Mechanosensitive channel gating by delipidation.
MscS
cryoelectron microscopy
delipidation
force-from-lipid principle
lipid–protein interaction
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
17 08 2021
17 08 2021
Historique:
entrez:
11
8
2021
pubmed:
12
8
2021
medline:
15
12
2021
Statut:
ppublish
Résumé
The mechanosensitive channel of small conductance (MscS) protects bacteria against hypoosmotic shock. It can sense the tension in the surrounding membrane and releases solutes if the pressure in the cell is getting too high. The membrane contacts MscS at sensor paddles, but lipids also leave the membrane and move along grooves between the paddles to reside as far as 15 Å away from the membrane in hydrophobic pockets. One sensing model suggests that a higher tension pulls lipids from the grooves back to the membrane, which triggers gating. However, it is still unclear to what degree this model accounts for sensing and what contribution the direct interaction of the membrane with the channel has. Here, we show that MscS opens when it is sufficiently delipidated by incubation with the detergent dodecyl-β-maltoside or the branched detergent lauryl maltose neopentyl glycol. After addition of detergent-solubilized lipids, it closes again. These results support the model that lipid extrusion causes gating: Lipids are slowly removed from the grooves and pockets by the incubation with detergent, which triggers opening. Addition of lipids in micelles allows lipids to migrate back into the pockets, which closes the channel even in the absence of a membrane. Based on the distribution of the aliphatic chains in the open and closed conformation, we propose that during gating, lipids leave the complex on the cytosolic leaflet at the height of highest lateral tension, while on the periplasmic side, lipids flow into gaps, which open between transmembrane helices.
Identifiants
pubmed: 34376558
pii: 2107095118
doi: 10.1073/pnas.2107095118
pmc: PMC8379960
pii:
doi:
Substances chimiques
Lipids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Déclaration de conflit d'intérêts
The authors declare no competing interest.
Références
Biophys J. 2004 Jun;86(6):3496-509
pubmed: 15189849
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Structure. 2011 Oct 12;19(10):1356-69
pubmed: 22000509
Nat Struct Mol Biol. 2007 Dec;14(12):1141-9
pubmed: 18037888
Biophys J. 2014 Apr 15;106(8):1660-70
pubmed: 24739165
Nat Protoc. 2018 May;13(5):1106-1120
pubmed: 29700483
Proc Natl Acad Sci U S A. 2012 May 29;109(22):8770-5
pubmed: 22586095
Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3614-9
pubmed: 24550493
Biochem Soc Trans. 2016 Aug 15;44(4):1019-25
pubmed: 27528747
J Biol Chem. 2011 Jan 7;286(1):877-88
pubmed: 20978126
Nat Methods. 2012 Sep;9(9):853-4
pubmed: 22842542
Biochim Biophys Acta Biomembr. 2020 May 1;1862(5):183203
pubmed: 31981589
Biochemistry. 2007 Sep 25;46(38):10899-908
pubmed: 17718516
Nat Protoc. 2013 Apr;8(4):639-51
pubmed: 23471109
Nat Struct Mol Biol. 2010 Apr;17(4):451-8
pubmed: 20208543
Can J Biochem Physiol. 1959 Aug;37(8):911-7
pubmed: 13671378
Nat Struct Mol Biol. 2005 Feb;12(2):113-9
pubmed: 15665866
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Biophys J. 2008 Apr 15;94(8):3003-13
pubmed: 18065458
J Struct Biol. 2015 Nov;192(2):216-21
pubmed: 26278980
Nat Commun. 2016 Jun 22;7:11984
pubmed: 27329693
Nature. 2021 Feb;590(7846):509-514
pubmed: 33568813
Annu Rev Plant Biol. 2015;66:113-37
pubmed: 25494462
J Mol Biol. 2019 Aug 9;431(17):3081-3090
pubmed: 31291591
Biochim Biophys Acta Biomembr. 2019 May 1;1861(5):939-957
pubmed: 30776334
Proc Natl Acad Sci U S A. 2020 Nov 17;117(46):28754-28762
pubmed: 33148804
Nature. 2009 May 21;459(7245):379-85
pubmed: 19458714
EMBO J. 2003 Jan 2;22(1):36-46
pubmed: 12505982
Ultramicroscopy. 2019 Aug;203:145-154
pubmed: 30738626
Elife. 2019 Dec 27;8:
pubmed: 31880537
Channels (Austin). 2012 Jul-Aug;6(4):272-81
pubmed: 22874652
Biochemistry. 2007 May 1;46(17):5200-8
pubmed: 17407265
Biochem J. 1964 Feb;90(2):374-8
pubmed: 4284220
Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):E2675-82
pubmed: 23012406
Elife. 2018 Nov 01;7:
pubmed: 30382938
Protein Sci. 2016 Nov;25(11):1954-1964
pubmed: 27530280
Protein Sci. 2021 Jan;30(1):70-82
pubmed: 32881101
J Biol Chem. 2010 Feb 19;285(8):5377-84
pubmed: 20037156
Microbiol Mol Biol Rev. 2020 Jan 15;84(1):
pubmed: 31941768
Cell Rep. 2016 Nov 8;17(7):1739-1746
pubmed: 27829145
Biochemistry. 1982 Aug 17;21(17):4144-51
pubmed: 6127102
EMBO J. 1999 Apr 1;18(7):1730-7
pubmed: 10202137
Biophys J. 2002 Jul;83(1):290-8
pubmed: 12080120
Nat Chem. 2015 Mar;7(3):255-62
pubmed: 25698336
Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11652-7
pubmed: 8876191
Biophys J. 1993 Jul;65(1):177-83
pubmed: 7690260
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Elife. 2020 Mar 03;9:
pubmed: 32125274
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Nat Struct Mol Biol. 2015 Dec;22(12):991-8
pubmed: 26551077
J Mol Biol. 2019 Aug 9;431(17):3339-3352
pubmed: 31173776
Methods Enzymol. 1975;35:396-425
pubmed: 164604
Biochemistry. 2020 Jun 16;59(23):2125-2134
pubmed: 32437610
Annu Rev Physiol. 2018 Feb 10;80:71-93
pubmed: 29195054
Protein Sci. 2013 Apr;22(4):502-9
pubmed: 23339071
J Struct Biol. 2015 Feb;189(2):114-22
pubmed: 25486611
Commun Biol. 2019 Jun 19;2:218
pubmed: 31240256
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
Science. 2008 Aug 29;321(5893):1179-83
pubmed: 18755969
Microbiol Mol Biol Rev. 2003 Mar;67(1):66-85, table of contents
pubmed: 12626684
Biochemistry. 2015 Jul 28;54(29):4519-30
pubmed: 26126964
Science. 2002 Nov 22;298(5598):1582-7
pubmed: 12446901
J Mol Biol. 2008 Apr 18;378(1):55-70
pubmed: 18343404
Annu Rev Physiol. 1997;59:633-57
pubmed: 9074781
J Membr Biol. 1998 Aug 1;164(3):253-62
pubmed: 9691118
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701