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10. Synthesis and Evaluation of a Library of Alternating Amphipathic Copolymers to Solubilize and Study Membrane Proteins

Author

Kopf, Adrian H., Lijding, Odette, Elenbaas, Barend O. W., Koorengevel, Martijn C., Dobruchowska, Justyna M., Walree, Cornelis A. van, Killian, J. Antoinette, Sub Membrane Biochemistry & Biophysics, Afd Chemical Biology and Drug Discovery, Membrane Biochemistry and Biophysics, Chemical Biology and Drug Discovery, Sub Membrane Biochemistry & Biophysics, Afd Chemical Biology and Drug Discovery, Membrane Biochemistry and Biophysics, and Chemical Biology and Drug Discovery

Subjects
Biomaterials, Polymers and Plastics, Polymers, Escherichia coli, Maleates, Materials Chemistry, Membrane Proteins, Polystyrenes, Bioengineering, Hydrophobic and Hydrophilic Interactions
Abstract

Amphipathic copolymers such as poly(styrene-maleic acid) (SMA) are promising tools for the facile extraction of membrane proteins (MPs) into native nanodiscs. Here, we designed and synthesized a library of well-defined alternating copolymers of SMA analogues in order to elucidate polymer properties that are important for MP solubilization and stability. MP extraction efficiency was determined using KcsA from E.coli membranes and general solubilization efficiency was investigated via turbidimetry experiments on membranes of E.coli, yeast mitochondria and synthetic lipids. Remarkably, halogenation of SMA copolymers dramatically improved solubilization efficiency in all systems, while substituents on the copolymer backbone improved resistance to Ca2+. Relevant polymer properties were found to include hydrophobic balance, size and positioning of substituents, rigidity and electronic effects. The library thus contributes to the rational design of copolymers for the study of MPs.

Published
2022

11. Synthesis and Evaluation of a Library of Alternating Amphipathic Copolymers to Solubilize and Study Membrane Proteins

Author

Sub Membrane Biochemistry & Biophysics, Afd Chemical Biology and Drug Discovery, Membrane Biochemistry and Biophysics, Chemical Biology and Drug Discovery, Kopf, Adrian H., Lijding, Odette, Elenbaas, Barend O. W., Koorengevel, Martijn C., Dobruchowska, Justyna M., Walree, Cornelis A. van, Killian, J. Antoinette, Sub Membrane Biochemistry & Biophysics, Afd Chemical Biology and Drug Discovery, Membrane Biochemistry and Biophysics, Chemical Biology and Drug Discovery, Kopf, Adrian H., Lijding, Odette, Elenbaas, Barend O. W., Koorengevel, Martijn C., Dobruchowska, Justyna M., Walree, Cornelis A. van, and Killian, J. Antoinette

Published
2022

15. Shortening of membrane lipid acyl chains compensates for phosphatidylcholine deficiency in choline-auxotroph yeast

Author

Sub Membrane Biochemistry & Biophysics, Sub Cryo - EM, Membrane Biochemistry and Biophysics, Bao, Xue, Koorengevel, Martijn C., Groot Koerkamp, Marian J.A., Homavar, Amir, Weijn, Amrah, Crielaard, Stefan, Renne, Mike F., Lorent, Joseph H., Geerts, Willie J.C., Surma, Michal A., Mari, Muriel, Holstege, Frank C.P., Klose, Christian, de Kroon, Anton I.P.M., Sub Membrane Biochemistry & Biophysics, Sub Cryo - EM, Membrane Biochemistry and Biophysics, Bao, Xue, Koorengevel, Martijn C., Groot Koerkamp, Marian J.A., Homavar, Amir, Weijn, Amrah, Crielaard, Stefan, Renne, Mike F., Lorent, Joseph H., Geerts, Willie J.C., Surma, Michal A., Mari, Muriel, Holstege, Frank C.P., Klose, Christian, and de Kroon, Anton I.P.M.

Published
2021

16. Acyl chain shortening induced by inhibition of acetyl-CoA carboxylase renders phosphatidylcholine redundant

Author

Bao, Xue, primary, Koorengevel, Martijn C., additional, Koerkamp, Marian J.A. Groot, additional, Homavar, Amir, additional, Weijn, Amrah, additional, Crielaard, Stefan, additional, Renne, Mike F., additional, Geerts, Willie J.C., additional, Surma, Michal A., additional, Mari, Muriel, additional, Holstege, Frank C.P., additional, Klose, Christian, additional, and Kroon, Anton I.P.M. de, additional

Published
2021
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19. Factors influencing the solubilization of membrane proteins from Escherichia coli membranes by styrene–maleic acid copolymers

Author

Sub Membrane Biochemistry & Biophysics, Membrane Biochemistry and Biophysics, Kopf, Adrian H., Dörr, Jonas M., Koorengevel, Martijn C., Antoniciello, Federico, Jahn, Helene, Killian, J. Antoinette, Sub Membrane Biochemistry & Biophysics, Membrane Biochemistry and Biophysics, Kopf, Adrian H., Dörr, Jonas M., Koorengevel, Martijn C., Antoniciello, Federico, Jahn, Helene, and Killian, J. Antoinette

Published
2020

20. Acidic interaction of the Colicin A pore-forming domain with model membranes of Escherichia coli lipids results in a large perturbation of acyl chain order and stabilization of the bilayer

Author

Geli, Vincent, Koorengevel, Martijn C., Demel, Rudy A., Lazdunski, Claude, and Killian, J. Antoinette

Subjects
Escherichia coli -- Research, Cell membranes -- Research, Toxins -- Research, Biological sciences, Chemistry
Abstract

The effects of the pore-forming domain of colicin A on acyl chain order and lipid organization of model membrane system derived from Escherichia coli were investigated using nuclear magnetic resonance (NMR) methods. A fatty acid auxotrophic mutant of E. coli was grown in the presence of deuterium-labeled oleic acid and was used for the NMR study. The colicin A pore-forming domain was inserted in the membrane and catalyzed at acidic pH. A major perturbing effect on acyl chain order was observed upon insertion of the pore-forming colicins but bilayer organization remained unaffected and exhibited stability.

Published
1992

22. A simple and convenient method for the hydrolysis of styrene-maleic anhydride copolymers to styrene-maleic acid copolymers

Author

Kopf, Adrian H, Koorengevel, Martijn C, van Walree, Cornelis A, Dafforn, Timothy R, Killian, J Antoinette, Kopf, Adrian H, Koorengevel, Martijn C, van Walree, Cornelis A, Dafforn, Timothy R, and Killian, J Antoinette

Abstract

Styrene-maleic acid (SMA) copolymers are increasingly gaining attention in the membrane protein field due to their ability to solubilize lipid membranes into discoidal nanoparticles. The copolymers are synthesized as styrene-maleic anhydride (SMAnh), and need to be converted to the free acid form (SMA) before they are capable of solubilizing membranes. This hydrolysis reaction is traditionally performed under rather cumbersome reflux conditions. Here we report an alternative method for the hydrolysis reaction using simple and readily available equipment found in virtually all biochemical laboratories, namely an autoclave. Based on the results we propose an optimum set of standard conditions for the hydrolysis reaction, that should make the method easily accessible to a wide scope of researchers.

Published
2019

23. A simple and convenient method for the hydrolysis of styrene-maleic anhydride copolymers to styrene-maleic acid copolymers

Author

Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Kopf, Adrian H, Koorengevel, Martijn C, van Walree, Cornelis A, Dafforn, Timothy R, Killian, J Antoinette, Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Kopf, Adrian H, Koorengevel, Martijn C, van Walree, Cornelis A, Dafforn, Timothy R, and Killian, J Antoinette

Published
2019

25. Membrane Solubilization by Styrene-Maleic Acid Copolymers: Delineating the Role of Polymer Length

Author

Domínguez Pardo, Juan J, Koorengevel, Martijn C, Uwugiaren, Naomi, Weijers, Jeroen, Kopf, Adrian H, Jahn, Helene, van Walree, Cornelis A, van Steenbergen, Mies J, Killian, J Antoinette, Domínguez Pardo, Juan J, Koorengevel, Martijn C, Uwugiaren, Naomi, Weijers, Jeroen, Kopf, Adrian H, Jahn, Helene, van Walree, Cornelis A, van Steenbergen, Mies J, and Killian, J Antoinette

Abstract

Styrene-maleic acid (SMA) copolymers have attracted interest in membrane research because they allow the solubilization and purification of membrane-spanning proteins from biological membranes in the form of native-like nanodisks. However, our understanding of the underlying SMA-lipid interactions is hampered by the fact that SMA preparations are very polydisperse. Here, we obtained fractions of the two most commonly used SMA preparations: SMA 2:1 and SMA 3:1 (both with specified Mw ∼10 kD), with different number-average molecular weight (Mn) and styrene content. The fractionation is based on the differential solubility of styrene-maleic anhydride (SMAnh) in hexane and acetone mixtures. SMAnh fractions were hydrolyzed to SMA and added to lipid self-assemblies. It was found that SMA fractions inserted in monolayers and solubilized vesicles to a different extent, with the highest efficiency being observed for low-Mn SMA polymers. Electron microscopy and dynamic light scattering size analyses confirmed the presence of nanodisks independent of the Mn of the SMA polymers forming the belt, and it was shown that the nanodisks all have approximately the same size. However, nanodisks bounded by high-Mn SMA polymers were more stable than those bounded by low-Mn polymers, as indicated by a better retention of the native lipid thermotropic properties and by slower exchange rates of lipids between nanodisks. In conclusion, we here present a simple method to separate SMAnh molecules based on their Mn from commercial SMAnh blends, which allowed us to obtain insights into the importance of SMA length for polymer-lipid interactions.

Published
2018

26. Membrane Solubilization by Styrene-Maleic Acid Copolymers: Delineating the Role of Polymer Length

Author

Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Afd Pharmaceutics, Pharmaceutics, Domínguez Pardo, Juan J, Koorengevel, Martijn C, Uwugiaren, Naomi, Weijers, Jeroen, Kopf, Adrian H, Jahn, Helene, van Walree, Cornelis A, van Steenbergen, Mies J, Killian, J Antoinette, Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Afd Pharmaceutics, Pharmaceutics, Domínguez Pardo, Juan J, Koorengevel, Martijn C, Uwugiaren, Naomi, Weijers, Jeroen, Kopf, Adrian H, Jahn, Helene, van Walree, Cornelis A, van Steenbergen, Mies J, and Killian, J Antoinette

Published
2018

27. The styrene-maleic acid copolymer:: a versatile tool in membrane research

Author

Dörr, Jonas M, Scheidelaar, Stefan, Koorengevel, Martijn C, Dominguez Pardo, Juan, Schäfer, Marre, van Walree, Cornelis A, Killian, J Antoinette, Membrane Biochemistry and Biophysics, and Sub Membrane Biochemistry & Biophysics

Subjects
Membrane proteins, Styrene–maleic acid copolymers, Lipodisq, Native nanodiscs, SMALPs Lipid–protein interactions
Abstract

A new and promising tool in membrane research is the detergent-free solubilization of membrane proteins by styrene-maleic acid copolymers (SMAs). These amphipathic molecules are able to solubilize lipid bilayers in the form of nanodiscs that are bounded by the polymer. Thus, membrane proteins can be directly extracted from cells in a water-soluble form while conserving a patch of native membrane around them. In this review article, we briefly discuss current methods of membrane protein solubilization and stabilization. We then zoom in on SMAs, describe their physico-chemical properties, and discuss their membrane-solubilizing effect. This is followed by an overview of studies in which SMA has been used to isolate and investigate membrane proteins. Finally, potential future applications of the methodology are discussed for structural and functional studies on membrane proteins in a near-native environment and for characterizing protein-lipid and protein-protein interactions.

Published
2016

30. Solubilization of lipids and lipid phases by the styrene-maleic acid copolymer

Author

Dominguez Pardo, Juan J, Dörr, Jonas M, Iyer, Aditya, Cox, Ruud C, Scheidelaar, Stefan, Koorengevel, Martijn C, Subramaniam, Vinod, Killian, J Antoinette, Dominguez Pardo, Juan J, Dörr, Jonas M, Iyer, Aditya, Cox, Ruud C, Scheidelaar, Stefan, Koorengevel, Martijn C, Subramaniam, Vinod, and Killian, J Antoinette

Abstract

A promising tool in membrane research is the use of the styrene-maleic acid (SMA) copolymer to solubilize membranes in the form of nanodiscs. Since membranes are heterogeneous in composition, it is important to know whether SMA thereby has a preference for solubilization of either specific types of lipids or specific bilayer phases. Here, we investigated this by performing partial solubilization of model membranes and analyzing the lipid composition of the solubilized fraction. We found that SMA displays no significant lipid preference in homogeneous binary lipid mixtures in the fluid phase, even when using lipids that by themselves show very different solubilization kinetics. By contrast, in heterogeneous phase-separated bilayers, SMA was found to have a strong preference for solubilization of lipids in the fluid phase as compared to those in either a gel phase or a liquid-ordered phase. Together the results suggest that (1) SMA is a reliable tool to characterize native interactions between membrane constituents, (2) any solubilization preference of SMA is not due to properties of individual lipids but rather due to properties of the membrane or membrane domains in which these lipids reside and (3) exploiting SMA resistance rather than detergent resistance may be an attractive approach for the isolation of ordered domains from biological membranes.

Published
2017

31. Solubilization of lipids and lipid phases by the styrene-maleic acid copolymer

Author

Sub Membrane Biochemistry & Biophysics, Membrane Biochemistry and Biophysics, Dominguez Pardo, Juan J, Dörr, Jonas M, Iyer, Aditya, Cox, Ruud C, Scheidelaar, Stefan, Koorengevel, Martijn C, Subramaniam, Vinod, Killian, J Antoinette, Sub Membrane Biochemistry & Biophysics, Membrane Biochemistry and Biophysics, Dominguez Pardo, Juan J, Dörr, Jonas M, Iyer, Aditya, Cox, Ruud C, Scheidelaar, Stefan, Koorengevel, Martijn C, Subramaniam, Vinod, and Killian, J Antoinette

Published
2017

32. Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: The power of native nanodiscs

Author

Dörr, Jonas M, Koorengevel, Martijn C, Schäfer, Marre, Prokofyev, Alexander V, Scheidelaar, Stefan, van der Cruijsen, Elwin A W, Dafforn, Timothy R, Baldus, Marc, Killian, J Antoinette, Sub Membrane Biochemistry & Biophysics, Sub NMR Spectroscopy, NMR Spectroscopy, and Membrane Biochemistry and Biophysics

Abstract

A major obstacle in the study of membrane proteins is their solubilization in a stable and active conformation when using detergents. Here, we explored a detergent-free approach to isolating the tetrameric potassium channel KcsA directly from the membrane of Escherichia coli, using a styrene-maleic acid copolymer. This polymer self-inserts into membranes and is capable of extracting membrane patches in the form of nanosize discoidal proteolipid particles or "native nanodiscs." Using circular dichroism and tryptophan fluorescence spectroscopy, we show that the conformation of KcsA in native nanodiscs is very similar to that in detergent micelles, but that the thermal stability of the protein is higher in the nanodiscs. Furthermore, as a promising new application, we show that quantitative analysis of the co-isolated lipids in purified KcsA-containing nanodiscs allows determination of preferential lipid-protein interactions. Thin-layer chromatography experiments revealed an enrichment of the anionic lipids cardiolipin and phosphatidylglycerol, indicating their close proximity to the channel in biological membranes and supporting their functional relevance. Finally, we demonstrate that KcsA can be reconstituted into planar lipid bilayers directly from native nanodiscs, which enables functional characterization of the channel by electrophysiology without first depriving the protein of its native environment. Together, these findings highlight the potential of the use of native nanodiscs as a tool in the study of ion channels, and of membrane proteins in general.

Published
2014

33. Effect of Polymer Composition and pH on Membrane Solubilization by Styrene-Maleic Acid Copolymers

Author

Sub Membrane Biochemistry & Biophysics, Sub Practicum, Membrane Biochemistry and Biophysics, Scheidelaar, Stefan, Koorengevel, Martijn C, van Walree, Cornelius A, Dominguez Pardo, Juan, Dörr, Jonas M, Killian, J Antoinette, Sub Membrane Biochemistry & Biophysics, Sub Practicum, Membrane Biochemistry and Biophysics, Scheidelaar, Stefan, Koorengevel, Martijn C, van Walree, Cornelius A, Dominguez Pardo, Juan, Dörr, Jonas M, and Killian, J Antoinette

Published
2016

34. The styrene-maleic acid copolymer:: a versatile tool in membrane research

Author

Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Dörr, Jonas M, Scheidelaar, Stefan, Koorengevel, Martijn C, Dominguez Pardo, Juan, Schäfer, Marre, van Walree, Cornelis A, Killian, J Antoinette, Membrane Biochemistry and Biophysics, Sub Membrane Biochemistry & Biophysics, Dörr, Jonas M, Scheidelaar, Stefan, Koorengevel, Martijn C, Dominguez Pardo, Juan, Schäfer, Marre, van Walree, Cornelis A, and Killian, J Antoinette

Published
2016

40. Cowpox virus protein CPXV012 eludes CTLs by blocking ATP binding to TAP

Author

Membrane Biochemistry and Biophysics, LS Virologie, Sub Membrane Biochemistry & Biophysics, Luteijn, Rutger D., Hoelen, Hanneke, Kruse, Elisabeth, van Leeuwen, Wouter F., Grootens, Jennine, Horst, Daniëlle, Koorengevel, Martijn, Drijfhout, Jan W., Kremmer, Elisabeth, Früh, Klaus, Neefjes, Jacques J., Killian, Antoinette, Lebbink, Robert Jan, Ressing, Maaike E., Wiertz, Emmanuel J H J, Membrane Biochemistry and Biophysics, LS Virologie, Sub Membrane Biochemistry & Biophysics, Luteijn, Rutger D., Hoelen, Hanneke, Kruse, Elisabeth, van Leeuwen, Wouter F., Grootens, Jennine, Horst, Daniëlle, Koorengevel, Martijn, Drijfhout, Jan W., Kremmer, Elisabeth, Früh, Klaus, Neefjes, Jacques J., Killian, Antoinette, Lebbink, Robert Jan, Ressing, Maaike E., and Wiertz, Emmanuel J H J

Published
2014

41. Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: The power of native nanodiscs

Author

Sub Membrane Biochemistry & Biophysics, Sub NMR Spectroscopy, NMR Spectroscopy, Membrane Biochemistry and Biophysics, Dörr, Jonas M, Koorengevel, Martijn C, Schäfer, Marre, Prokofyev, Alexander V, Scheidelaar, Stefan, van der Cruijsen, Elwin A W, Dafforn, Timothy R, Baldus, Marc, Killian, J Antoinette, Sub Membrane Biochemistry & Biophysics, Sub NMR Spectroscopy, NMR Spectroscopy, Membrane Biochemistry and Biophysics, Dörr, Jonas M, Koorengevel, Martijn C, Schäfer, Marre, Prokofyev, Alexander V, Scheidelaar, Stefan, van der Cruijsen, Elwin A W, Dafforn, Timothy R, Baldus, Marc, and Killian, J Antoinette

Published
2014

43. Cowpox Virus Protein CPXV012 Eludes CTLs by Blocking ATP Binding to TAP

Author

Luteijn, Rutger D., primary, Hoelen, Hanneke, additional, Kruse, Elisabeth, additional, van Leeuwen, Wouter F., additional, Grootens, Jennine, additional, Horst, Daniëlle, additional, Koorengevel, Martijn, additional, Drijfhout, Jan W., additional, Kremmer, Elisabeth, additional, Früh, Klaus, additional, Neefjes, Jacques J., additional, Killian, Antoinette, additional, Lebbink, Robert Jan, additional, Ressing, Maaike E., additional, and Wiertz, Emmanuel J. H. J., additional

Published
2014
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