Lipid packing in biological membranes governs protein localization and membrane permeability.
Journal
Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626
Informations de publication
Date de publication:
11 07 2023
11 07 2023
Historique:
received:
16
12
2022
revised:
18
04
2023
accepted:
25
05
2023
pmc-release:
11
07
2024
medline:
14
7
2023
pubmed:
31
5
2023
entrez:
31
5
2023
Statut:
ppublish
Résumé
Plasma membrane (PM) heterogeneity has long been implicated in various cellular functions. However, mechanistic principles governing functional regulations of lipid environment are not well understood due to the inherent complexities associated with the relevant length and timescales that limit both direct experimental measurements and their interpretation. In this context, computer simulations hold immense potential to investigate molecular-level interactions and mechanisms that lead to PM heterogeneity and its functions. Herein, we investigate spatial and dynamic heterogeneity in model membranes with coexisting liquid ordered and liquid disordered phases and characterize the membrane order in terms of the local topological changes in lipid environment using the nonaffine deformation framework. Furthermore, we probe the packing defects in these membranes, which can be considered as the conjugate of membrane order assessed in terms of the nonaffine parameter. In doing so, we formalize the connection between membrane packing and local membrane order and use that to explore the mechanistic principles behind their functions. Our observations suggest that heterogeneity in mixed phase membranes is a consequence of local lipid topology and its temporal evolution, which give rise to disparate lipid packing in ordered and disordered domains. This in turn governs the distinct nature of packing defects in these domains that can play a crucial role in preferential localization of proteins in mixed phase membranes. Furthermore, we observe that lipid packing also leads to contrasting distribution of free volume in the membrane core region in ordered and disordered membranes, which can lead to distinctive membrane permeability of small molecules. Our results, thus, indicate that heterogeneity in mixed phase membranes closely governs the membrane functions that may emerge from packing-related basic design principles.
Identifiants
pubmed: 37254482
pii: S0006-3495(23)00340-5
doi: 10.1016/j.bpj.2023.05.028
pmc: PMC10397809
pii:
doi:
Substances chimiques
Lipid Bilayers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2727-2743Informations de copyright
Copyright © 2023 Biophysical Society. Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
J Exp Med. 1925 Mar 31;41(4):439-43
pubmed: 19868999
Biophys J. 2005 Jul;89(1):745-52
pubmed: 15951371
Nat Commun. 2019 Dec 9;10(1):5616
pubmed: 31819053
Annu Rev Phys Chem. 2021 Apr 20;72:51-72
pubmed: 33710910
Soft Matter. 2020 Aug 7;16(29):6752-6764
pubmed: 32628232
Biophys J. 2003 Nov;85(5):3074-83
pubmed: 14581208
Cell Microbiol. 2005 May;7(5):613-20
pubmed: 15839890
Annu Rev Biophys Biomol Struct. 2005;34:351-78
pubmed: 15869394
Biophys J. 2001 Nov;81(5):2484-94
pubmed: 11606264
J Biol Chem. 2005 May 13;280(19):18931-42
pubmed: 15753089
Annu Rev Biophys. 2012;41:429-52
pubmed: 22577825
Biophys J. 2018 Jul 3;115(1):117-128
pubmed: 29972803
Proc Natl Acad Sci U S A. 2020 Aug 18;117(33):19943-19952
pubmed: 32759206
J Phys Chem B. 2018 Oct 25;122(42):9713-9723
pubmed: 30281310
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
Biophys J. 2016 Apr 26;110(8):1800-1810
pubmed: 27119640
J Cell Sci. 2016 Jan 15;129(2):257-68
pubmed: 26743083
Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22050-4
pubmed: 21131568
Soft Matter. 2015 Dec 21;11(47):9055-72
pubmed: 26428538
Biophys J. 2018 Aug 7;115(3):436-444
pubmed: 30055754
Annu Rev Biophys Biomol Struct. 2004;33:269-95
pubmed: 15139814
Nat Rev Mol Cell Biol. 2023 Feb;24(2):107-122
pubmed: 36056103
J Phys Chem B. 2020 Feb 27;124(8):1487-1494
pubmed: 32026676
Biophys J. 2013 Feb 5;104(3):575-84
pubmed: 23442908
Biochim Biophys Acta. 2014 Jun;1838(6):1451-66
pubmed: 24189436
Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8500-5
pubmed: 24912166
Traffic. 2018 Jul;19(7):536-545
pubmed: 29573133
J Lipid Res. 2006 Jul;47(7):1597-8
pubmed: 16645198
Trends Biochem Sci. 2005 Aug;30(8):430-6
pubmed: 15996869
Nat Rev Mol Cell Biol. 2010 Aug;11(8):593-8
pubmed: 20606693
Dev Cell. 2018 Jan 08;44(1):73-86.e4
pubmed: 29316443
Nat Commun. 2016 May 26;7:11701
pubmed: 27226072
Elife. 2017 Feb 01;6:
pubmed: 28145867
Front Plant Sci. 2019 Feb 21;10:198
pubmed: 30846999
Biochim Biophys Acta. 2009 Jan;1788(1):97-121
pubmed: 18823938
J Comput Chem. 2005 Dec;26(16):1781-802
pubmed: 16222654
J Am Chem Soc. 2014 Jan 15;136(2):725-32
pubmed: 24345334
Nat Commun. 2022 Mar 25;13(1):1605
pubmed: 35338137
Biophys J. 2018 Apr 24;114(8):1936-1944
pubmed: 29694870
Biochemistry. 2007 Feb 20;46(7):1779-90
pubmed: 17253781
Soft Matter. 2021 Jul 28;17(29):6910-6928
pubmed: 34235519
Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1343-8
pubmed: 21205902
Annu Rev Biophys Biomol Struct. 2003;32:257-83
pubmed: 12543707
Sci Rep. 2017 Apr 25;7(1):1143
pubmed: 28442766
Biochemistry. 2004 Dec 14;43(49):15318-28
pubmed: 15581344
Cell. 2004 Feb 20;116(4):577-89
pubmed: 14980224
Trends Cell Biol. 2013 Jan;23(1):1-8
pubmed: 22980035
J Chem Theory Comput. 2020 Dec 8;16(12):7800-7816
pubmed: 33226805
Nat Commun. 2020 Nov 27;11(1):6060
pubmed: 33247142
J Comput Chem. 2009 Jul 30;30(10):1545-614
pubmed: 19444816
Phys Rev Lett. 2012 Nov 2;109(18):188103
pubmed: 23215336
Trends Biochem Sci. 2016 Nov;41(11):954-969
pubmed: 27663237
J Cell Sci. 2011 Jan 1;124(Pt 1):5-8
pubmed: 21172818
Br J Anaesth. 2015 Apr;114(4):537-41
pubmed: 25788629
Biophys J. 2005 Jun;88(6):4434-8
pubmed: 15805166
Biophys J. 2011 Mar 2;100(5):1271-9
pubmed: 21354400
Appl Magn Reson. 2021 Oct;52(10):1237-1260
pubmed: 36267674
Proc Natl Acad Sci U S A. 2022 Jul 26;119(30):e2123056119
pubmed: 35867835
Semin Cell Dev Biol. 2007 Oct;18(5):573-82
pubmed: 17942350
R Soc Open Sci. 2018 Feb 28;5(2):171710
pubmed: 29515878
EMBO J. 2005 Jul 6;24(13):2244-53
pubmed: 15944734
Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3165-70
pubmed: 17360623
Faraday Discuss. 2013;161:347-63; discussion 419-59
pubmed: 23805749
Science. 1972 Feb 18;175(4023):720-31
pubmed: 4333397
Biophys J. 2013 Feb 5;104(3):585-93
pubmed: 23442909
Traffic. 2004 Apr;5(4):231-40
pubmed: 15030564
Cell. 2012 Jun 8;149(6):1353-67
pubmed: 22682254
J Biol Chem. 2022 Jul;298(7):102136
pubmed: 35714773
J Biol Chem. 2017 Jun 30;292(26):10755-10766
pubmed: 28490630
Chem Phys Lipids. 2020 Nov;233:104991
pubmed: 33121937
Nat Commun. 2016 Apr 26;7:11401
pubmed: 27113279
Dev Cell. 2012 Nov 13;23(5):886-95
pubmed: 23153485
Science. 2010 Jan 1;327(5961):46-50
pubmed: 20044567
J Phys Chem B. 2010 Jun 17;114(23):7830-43
pubmed: 20496934
Biophys J. 2004 Aug;87(2):1076-91
pubmed: 15298912
Annu Rev Biochem. 2014;83:79-98
pubmed: 24606142
Soft Matter. 2021 Sep 14;17(34):7963-7977
pubmed: 34378608
J Chem Theory Comput. 2017 Jun 13;13(6):2962-2976
pubmed: 28482659
Protein Sci. 2020 Jun;29(6):1355-1365
pubmed: 32297381
J Mol Biol. 1973 Sep 15;79(2):351-71
pubmed: 4760134
Nat Rev Mol Cell Biol. 2017 Jun;18(6):361-374
pubmed: 28356571
J Chem Phys. 2020 Sep 28;153(12):124107
pubmed: 33003739
Nat Rev Mol Cell Biol. 2015 Dec;16(12):753-61
pubmed: 26507169
Biophys J. 1999 Apr;76(4):2081-9
pubmed: 10096903
Biochemistry. 1992 Jul 28;31(29):6739-47
pubmed: 1637810
Biochim Biophys Acta. 2009 Jan;1788(1):47-52
pubmed: 18805392
Biophys J. 2023 Jun 6;122(11):2256-2266
pubmed: 36641625
Biophys J. 2017 Jun 6;112(11):2336-2347
pubmed: 28591606
Trends Cell Biol. 2020 May;30(5):341-353
pubmed: 32302547
Nature. 1997 Jun 5;387(6633):569-72
pubmed: 9177342
J Phys Chem Lett. 2019 May 2;10(9):2024-2030
pubmed: 30964299
J Mol Biol. 2016 Dec 4;428(24 Pt A):4749-4764
pubmed: 27575334
Proc Natl Acad Sci U S A. 2020 Aug 18;117(33):19713-19719
pubmed: 32759217
Nat Commun. 2014 Sep 15;5:4916
pubmed: 25222832
Biophys J. 2015 Sep 1;109(5):948-55
pubmed: 26331252
J Membr Biol. 2020 Dec;253(6):551-562
pubmed: 33170308
Nature. 2009 Feb 26;457(7233):1159-62
pubmed: 19098897