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PMID: 11904391 Published · ppublish English Journal Article

Gramicidin A channels switch between stretch activation and stretch inactivation depending on bilayer thickness.

Martinac B, Hamill OP

Abstract

The patch clamp-liposome technique was used to examine the stretch sensitivity of a model membrane ion channel, gramicidin A, in membrane patches of different bilayer thickness. We found that small changes in phospholipid acyl chain length (i.e., PC-20 to PC-18) can switch gramicidin A from a stretch-activated to a stretch-inactivated channel. The demonstration that subnanometer changes in bilayer thickness can reverse the response polarity of a model channel has implications for other signaling proteins that may experience local changes in bilayer thickness as a consequence of dynamic targeting to lipid microdomains, electrocompression, or chemical modification of the bilayer.

MeSH Terms
Gramicidin/chemistry,metabolism Ion Channels/chemistry Lipid Bilayers/chemistry Patch-Clamp Techniques
Chemicals
Ion Channels Lipid Bilayers Gramicidin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Martinac Boris
Department of Pharmacology, University of Western Australia, Crawley, West Australia 6009.
Hamill Owen P
References (49)
49 references, click to expand
  1. Apical sorting of a voltage- and Ca2+-activated K+ channel alpha -subunit in Madin-Darby canine kidney cells is independent of N-glycosylation.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13114-9 PMID: 11069304
  2. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  3. Cell surface area regulation and membrane tension.
    J Membr Biol. 2001 Jan 15,;179(2):79-102 PMID: 11220366
  4. On the discrepancy between whole-cell and membrane patch mechanosensitivity in Xenopus oocytes.
    J Physiol. 2000 Feb 15;523 Pt 1:101-15 PMID: 10673547
  5. Mechanically gated channel activity in cytoskeleton-deficient plasma membrane blebs and vesicles from Xenopus oocytes.
    J Physiol. 2000 Feb 15;523 Pt 1:117-30 PMID: 10673548
  6. Differential targeting of Shaker-like potassium channels to lipid rafts.
    J Biol Chem. 2000 Mar 17;275(11):7443-6 PMID: 10713042
  7. Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains.
    J Biol Chem. 2000 Apr 21;275(16):11934-42 PMID: 10766822
  8. Molecular basis of mechanotransduction in living cells.
    Physiol Rev. 2001 Apr;81(2):685-740 PMID: 11274342
  9. Structural determinants of MscL gating studied by molecular dynamics simulations.
    Biophys J. 2001 May;80(5):2074-81 PMID: 11325711
  10. Stretch-activation and stretch-inactivation of Shaker-IR, a voltage-gated K+ channel.
    Biophys J. 2001 Jun;80(6):2678-93 PMID: 11371444
  11. Lipid rafts and signal transduction.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9 PMID: 11413487
  12. Brefeldin A block of integrin-dependent mechanosensitive ATP release from Xenopus oocytes reveals a novel mechanism of mechanotransduction.
    J Biol Chem. 2001 Jun 29;276(26):23867-72 PMID: 11320093
  13. Site-directed spin-labeling analysis of reconstituted Mscl in the closed state.
    J Gen Physiol. 2001 Aug;118(2):193-206 PMID: 11479346
  14. Synthesis of minigramicidin ion channels and test of their hydrophobic match with the membrane.
    Chembiochem. 2001 Mar 2;2(3):221-3 PMID: 11828448
  15. Mechanosensitive channel of Thermoplasma, the cell wall-less archaea: cloning and molecular characterization.
    Cell Biochem Biophys. 2001;34(3):321-47 PMID: 11898860
  16. The gramicidin A transmembrane channel: characteristics of head-to-head dimerized (L,D) helices.
    Proc Natl Acad Sci U S A. 1971 Aug;68(8):1907-11 PMID: 5288776
  17. Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel.
    Biochim Biophys Acta. 1972 Aug 9;274(2):294-312 PMID: 5048999
  18. Simultaneous fluorescence and conductance studies of planar bilayer membranes containing a highly active and fluorescent analog of gramicidin A.
    J Mol Biol. 1975 Nov 25;99(1):75-92 PMID: 54431
  19. Influence of membrane thickness and ion concentration on the properties of the gramicidin a channel. Autocorrelation, spectral power density, relaxation and single-channel studies.
    Biochim Biophys Acta. 1977 Jan 4;464(1):127-41 PMID: 64260
  20. The influence of phospholipid polar groups on gramicidin channels.
    Biochim Biophys Acta. 1977 Jan 4;464(1):37-44 PMID: 64261
  21. Gramicidin A crystals contain two cation binding sites per channel.
    Nature. 1979 Jun 21;279(5715):723-5 PMID: 88018
  22. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  23. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles.
    J Mol Biol. 1983 May 15;166(2):211-7 PMID: 6854644
  24. The effects of bilayer thickness and tension on gramicidin single-channel lifetime.
    Biochim Biophys Acta. 1983 Oct 26;735(1):95-103 PMID: 6194820
  25. Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime.
    Biophys J. 1986 Dec;50(6):1061-70 PMID: 2432948
  26. Stretch-inactivated ion channels coexist with stretch-activated ion channels.
    Science. 1989 Feb 10;243(4892):807-9 PMID: 2536958
  27. Modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels.
    Biophys J. 1989 Sep;56(3):631-6 PMID: 2477074
  28. Calculation of deformation energies and conformations in lipid membranes containing gramicidin channels.
    Biophys J. 1990 May;57(5):1075-84 PMID: 1692748
  29. Hydrophobic mismatch in gramicidin A'/lecithin systems.
    Biochemistry. 1990 Jul 3;29(26):6215-21 PMID: 1698451
  30. Mechanosensitive ion channels of E. coli activated by amphipaths.
    Nature. 1990 Nov 15;348(6298):261-3 PMID: 1700306
  31. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective.
    Q Rev Biophys. 1991 Aug;24(3):293-397 PMID: 1749824
  32. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure.
    Biophys J. 1992 Feb;61(2):434-47 PMID: 1547331
  33. Gramicidin and gramicidin-lipid interactions.
    Biochim Biophys Acta. 1992 Dec 11;1113(3-4):391-425 PMID: 1280467
  34. Transduction of membrane tension by the ion channel alamethicin.
    Biophys J. 1994 Jan;66(1):71-4 PMID: 7510531
  35. Gramicidin A/short-chain phospholipid dispersions: chain length dependence of gramicidin conformation and lipid organization.
    Biochemistry. 1994 Apr 12;33(14):4291-9 PMID: 7512381
  36. Lysophospholipids modulate channel function by altering the mechanical properties of lipid bilayers.
    J Gen Physiol. 1994 Oct;104(4):645-73 PMID: 7530766
  37. Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli.
    J Biol Chem. 1995 Aug 4;270(31):18329-34 PMID: 7543101
  38. Tensile strength and dilatational elasticity of giant sarcolemmal vesicles shed from rabbit muscle.
    J Physiol. 1996 May 15;493 ( Pt 1):187-98 PMID: 8735704
  39. Engineering the gramicidin channel.
    Annu Rev Biophys Biomol Struct. 1996;25:231-58 PMID: 8800470
  40. The pharmacology of mechanogated membrane ion channels.
    Pharmacol Rev. 1996 Jun;48(2):231-52 PMID: 8804105
  41. Regulation of endocytosis, exocytosis, and shape by membrane tension.
    Cold Spring Harb Symp Quant Biol. 1995;60:567-71 PMID: 8824429
  42. Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes.
    J Biol Chem. 1997 Jul 11;272(28):17744-8 PMID: 9211926
  43. The conformational preference of gramicidin channels is a function of lipid bilayer thickness.
    FEBS Lett. 1997 Jul 21;412(1):15-20 PMID: 9257681
  44. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains.
    Curr Opin Cell Biol. 1997 Aug;9(4):534-42 PMID: 9261060
  45. Gramicidin channel kinetics under tension.
    Biophys J. 1998 Jan;74(1):328-37 PMID: 9449333
  46. Energetics of inclusion-induced bilayer deformations.
    Biophys J. 1998 Apr;74(4):1966-83 PMID: 9545056
  47. Mechanosensitive ion channels in nonspecialized cells.
    Rev Physiol Biochem Pharmacol. 1998;132:1-77 PMID: 9558913
  48. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel.
    Science. 1998 Dec 18;282(5397):2220-6 PMID: 9856938
  49. The gating mechanism of the large mechanosensitive channel MscL.
    Nature. 2001 Feb 8;409(6821):720-4 PMID: 11217861
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-04-02
Epub
2002-00-19
Pages
4308-12
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC123644
Subset
IM
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