Home LiteratureArticle Details
PMID: 9679160 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The selectivity filter of a potassium channel, murine kir2.1, investigated using scanning cysteine mutagenesis.

The Journal of physiology ·Vol. 511 ( Pt 1) ·1998-08-15 ·Pages 25-32

Dart C, Leyland ML, Spencer PJ, Stanfield PR, Sutcliffe MJ

Abstract

We have produced a structural model of the pore-forming H5 (or P) region of the strong inward rectifier K+ channel, Kir2.1, based initially on an existing molecular model of the pore region of the voltage-gated K+ channel, Kv1.3. Cysteine-scanning mutagenesis and subsequent blockage by Ag+ was used to test our model by determining the residues in H5 whose side chains line the ion conduction pathway. Mutations made in eight positions within the highly conserved H5 region resulted in apparently non-functional channels. Constructing covalently linked dimers, which carry a cysteine substitution in only one of the linked subunits, rescued six of these mutants; a covalently linked tetramer, carrying a cysteine substitution on only one of the linked subunits, rescued a further mutant. Our results using the dimers and tetramers suggest that residues Thr141, Thr142, Ile143, Tyr145, Phe147 and Cys149 are accessible to externally applied Ag+ (100-200 nM) and therefore that their side chains line the channel pore. We conclude that the topology of the Kir pore is similar, but not identical, to that of Kv channels. Additionally, the molecular model suggests that selectivity may be conferred both by aromatic residues (Tyr145 and Phe147) via cation-pi interactions and by backbone carbonyl groups (Thr142 and Gly144).

MeSH Terms
Amino Acid Sequence Amino Acid Substitution Animals CHO Cells Computer Graphics Cricetinae Cysteine Macromolecular Substances Membrane Potentials Mice Models, Molecular Molecular Sequence Data Mutagenesis, Site-Directed Point Mutation Potassium Channels/biosynthesis,chemistry,physiology Potassium Channels, Inwardly Rectifying Protein Structure, Secondary Recombinant Proteins/biosynthesis,chemistry,metabolism Sequence Alignment Sequence Homology, Amino Acid Transfection
Chemicals
Macromolecular Substances Potassium Channels Potassium Channels, Inwardly Rectifying Recombinant Proteins Cysteine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dart C
Ion Channel Group, Department of Cell Physiology and Pharmacology, University of Leicester, PO Box 138, Leicester LE1 9HN, UK.
Leyland M L
Spencer P J
Stanfield P R
Sutcliffe M J
References (31)
31 references, click to expand
  1. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons.
    J Gen Physiol. 1972 Nov;60(5):588-608 PMID: 4644327
  2. Functional effects of the mouse weaver mutation on G protein-gated inwardly rectifying K+ channels.
    Neuron. 1996 Feb;16(2):321-31 PMID: 8789947
  3. Mutations affecting TEA blockade and ion permeation in voltage-activated K+ channels.
    Science. 1990 Oct 12;250(4978):276-9 PMID: 2218530
  4. Alteration of ionic selectivity of a K+ channel by mutation of the H5 region.
    Nature. 1991 Feb 21;349(6311):700-4 PMID: 1899917
  5. Mutations affecting internal TEA blockade identify the probable pore-forming region of a K+ channel.
    Science. 1991 Feb 22;251(4996):939-42 PMID: 2000494
  6. Determination of the subunit stoichiometry of a voltage-activated potassium channel.
    Nature. 1991 Mar 21;350(6315):232-5 PMID: 1706481
  7. The aromatic binding site for tetraethylammonium ion on potassium channels.
    Neuron. 1992 Mar;8(3):483-91 PMID: 1550673
  8. Acetylcholine receptor channel structure probed in cysteine-substitution mutants.
    Science. 1992 Oct 9;258(5080):307-10 PMID: 1384130
  9. The signature sequence of voltage-gated potassium channels projects into the external vestibule.
    J Biol Chem. 1996 Dec 6;271(49):31013-6 PMID: 8940091
  10. Stabilization of ion selectivity filter by pore loop ion pairs in an inwardly rectifying potassium channel.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1568-72 PMID: 9037094
  11. Purification, characterization, and synthesis of an inward-rectifier K+ channel inhibitor from scorpion venom.
    Biochemistry. 1997 Jun 10;36(23):6936-40 PMID: 9188688
  12. Protein-water-ion interactions in a model of the pore domain of a potassium channel: a simulation study.
    Biochim Biophys Acta. 1998 Mar 6;1370(1):1-7 PMID: 9518528
  13. The structure of the potassium channel: molecular basis of K+ conduction and selectivity.
    Science. 1998 Apr 3;280(5360):69-77 PMID: 9525859
  14. The dependence of Ag+ block of a potassium channel, murine kir2.1, on a cysteine residue in the selectivity filter.
    J Physiol. 1998 Aug 15;511 ( Pt 1):15-24 PMID: 9679159
  15. Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs.
    Neuron. 1992 Nov;9(5):861-71 PMID: 1419000
  16. Cloning and expression of an inwardly rectifying ATP-regulated potassium channel.
    Nature. 1993 Mar 4;362(6415):31-8 PMID: 7680431
  17. Primary structure and functional expression of a mouse inward rectifier potassium channel.
    Nature. 1993 Mar 11;362(6416):127-33 PMID: 7680768
  18. Regulation of K+/Rb+ selectivity and internal TEA blockade by mutations at a single site in K+ pores.
    Pflugers Arch. 1993 Apr;423(1-2):104-12 PMID: 7683786
  19. A mechanism for ion selectivity in potassium channels: computational studies of cation-pi interactions.
    Science. 1993 Sep 24;261(5129):1708-10 PMID: 8378771
  20. Comparative protein modelling by satisfaction of spatial restraints.
    J Mol Biol. 1993 Dec 5;234(3):779-815 PMID: 8254673
  21. Mutations in the K+ channel signature sequence.
    Biophys J. 1994 Apr;66(4):1061-7 PMID: 8038378
  22. Silver as a probe of pore-forming residues in a potassium channel.
    Science. 1995 Apr 14;268(5208):304-7 PMID: 7716526
  23. Revealing the architecture of a K+ channel pore through mutant cycles with a peptide inhibitor.
    Science. 1995 Apr 14;268(5208):307-10 PMID: 7716527
  24. K+ pore structure revealed by reporter cysteines at inner and outer surfaces.
    Neuron. 1995 May;14(5):1055-63 PMID: 7748553
  25. Side-chain accessibilities in the pore of a K+ channel probed by sulfhydryl-specific reagents after cysteine-scanning mutagenesis.
    Biophys J. 1995 Mar;68(3):900-5 PMID: 7756555
  26. Topology of the pore-region of a K+ channel revealed by the NMR-derived structures of scorpion toxins.
    Neuron. 1995 Nov;15(5):1169-81 PMID: 7576659
  27. Determination of the subunit stoichiometry of an inwardly rectifying potassium channel.
    Neuron. 1995 Dec;15(6):1441-7 PMID: 8845166
  28. Spatial localization of the K+ channel selectivity filter by mutant cycle-based structure analysis.
    Neuron. 1996 Jan;16(1):131-9 PMID: 8562077
  29. Functional analysis of the weaver mutant GIRK2 K+ channel and rescue of weaver granule cells.
    Neuron. 1996 May;16(5):941-52 PMID: 8630252
  30. Nonselective and G betagamma-insensitive weaver K+ channels.
    Science. 1996 Jun 28;272(5270):1950-3 PMID: 8658170
  31. Potassium channels in myelinated nerve. Selective permeability to small cations.
    J Gen Physiol. 1973 Jun;61(6):669-86 PMID: 4541077
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1998-08-15
Pages
25-32
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2231101
Subset
IM
Grants
Wellcome Trust · United Kingdom
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