The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study

Stephen C.L. Hall; Cecilia Tognoloni; Richard A. Campbell; Joanna Richens; Paul O'Shea; Ann E. Terry; Gareth J. Price; Tim R. Dafforn; Karen J. Edler; Thomas Arnold

doi:10.1016/j.jcis.2022.03.102

The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study

Stephen C.L. Hall, Cecilia Tognoloni, Richard A. Campbell, Joanna Richens, Paul O'Shea, Ann E. Terry, Gareth J. Price, Tim R. Dafforn, Karen J. Edler, Thomas Arnold

Research output: Contribution to journal › Article › peer-review

7 Citations (SciVal)

Abstract

Hypothesis: Self-assembly of amphipathic styrene maleic acid copolymers with phospholipids in aqueous solution results in the formation of ‘nanodiscs’ containing a planar segment of phospholipid bilayer encapsulated by a polymer belt. Recently, studies have reported that lipids rapidly exchange between both nanodiscs in solution and external sources of lipids. Outstanding questions remain regarding details of polymer-lipid interactions, factors influencing lipid exchange and structural effects of such exchange processes. Here, the dynamic behaviour of nanodiscs is investigated, specifically the role of membrane charge and polymer chemistry. Experiments: Two model systems are investigated: fluorescently labelled phospholipid vesicles, and Langmuir monolayers of phospholipids. Using fluorescence spectroscopy and time-resolved neutron reflectometry, the membrane potential, monolayer structure and composition are monitored with respect to time upon polymer and nanodisc interactions. Findings: In the presence of external lipids, polymer chains embed throughout lipid membranes, the extent of which is governed by the net membrane charge. Nanodiscs stabilised by three different polymers will all exchange lipids and polymer with monolayers to differing extents, related to the properties of the stabilising polymer belt. These results demonstrate the dynamic nature of nanodiscs which interact with the local environment and are likely to deposit both lipids and polymer at all stages of use.

Original language	English
Pages (from-to)	220-236
Number of pages	17
Journal	Journal of Colloid and Interface Science
Volume	625
Early online date	31 Mar 2022
DOIs	https://doi.org/10.1016/j.jcis.2022.03.102
Publication status	Published - 30 Nov 2022

Bibliographical note

Funding Information:
This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74]. We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation.

Funding Information:
This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990 ) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74] . We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation.

Funding

This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74]. We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation. This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990 ) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74] . We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation.

Keywords

Adsorption
Langmuir monolayer
Lipid Exchange
Nanodisc
Neutron reflectometry
Polymer
Reversible, Addition−Fragmentation Chain-Transfer (RAFT)
Styrene Maleic Acid (SMA)
Styrene Maleic Acid Lipid Particle (SMALP)

ASJC Scopus subject areas

Electronic, Optical and Magnetic Materials
Biomaterials
Surfaces, Coatings and Films
Colloid and Surface Chemistry

Access to Document

10.1016/j.jcis.2022.03.102Licence: CC BY

Cite this

Hall, S. C. L., Tognoloni, C., Campbell, R. A., Richens, J., O'Shea, P., Terry, A. E., Price, G. J., Dafforn, T. R., Edler, K. J., & Arnold, T. (2022). The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study. Journal of Colloid and Interface Science, 625, 220-236. https://doi.org/10.1016/j.jcis.2022.03.102

Hall, SCL, Tognoloni, C, Campbell, RA, Richens, J, O'Shea, P, Terry, AE, Price, GJ, Dafforn, TR, Edler, KJ & Arnold, T 2022, 'The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study', Journal of Colloid and Interface Science, vol. 625, pp. 220-236. https://doi.org/10.1016/j.jcis.2022.03.102

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title = "The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study",

abstract = "Hypothesis: Self-assembly of amphipathic styrene maleic acid copolymers with phospholipids in aqueous solution results in the formation of {\textquoteleft}nanodiscs{\textquoteright} containing a planar segment of phospholipid bilayer encapsulated by a polymer belt. Recently, studies have reported that lipids rapidly exchange between both nanodiscs in solution and external sources of lipids. Outstanding questions remain regarding details of polymer-lipid interactions, factors influencing lipid exchange and structural effects of such exchange processes. Here, the dynamic behaviour of nanodiscs is investigated, specifically the role of membrane charge and polymer chemistry. Experiments: Two model systems are investigated: fluorescently labelled phospholipid vesicles, and Langmuir monolayers of phospholipids. Using fluorescence spectroscopy and time-resolved neutron reflectometry, the membrane potential, monolayer structure and composition are monitored with respect to time upon polymer and nanodisc interactions. Findings: In the presence of external lipids, polymer chains embed throughout lipid membranes, the extent of which is governed by the net membrane charge. Nanodiscs stabilised by three different polymers will all exchange lipids and polymer with monolayers to differing extents, related to the properties of the stabilising polymer belt. These results demonstrate the dynamic nature of nanodiscs which interact with the local environment and are likely to deposit both lipids and polymer at all stages of use.",

keywords = "Adsorption, Langmuir monolayer, Lipid Exchange, Nanodisc, Neutron reflectometry, Polymer, Reversible, Addition−Fragmentation Chain-Transfer (RAFT), Styrene Maleic Acid (SMA), Styrene Maleic Acid Lipid Particle (SMALP)",

author = "Hall, {Stephen C.L.} and Cecilia Tognoloni and Campbell, {Richard A.} and Joanna Richens and Paul O'Shea and Terry, {Ann E.} and Price, {Gareth J.} and Dafforn, {Tim R.} and Edler, {Karen J.} and Thomas Arnold",

note = "Funding Information: This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74]. We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation. Funding Information: This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990 ) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74] . We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation. ",

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T1 - The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study

AU - Hall, Stephen C.L.

AU - Tognoloni, Cecilia

AU - Campbell, Richard A.

AU - Richens, Joanna

AU - O'Shea, Paul

AU - Terry, Ann E.

AU - Price, Gareth J.

AU - Dafforn, Tim R.

AU - Edler, Karen J.

AU - Arnold, Thomas

N1 - Funding Information: This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74]. We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation. Funding Information: This work has been supported by an Engineering and Physical Sciences Research Council (EPSRC: EP/M506461/1) and Diamond Light Source studentship for SCLH and funding from the Biotechnology and Biological Sciences Research Council (BBSRC: BB/M018261/1 [TRD]). CT acknowledges STFC BioMedNet (studentship agreement #2990 ) and the University of Bath for PhD studentship funding. We thank the Institut Laue-Langevin for beamtime allocations using FIGARO (Experiment numbers 9-12-458 and 9-12-457) [73,74] . We also thank Bert Klumperman for assistance with RAFT-SMA synthesis and George Neville for assistance with polymer characterisation.

PY - 2022/11/30

Y1 - 2022/11/30

N2 - Hypothesis: Self-assembly of amphipathic styrene maleic acid copolymers with phospholipids in aqueous solution results in the formation of ‘nanodiscs’ containing a planar segment of phospholipid bilayer encapsulated by a polymer belt. Recently, studies have reported that lipids rapidly exchange between both nanodiscs in solution and external sources of lipids. Outstanding questions remain regarding details of polymer-lipid interactions, factors influencing lipid exchange and structural effects of such exchange processes. Here, the dynamic behaviour of nanodiscs is investigated, specifically the role of membrane charge and polymer chemistry. Experiments: Two model systems are investigated: fluorescently labelled phospholipid vesicles, and Langmuir monolayers of phospholipids. Using fluorescence spectroscopy and time-resolved neutron reflectometry, the membrane potential, monolayer structure and composition are monitored with respect to time upon polymer and nanodisc interactions. Findings: In the presence of external lipids, polymer chains embed throughout lipid membranes, the extent of which is governed by the net membrane charge. Nanodiscs stabilised by three different polymers will all exchange lipids and polymer with monolayers to differing extents, related to the properties of the stabilising polymer belt. These results demonstrate the dynamic nature of nanodiscs which interact with the local environment and are likely to deposit both lipids and polymer at all stages of use.

AB - Hypothesis: Self-assembly of amphipathic styrene maleic acid copolymers with phospholipids in aqueous solution results in the formation of ‘nanodiscs’ containing a planar segment of phospholipid bilayer encapsulated by a polymer belt. Recently, studies have reported that lipids rapidly exchange between both nanodiscs in solution and external sources of lipids. Outstanding questions remain regarding details of polymer-lipid interactions, factors influencing lipid exchange and structural effects of such exchange processes. Here, the dynamic behaviour of nanodiscs is investigated, specifically the role of membrane charge and polymer chemistry. Experiments: Two model systems are investigated: fluorescently labelled phospholipid vesicles, and Langmuir monolayers of phospholipids. Using fluorescence spectroscopy and time-resolved neutron reflectometry, the membrane potential, monolayer structure and composition are monitored with respect to time upon polymer and nanodisc interactions. Findings: In the presence of external lipids, polymer chains embed throughout lipid membranes, the extent of which is governed by the net membrane charge. Nanodiscs stabilised by three different polymers will all exchange lipids and polymer with monolayers to differing extents, related to the properties of the stabilising polymer belt. These results demonstrate the dynamic nature of nanodiscs which interact with the local environment and are likely to deposit both lipids and polymer at all stages of use.

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KW - Langmuir monolayer

KW - Lipid Exchange

KW - Nanodisc

KW - Neutron reflectometry

KW - Polymer

KW - Reversible, Addition−Fragmentation Chain-Transfer (RAFT)

KW - Styrene Maleic Acid (SMA)

KW - Styrene Maleic Acid Lipid Particle (SMALP)

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The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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The interaction of styrene maleic acid copolymers with phospholipids in Langmuir monolayers, vesicles and nanodiscs; a structural study

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Equipment

HPLC System

Cite this