10.1039/D0CC01737J. PubMed DOI PMC

Kopf AH, Lijding O, Elenbaas BOW, Koorengevel MC, Dobruchowska JM, van Walree CA, Killian JA, Synthesis and Evaluation of a Library of Alternating Amphipathic Copolymers to Solubilize and Study Membrane Proteins, Biomacromolecules 23 (3) (2022) 743–759. 10.1021/acs.biomac.1c01166. PubMed DOI PMC

Glueck D, Grethen A, Das M, Mmeka OP, Patallo EP, Meister A, Rajender R, Kins S, Raschle M, Victor J, Chu C, Etzkorn M, Köck Z, Bernhard F, Babalola JO, Vargas C, Keller S, Electroneutral Polymer Nanodiscs Enable Interference-Free Probing of Membrane Proteins in a Lipid-Bilayer Environment, Small 18 (47) (2022) 2202492. 10.1002/smll.202202492. PubMed DOI

Workman CE, Cawthon B, Brady NG, Bruce BD, Long BK, Effects of Esterified Styrene–Maleic Acid Copolymer Degradation on Integral Membrane Protein Extraction, Biomacromolecules 23 (11) (2022) 4749–4755. 10.1021/acs.biomac.2c00928. PubMed DOI

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 56 (7) (2017) 1919–1924. 10.1002/anie.201610778. PubMed DOI PMC

Oluwole AO, Klingler J, Danielczak B, Babalola JO, Vargas C, Pabst G, Keller S, Formation of Lipid-Bilayer Nanodiscs by Diisobutylene/Maleic Acid (DIBMA) Copolymer, Langmuir 33 (50) (2017) 14378–14388. 10.1021/acs.langmuir.7b03742. PubMed DOI

Ball LE, Riley LJ, Hadasha W, Pfukwa R, Smith CJI, Dafforn TR, Klumperman B, Influence of DIBMA Polymer Length on Lipid Nanodisc Formation and Membrane Protein Extraction, Biomacromolecules 22 (2) (2021) 763–772. 10.1021/acs.biomac.0c01538. PubMed DOI

Danielczak B, Rasche M, Lenz J, Pérez Patallo E, Weyrauch S, Mahler F, Agbadaola MT, Meister A, Babalola JO, Vargas C, Kolar C, Keller S, A bioinspired glycopolymer for capturing membrane proteins in native-like lipid-bilayer nanodiscs, Nanoscale 14 (5) (2022) 1855–1867. 10.1039/DlNR03811G. PubMed DOI

Janson K, Zierath J, Kyrilis FL, Semchonok DA, Hamdi F, Skalidis I, Kopf AH, Das M, Kolar C, Rasche M, Vargas C, Keller S, Kastritis PL, Meister A, Solubilization of artificial mitochondrial membranes by amphiphilic copolymers of different charge, Biochim. Biophys. Acta, Biomembr 1863 (12) (2021) 183725. 10.1016/j.bbamem.2021.183725. PubMed DOI

Yasuhara K, Arakida J, Ravula T, Ramadugu SK, Sahoo B, Kikuchi J.-i., Ramamoorthy A, Spontaneous Lipid Nanodisc Fomation by Amphiphilic Polymethacrylate Copolymers, J. Am. Chem. Soc 139 (51) (2017) 18657–18663. 10.1021/jacs.7b10591. PubMed DOI PMC

Janata M, Čadová E, Angelisová P, Charnavets T, Hořejší V, Raus V, Tailoring Butyl Methacrylate/Methacrylic Acid Copolymers for the Solubilization of Membrane Proteins: The Influence of Composition and Molecular Weight, Macromol. Biosci 22 (10) (2022) 2200284. 10.1002/mabi.202200284. PubMed DOI

Hardin NZ, Ravula T, Mauro GD, Ramamoorthy A, Hydrophobic Functionalization of Polyacrylic Acid as a Versatile Platform for the Development of Polymer Lipid Nanodisks, Small 15 (9) (2019) 1804813. 10.1002/smll.201804813. PubMed DOI PMC

Timcenko M, Autzen AAA, Autzen HE, Characterization of Divalent Cation Interactions with AASTY Nanodiscs, ACS Appl. Polym. Mater 4 (2) (2022) 1071–1083. 10.1021/acsapm.1c01507. DOI

Ravula T, Ramamoorthy A, Synthesis, Characterization, and Nanodisc Formation of Non-ionic Polymers, Angew. Chem. Int. Ed 60 (31) (2021) 16885–16888. 10.1002/anie.202101950. PubMed DOI PMC

Krishnarjuna B, Marte J, Ravula T, Ramamoorthy A, Enhancing the stability and homogeneity of non-ionic polymer nanodiscs by tuning electrostatic interactions, J. Colloid Interface Sci 634 (2023) 887–896. 10.1016/j.jcis.2022.12.112. PubMed DOI PMC

Esmaili M, Brown CJ, Shaykhutdinov R, Acevedo-Morantes C, Wang YL, Wille H, Gandour RD, Turner SR, Overduin M, Homogeneous nanodiscs of native membranes formed by stilbene–maleic-acid copolymers, Nanoscale 12 (32) (2020) 16705–16709. 10.1039/D0NR03435E. PubMed DOI

Marconnet A, Michon B, Le Bon C, Giusti F, Tribet C, Zoonens M, Solubilization and Stabilization of Membrane Proteins by Cycloalkane-Modified Amphiphilic Polymers, Biomacromolecules 21 (8) (2020) 3459–3467. 10.1021/acs.biomac.0c00929. PubMed DOI

Marconnet A, Michon B, Prost B, Solgadi A, Le Bon C, Giusti F, Tribet C, Zoonens M, Influence of Hydrophobic Groups Attached to Amphipathic Polymers on the Solubilization of Membrane Proteins along with Their Lipids, Anal. Chem 94 (41) (2022) 14151–14158. 10.1021/acs.analchem.2c01746. PubMed DOI

Yu T, Omarova M, Zhang M, Hossain I, Chen J, Darvish O, John VT, Zhang D, Uncovering the Optimal Molecular Characteristics of Hydrophobe-Containing Polypeptoids to Induce Liposome or Cell Membrane Fragmentation, Biomacromolecules 24 (3) (2023) 1511–1521. 10.1021/acs.biomac.3c00028. PubMed DOI PMC

Mahler F, Meister A, Vargas C, Durand G, Keller S, Self-Assembly of Protein-Containing Lipid-Bilayer Nanodiscs from Small-Molecule Amphiphiles, Small 17 (49) (2021) 2103603. 10.1002/smll.202103603. PubMed DOI

McCalpin SD, Ravula T, Ramamoorthy A, Saponins Form Nonionic Lipid Nanodiscs for Protein Structural Studies by Nuclear Magnetic Resonance Spectroscopy, J. Phys. Chem. Lett 13 (7) (2022) 1705–1712. 10.1021/acs.jpclett.1c04185. PubMed DOI PMC

Grime RL, Logan RT, Nestorow SA, Sridhar P, Edwards PC, Tate CG, Klumperman B, Dafforn TR, Poyner DR, Reeves PJ, Wheatley M, Differences in SMA-like polymer architecture dictate the conformational changes exhibited by the membrane protein rhodopsin encapsulated in lipid nanoparticles, Nanoscale 13 (31) (2021) 13519–13528. 10.1039/D1NR02419A. PubMed DOI PMC

Real Hernandez LM, Levental I, Lipid packing is disrupted in copolymeric nanodiscs compared with intact membranes, Biophys. J (2023). 10.1016/j.bpj.2023.01.013. PubMed DOI PMC

Morrison KA, Wood L, Edler KJ, Doutch J, Price GJ, Koumanov F, Whitley P, Membrane extraction with styrene-maleic acid copolymer results in insulin receptor autophosphorylation in the absence of ligand, Sci. Rep 12 (1) (2022) 3532. 10.1038/s41598-022-07606-5. PubMed DOI PMC

Kamilar E, Bariwal J, Zheng W, Ma H, Liang H, SMALPs Are Not Simply Nanodiscs: The Polymer-to-Lipid Ratios of Fractionated SMALPs Underline Their Heterogeneous Nature, Biomacromolecules 24 (4) (2023) 1819–1838. 10.1021/acs.biomac.3c00034. PubMed DOI

Ravula T, Hardin NZ, Bai J, Im S-C, Waskell L, Ramamoorthy A, Effect of polymer charge on functional reconstitution of membrane proteins in polymer nanodiscs, Chem. Commun 54 (69) (2018) 9615–9618. 10.1039/C8CC04184A. PubMed DOI PMC

Overduin M, Klumperman B, Advancing membrane biology with poly(styrene-co-maleic acid)-based native nanodiscs, Eur. Polym. J 110 (2019) 63–68. 10.1016/j.eurpolymj.2018.11.015. DOI

Krishnarjuna B, Sharma G, Ravula T, Ramamoorthy A, Factors influencing the detergent-free membrane protein isolation using synthetic nanodisc-forming polymers, bioRxiv (2023) 2023.05.12.540572. 10.1101/2023.05.12.540572. PubMed DOI PMC

Dobrynin AV, Rubinstein M, Theory of polyelectrolytes in solutions and at surfaces, Prog. Polym. Sci 30 (11) (2005) 1049–1118. 10.1016/j.progpolymsci.2005.07.006. DOI

Janata M, Kůdela V, Gromadzki D, štěpánek P, Nallet F, Diat O, Vlček P, Toman L, Synthesis of highly sulfonated polystyrene-based block copolymers soluble in tetrahydrofuran, e-Polymers 6 (1) (2006). 10.1515/epoly.2006.6.1.702. DOI

Baigl D, Seery TAP, Williams CE, Preparation and Characterization of Hydrosoluble, Partially Charged Poly(styrenesulfonate)s of Various Controlled Charge Fractions and Chain Lengths, Macromolecules 35 (6) (2002) 2318–2326. 10.1021/ma011707o. DOI

Elabd YA, Napadensky E, Sulfonation and characterization of poly(styrene-isobutylene-styrene) triblock copolymers at high ion-exchange capacities, Polymer 45 (9) (2004) 3037–3043. 10.1016/j.polymer.2004.02.061. DOI

Jamshad M, Grimard V, Idini I, Knowles TJ, Dowle MR, Schofield N, Sridhar P, Lin Y, Finka R, Wheatley M, Thomas ORT, Palmer RE, Overduin M, Govaerts C, Ruysschaert J-M, Edler KJ, Dafforn TR, Structural analysis of a nanoparticle containing a lipid bilayer used for detergent-free extraction of membrane proteins, Nano Res. 8 (3) (2015) 774–789. 10.1007/s12274-014-0560-6. PubMed DOI PMC

Morrison KA, Akram A, Mathews A, Khan ZA, Patel JH, Zhou C, Hardy DJ, Moore-Kelly C, Patel R, Odiba V, Knowles TJ, Javed M.-u.-H., Chmel NP, Dafforn TR, Rothnie AJ, Membrane protein extraction and purification using styrene–maleic acid (SMA) copolymer: effect of variations in polymer structure, Biochem. J 473 (23) (2016) 4349–4360. 10.1042/BCJ20160723. PubMed DOI

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, Biomembr 1859 (10) (2017) 2133–2143. 10.1016/j.bbamem.2017.07.011. PubMed DOI PMC

Sezgin E, Levental I, Mayor S, Eggeling C, The mystery of membrane organization: composition, regulation and roles of lipid rafts, Nat. Rev. Mol. Cell Biol 18 (6) (2017) 361–374. 10.1038/nrm.2017.16. PubMed DOI PMC

Angelisová P, Ballek O, Sýkora J, Benada O, Čajka T, Pokorná J, Pinkas D, Hořejší V, The use of styrene-maleic acid copolymer (SMA) for studies on T cell membrane rafts, Biochim. Biophys. Acta, Biomembr 1861 (1) (2019) 130–141. 10.1016/j.bbamem.2018.08.006. PubMed DOI

Sahoo BR, Genjo T, Moharana KC, Ramamoorthy A, Self-Assembly of Polymer-Encased Lipid Nanodiscs and Membrane Protein Reconstitution, J. Phys. Chem. B 123 (21) (2019) 4562–4570. 10.1021/acs.jpcb.9b03681. PubMed DOI PMC

Bjørnestad VA, Orwick-Rydmark M, Lund R, Understanding the Structural Pathways for Lipid Nanodisc Formation: How Styrene Maleic Acid Copolymers Induce Membrane Fracture and Disc Formation, Langmuir 37 (20) (2021) 6178–6188. 10.1021/acs.langmuir.1c00304. PubMed DOI PMC

Novel class of peptides disintegrating biological membranes to aid in the characterization of membrane proteins