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Molecular basis of force-from-lipids gating in the mechanosensitive channel MscS.

<div class='caption-title'>Structure of membrane-embedded MscS (MscS-ND) and its anchor domain.</div>
<div class='caption-title'>MscS Constructs, Nanodisc Composition, and Purification MscS Nanodiscs.</div>
<div class='caption-title'>Overview of MscS ND Density Refinement Workflow.</div>
Reddy B, Bavi N, Lu A, Park Y, Perozo E
OpenAccess logo Elife 8 (2019)
Related entries: 6pwo, 6pwp

Cited: 52 times
EuropePMC logo PMID: 31880537

Abstract

Prokaryotic mechanosensitive (MS) channels open by sensing the physical state of the membrane. As such, lipid-protein interactions represent the defining molecular process underlying mechanotransduction. Here, we describe cryo-electron microscopy (cryo-EM) structures of the E. coli small-conductance mechanosensitive channel (MscS) in nanodiscs (ND). They reveal a novel membrane-anchoring fold that plays a significant role in channel activation and establish a new location for the lipid bilayer, shifted ~14 Å from previous consensus placements. Two types of lipid densities are explicitly observed. A phospholipid that 'hooks' the top of each TM2-TM3 hairpin and likely plays a role in force sensing, and a bundle of acyl chains occluding the permeation path above the L105 cuff. These observations reshape our understanding of force-from-lipids gating in MscS and highlight the key role of allosteric interactions between TM segments and phospholipids bound to key dynamic components of the channel.

Reviews - 6pwn mentioned but not cited (3)

  1. Discoveries in structure and physiology of mechanically activated ion channels. Kefauver JM, Ward AB, Patapoutian A. Nature 587 567-576 (2020)
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Articles - 6pwn mentioned but not cited (5)

  1. Molecular basis of force-from-lipids gating in the mechanosensitive channel MscS. Reddy B, Bavi N, Lu A, Park Y, Perozo E. Elife 8 e50486 (2019)
  2. Spatial arrangement of proteins in planar and curved membranes by PPM 3.0. Lomize AL, Todd SC, Pogozheva ID. Protein Sci 31 209-220 (2022)
  3. New approach for membrane protein reconstitution into peptidiscs and basis for their adaptability to different proteins. Angiulli G, Dhupar HS, Suzuki H, Wason IS, Duong Van Hoa F, Walz T. Elife 9 e53530 (2020)
  4. State-specific morphological deformations of the lipid bilayer explain mechanosensitive gating of MscS ion channels. Park YC, Reddy B, Bavi N, Perozo E, Faraldo-Gómez JD. Elife 12 e81445 (2023)
  5. Mechanosensitive channel YnaI has lipid-bound extended sensor paddles. Hu W, Wang Z, Zheng H. Commun Biol 4 602 (2021)


Reviews citing this publication (11)

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Articles citing this publication (33)

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  4. The MscS-like channel YnaI has a gating mechanism based on flexible pore helices. Flegler VJ, Rasmussen A, Rao S, Wu N, Zenobi R, Sansom MSP, Hedrich R, Rasmussen T, Böttcher B. Proc Natl Acad Sci U S A 117 28754-28762 (2020)
  5. Cyclodextrins increase membrane tension and are universal activators of mechanosensitive channels. Cox CD, Zhang Y, Zhou Z, Walz T, Martinac B. Proc Natl Acad Sci U S A 118 e2104820118 (2021)
  6. A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi. Dave N, Cetiner U, Arroyo D, Fonbuena J, Tiwari M, Barrera P, Lander N, Anishkin A, Sukharev S, Jimenez V. Elife 10 e67449 (2021)
  7. Enhancing proline-rich antimicrobial peptide action by homodimerization: influence of bifunctional linker. Li W, Lin F, Hung A, Barlow A, Sani MA, Paolini R, Singleton W, Holden J, Hossain MA, Separovic F, O'Brien-Simpson NM, Wade JD. Chem Sci 13 2226-2237 (2022)
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  13. Charged pore-lining residues are required for normal channel kinetics in the eukaryotic mechanosensitive ion channel MSL1. Schlegel AM, Haswell ES. Channels (Austin) 14 310-325 (2020)
  14. Exploring the diversity of mechanosensitive channels in bacterial genomes. Johnson SC, Veres J, Malcolm HR. Eur Biophys J 50 25-36 (2021)
  15. Structural basis for mechanotransduction in a potassium-dependent mechanosensitive ion channel. Mount J, Maksaev G, Summers BT, Fitzpatrick JAJ, Yuan P. Nat Commun 13 6904 (2022)
  16. A mechanical-coupling mechanism in OSCA/TMEM63 channel mechanosensitivity. Zhang M, Shan Y, Cox CD, Pei D. Nat Commun 14 3943 (2023)
  17. Hysteresis of a Tension-Sensitive K+ Channel Revealed by Time-Lapse Tension Measurements. Iwamoto M, Oiki S. JACS Au 1 467-474 (2021)
  18. Asymmetric effects of amphipathic molecules on mechanosensitive channels. Bavi O, Zhou Z, Bavi N, Mehdi Vaez Allaei S, Cox CD, Martinac B. Sci Rep 12 9976 (2022)
  19. Cryo-EM structures of an LRRC8 chimera with native functional properties reveal heptameric assembly. Takahashi H, Yamada T, Denton JS, Strange K, Karakas E. Elife 12 e82431 (2023)
  20. Genetic and cellular characterization of MscS-like putative channels in the filamentous fungus Aspergillus nidulans. Dionysopoulou M, Yan N, Wang B, Pliotas C, Diallinas G. Channels (Austin) 16 148-158 (2022)
  21. Mechanosensitive membrane proteins: Usual and unusual suspects in mediating mechanotransduction. Goodman MB, Haswell ES, Vásquez V. J Gen Physiol 155 e202213248 (2023)
  22. Architecture of Dispatched, a Transmembrane Protein Responsible for Hedgehog Release. Luo Y, Wan G, Zhou X, Wang Q, Zhang Y, Bao J, Cong Y, Zhao Y, Li D. Front Mol Biosci 8 701826 (2021)
  23. Cyclodextrins for structural and functional studies of mechanosensitive channels. Zhang Y, Angiulli G, Martinac B, Cox CD, Walz T. J Struct Biol X 5 100053 (2021)
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  25. Microscopic mechanism of PIEZO1 activation by pressure-induced membrane stretch. Wijerathne TD, Ozkan AD, Lacroix JJ. J Gen Physiol 155 e202213260 (2023)
  26. Structure of mechanically activated ion channel OSCA2.3 reveals mobile elements in the transmembrane domain. Jojoa-Cruz S, Burendei B, Lee WH, Ward AB. Structure 32 157-167.e5 (2024)
  27. "Force-From-Lipids" Dependence of the MscCG Mechanosensitive Channel Gating on Anionic Membranes. Nakayama Y, Rohde PR, Martinac B. Microorganisms 11 194 (2023)
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  31. Open structure and gating of the Arabidopsis mechanosensitive ion channel MSL10. Zhang J, Maksaev G, Yuan P. Nat Commun 14 6284 (2023)
  32. OzTracs: Optical Osmolality Reporters Engineered from Mechanosensitive Ion Channels. Kleist TJ, Lin IW, Xu S, Maksaev G, Sadoine M, Haswell ES, Frommer WB, Wudick MM. Biomolecules 12 787 (2022)
  33. When is a hydrophobic gate not a hydrophobic gate? Seiferth D, Biggin PC, Tucker SJ. J Gen Physiol 154 e202213210 (2022)


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