Home LiteratureArticle Details
PMID: 15339809 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Defining the physical gate of a mechanosensitive channel, MscL, by engineering metal-binding sites.

Biophysical journal ·Vol. 87 ·No. 5 ·2004-11-00 ·Pages 3172-80

Iscla I, Levin G, Wray R, Reynolds R, Blount P

Abstract

The mechanosensitive channel of large conductance, MscL, of Escherichia coli is one of the best-studied mechanosensitive proteins. Although the structure of the closed or "nearly-closed" state of the Mycobacterium tuberculosis ortholog has been solved and mechanisms of gating have been proposed, the transition from the closed to the open states remains controversial. Here, we probe the relative position of specific residues predicted to line the pore of MscL in either the closed state or during the closed-to-open transition by engineering single-site histidine substitutions and assessing the ability of Ni2+, Cd2+ or Zn2+ ions to affect channel activity. All residues predicted to be within the pore led to a change in channel threshold pressure, although the direction and extent of this change were dependent upon the mutation and metal used. One of the MscL mutants, L19H, exhibited gating that was inhibited by Cd2+ but stimulated by Ni2+, suggesting that these metals bind to and influence different states of the channel. Together, the results derived from this study support the hypotheses that the crystal structure depicts a "nearly closed" rather than a "fully closed" state of MscL, and that a clockwise rotation of transmembrane domain 1 occurs early in the gating process.

MeSH Terms
Binding Sites Escherichia coli/drug effects,physiology Escherichia coli Proteins/chemistry,drug effects,genetics,metabolism Ion Channel Gating/drug effects,physiology Ion Channels/chemistry,drug effects,genetics,metabolism Mechanotransduction, Cellular/drug effects,physiology Metals/pharmacology Mutagenesis, Site-Directed Pressure Protein Binding Protein Engineering/methods Recombinant Proteins/metabolism Spheroplasts/drug effects,physiology Stress, Mechanical Structure-Activity Relationship
Chemicals
Escherichia coli Proteins Ion Channels Metals MscL protein, E coli Recombinant Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Iscla Irene
Department of Physiology, University of Texas-Southwestern Medical Center, Dallas, Texas 75390-9040, USA.
Levin Gal
Wray Robin
Reynolds Robert
Blount Paul
References (33)
33 references, click to expand
  1. pH-dependent inhibition of voltage-gated H(+) currents in rat alveolar epithelial cells by Zn(2+) and other divalent cations.
    J Gen Physiol. 1999 Dec;114(6):819-38 PMID: 10578017
  2. Intragenic suppression of gain-of-function mutations in the Escherichia coli mechanosensitive channel, MscL.
    Mol Microbiol. 2004 Jul;53(2):485-95 PMID: 15228529
  3. The gating mechanism of the large mechanosensitive channel MscL.
    Nature. 2001 Feb 8;409(6821):720-4 PMID: 11217861
  4. Molecular basis of mechanotransduction in living cells.
    Physiol Rev. 2001 Apr;81(2):685-740 PMID: 11274342
  5. Structural models of the MscL gating mechanism.
    Biophys J. 2001 Aug;81(2):917-36 PMID: 11463635
  6. Voltage-controlled gating at the intracellular entrance to a hyperpolarization-activated cation channel.
    J Gen Physiol. 2002 Jan;119(1):83-91 PMID: 11773240
  7. Gating the bacterial mechanosensitive channel MscL invivo.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5643-8 PMID: 11960017
  8. Analysis of the kefA2 mutation suggests that KefA is a cation-specific channel involved in osmotic adaptation in Escherichia coli.
    Mol Microbiol. 2002 Jan;43(2):521-36 PMID: 11985727
  9. A large iris-like expansion of a mechanosensitive channel protein induced by membrane tension.
    Nat Struct Biol. 2002 Sep;9(9):704-10 PMID: 12172538
  10. Open channel structure of MscL and the gating mechanism of mechanosensitive channels.
    Nature. 2002 Aug 29;418(6901):942-8 PMID: 12198539
  11. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli.
    EMBO J. 2002 Oct 15;21(20):5323-30 PMID: 12374733
  12. An in vivo assay identifies changes in residue accessibility on mechanosensitive channel gating.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10161-5 PMID: 15226501
  13. Potassium-dependant mutants of Escherichia coli K-12.
    J Bacteriol. 1970 Mar;101(3):836-43 PMID: 4908783
  14. 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
  15. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure.
    J Membr Biol. 1996 May;151(2):175-87 PMID: 8661505
  16. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11652-7 PMID: 8876191
  17. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli.
    EMBO J. 1996 Sep 16;15(18):4798-805 PMID: 8890153
  18. Gated access to the pore of a voltage-dependent K+ channel.
    Neuron. 1997 Jul;19(1):175-84 PMID: 9247273
  19. Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli.
    Biophys J. 1997 Oct;73(4):1925-31 PMID: 9336188
  20. Mutations in a bacterial mechanosensitive channel change the cellular response to osmotic stress.
    J Biol Chem. 1997 Dec 19;272(51):32150-7 PMID: 9405414
  21. One face of a transmembrane helix is crucial in mechanosensitive channel gating.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11471-5 PMID: 9736761
  22. The activation gate of a voltage-gated K+ channel can be trapped in the open state by an intersubunit metal bridge.
    Neuron. 1998 Sep;21(3):617-21 PMID: 9768847
  23. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel.
    Science. 1998 Dec 18;282(5397):2220-6 PMID: 9856938
  24. Mechanosensitive channels of bacteria.
    Methods Enzymol. 1999;294:458-82 PMID: 9916243
  25. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity.
    EMBO J. 1999 Apr 1;18(7):1730-7 PMID: 10202137
  26. Bacterial mechanosensitive channels: integrating physiology, structure and function.
    Trends Microbiol. 1999 Oct;7(10):420-4 PMID: 10498951
  27. Hydrophilicity of a single residue within MscL correlates with increased channel mechanosensitivity.
    Biophys J. 1999 Oct;77(4):1960-72 PMID: 10512816
  28. Generation and evaluation of a large mutational library from the Escherichia coli mechanosensitive channel of large conductance, MscL: implications for channel gating and evolutionary design.
    J Biol Chem. 2003 Jun 6;278(23):21076-82 PMID: 12670944
  29. Mechanism of proton transfer inhibition by Cd(2+) binding to bacterial reaction centers: determination of the pK(A) of functionally important histidine residues.
    Biochemistry. 2003 Aug 19;42(32):9626-32 PMID: 12911304
  30. Movements near the gate of a hyperpolarization-activated cation channel.
    J Gen Physiol. 2003 Nov;122(5):501-10 PMID: 14557404
  31. Intracellular gate opening in Shaker K+ channels defined by high-affinity metal bridges.
    Nature. 2004 Apr 22;428(6985):864-8 PMID: 15103379
  32. Cysteine scanning of MscL transmembrane domains reveals residues critical for mechanosensitive channel gating.
    Biophys J. 2004 May;86(5):2862-70 PMID: 15111403
  33. Correlating a protein structure with function of a bacterial mechanosensitive channel.
    J Biol Chem. 2000 Oct 6;275(40):31121-7 PMID: 10846181
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2004-11-00
Epub
2004-00-31
Pages
3172-80
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1304787
Subset
IM
Grants
NIGMS NIH HHS · R01 GM061028 · United States
NIDDK NIH HHS · DK60818 · United States
NIGMS NIH HHS · GM61028 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com