Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity

Helgi I. Ingólfsson; Harsh Bhatia; Talia Zeppelin; W. F.Drew Bennett; Kristy A. Carpenter; Pin Chia Hsu; Gautham Dharuman; Peer Timo Bremer; Birgit Schiøtt; Felice C. Lightstone; Timothy S. Carpenter

doi:10.1021/acs.jpcb.0c03368

Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity

Helgi I. Ingólfsson, Harsh Bhatia, Talia Zeppelin, W. F.Drew Bennett, Kristy A. Carpenter, Pin Chia Hsu, Gautham Dharuman, Peer Timo Bremer, Birgit Schiøtt, Felice C. Lightstone, Timothy S. Carpenter^*

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

41 Citations (Scopus)

Abstract

Plasma membranes (PMs) contain hundreds of different lipid species that contribute differently to overall bilayer properties. By modulation of these properties, membrane protein function can be affected. Furthermore, inhomogeneous lipid mixing and domains of lipid enrichment/depletion can sort proteins and provide optimal local environments. Recent coarse-grained (CG) Martini molecular dynamics efforts have provided glimpses into lipid organization of different PMs: an "Average" and a "Brain" PM. Their high complexity and large size require long simulations (∼80 μs) for proper sampling. Thus, these simulations are computationally taxing. This level of complexity is beyond the possibilities of all-atom simulations, raising the question-what complexity is needed for "realistic" bilayer properties? We constructed CG Martini PM models of varying complexity (63 down to 8 different lipids). Lipid tail saturations and headgroup combinations were kept as consistent as possible for the "tissues'" (Average/Brain) at three levels of compositional complexity. For each system, we analyzed membrane properties to evaluate which features can be retained at lower complexity and validate eight-component bilayers that can act as reliable mimetics for Average or Brain PMs. Systems of reduced complexity deliver a more robust and malleable tool for computational membrane studies and allow for equivalent all-atom simulations and experiments.

Original language	English
Journal	The journal of physical chemistry. B
Volume	124
Issue	36
Pages (from-to)	7819-7829
Number of pages	11
ISSN	1520-6106
DOIs	https://doi.org/10.1021/acs.jpcb.0c03368
Publication status	Published - Sept 2020

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https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7553384/pdf/jp0c03368.pdf

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Ingólfsson, H. I., Bhatia, H., Zeppelin, T., Bennett, W. F. D., Carpenter, K. A., Hsu, P. C., Dharuman, G., Bremer, P. T., Schiøtt, B., Lightstone, F. C., & Carpenter, T. S. (2020). Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity. The journal of physical chemistry. B, 124(36), 7819-7829. https://doi.org/10.1021/acs.jpcb.0c03368

@article{8727b7f84ef548dd94003f8470d181d8,

title = "Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity",

abstract = "Plasma membranes (PMs) contain hundreds of different lipid species that contribute differently to overall bilayer properties. By modulation of these properties, membrane protein function can be affected. Furthermore, inhomogeneous lipid mixing and domains of lipid enrichment/depletion can sort proteins and provide optimal local environments. Recent coarse-grained (CG) Martini molecular dynamics efforts have provided glimpses into lipid organization of different PMs: an {"}Average{"} and a {"}Brain{"} PM. Their high complexity and large size require long simulations (∼80 μs) for proper sampling. Thus, these simulations are computationally taxing. This level of complexity is beyond the possibilities of all-atom simulations, raising the question-what complexity is needed for {"}realistic{"} bilayer properties? We constructed CG Martini PM models of varying complexity (63 down to 8 different lipids). Lipid tail saturations and headgroup combinations were kept as consistent as possible for the {"}tissues'{"} (Average/Brain) at three levels of compositional complexity. For each system, we analyzed membrane properties to evaluate which features can be retained at lower complexity and validate eight-component bilayers that can act as reliable mimetics for Average or Brain PMs. Systems of reduced complexity deliver a more robust and malleable tool for computational membrane studies and allow for equivalent all-atom simulations and experiments.",

author = "Ing{\'o}lfsson, {Helgi I.} and Harsh Bhatia and Talia Zeppelin and Bennett, {W. F.Drew} and Carpenter, {Kristy A.} and Hsu, {Pin Chia} and Gautham Dharuman and Bremer, {Peer Timo} and Birgit Schi{\o}tt and Lightstone, {Felice C.} and Carpenter, {Timothy S.}",

year = "2020",

month = sep,

doi = "10.1021/acs.jpcb.0c03368",

language = "English",

volume = "124",

pages = "7819--7829",

journal = "The journal of physical chemistry. B",

issn = "1520-6106",

publisher = "American Chemical Society",

number = "36",

}

Ingólfsson, HI, Bhatia, H, Zeppelin, T, Bennett, WFD, Carpenter, KA, Hsu, PC, Dharuman, G, Bremer, PT, Schiøtt, B, Lightstone, FC & Carpenter, TS 2020, 'Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity', The journal of physical chemistry. B, vol. 124, no. 36, pp. 7819-7829. https://doi.org/10.1021/acs.jpcb.0c03368

Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity. / Ingólfsson, Helgi I.; Bhatia, Harsh; Zeppelin, Talia et al.
In: The journal of physical chemistry. B, Vol. 124, No. 36, 09.2020, p. 7819-7829.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity

AU - Ingólfsson, Helgi I.

AU - Bhatia, Harsh

AU - Zeppelin, Talia

AU - Bennett, W. F.Drew

AU - Carpenter, Kristy A.

AU - Hsu, Pin Chia

AU - Dharuman, Gautham

AU - Bremer, Peer Timo

AU - Schiøtt, Birgit

AU - Lightstone, Felice C.

AU - Carpenter, Timothy S.

PY - 2020/9

Y1 - 2020/9

N2 - Plasma membranes (PMs) contain hundreds of different lipid species that contribute differently to overall bilayer properties. By modulation of these properties, membrane protein function can be affected. Furthermore, inhomogeneous lipid mixing and domains of lipid enrichment/depletion can sort proteins and provide optimal local environments. Recent coarse-grained (CG) Martini molecular dynamics efforts have provided glimpses into lipid organization of different PMs: an "Average" and a "Brain" PM. Their high complexity and large size require long simulations (∼80 μs) for proper sampling. Thus, these simulations are computationally taxing. This level of complexity is beyond the possibilities of all-atom simulations, raising the question-what complexity is needed for "realistic" bilayer properties? We constructed CG Martini PM models of varying complexity (63 down to 8 different lipids). Lipid tail saturations and headgroup combinations were kept as consistent as possible for the "tissues'" (Average/Brain) at three levels of compositional complexity. For each system, we analyzed membrane properties to evaluate which features can be retained at lower complexity and validate eight-component bilayers that can act as reliable mimetics for Average or Brain PMs. Systems of reduced complexity deliver a more robust and malleable tool for computational membrane studies and allow for equivalent all-atom simulations and experiments.

AB - Plasma membranes (PMs) contain hundreds of different lipid species that contribute differently to overall bilayer properties. By modulation of these properties, membrane protein function can be affected. Furthermore, inhomogeneous lipid mixing and domains of lipid enrichment/depletion can sort proteins and provide optimal local environments. Recent coarse-grained (CG) Martini molecular dynamics efforts have provided glimpses into lipid organization of different PMs: an "Average" and a "Brain" PM. Their high complexity and large size require long simulations (∼80 μs) for proper sampling. Thus, these simulations are computationally taxing. This level of complexity is beyond the possibilities of all-atom simulations, raising the question-what complexity is needed for "realistic" bilayer properties? We constructed CG Martini PM models of varying complexity (63 down to 8 different lipids). Lipid tail saturations and headgroup combinations were kept as consistent as possible for the "tissues'" (Average/Brain) at three levels of compositional complexity. For each system, we analyzed membrane properties to evaluate which features can be retained at lower complexity and validate eight-component bilayers that can act as reliable mimetics for Average or Brain PMs. Systems of reduced complexity deliver a more robust and malleable tool for computational membrane studies and allow for equivalent all-atom simulations and experiments.

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U2 - 10.1021/acs.jpcb.0c03368

DO - 10.1021/acs.jpcb.0c03368

M3 - Journal article

C2 - 32790367

AN - SCOPUS:85090870663

SN - 1520-6106

VL - 124

SP - 7819

EP - 7829

JO - The journal of physical chemistry. B

JF - The journal of physical chemistry. B

IS - 36

ER -

Capturing Biologically Complex Tissue-Specific Membranes at Different Levels of Compositional Complexity

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