Home LiteratureArticle Details
PMID: 2435331 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

How pore mouth charge distributions alter the permeability of transmembrane ionic channels.

Biophysical journal ·Vol. 51 ·No. 2 ·1987-02-00 ·Pages 297-311

Jordan PC

Abstract

This paper investigates the effects that surface dipole layers and surface charge layers along the pore mouth-water interface can have on the electrical properties of a transmembrane channel. Three specific molecular sources are considered: dipole layers formed by membrane phospholipids, dipole layers lining the mouth of a channel-forming protein, and charged groups in the mouth of a channel-forming protein. We find, consistent with previous work, that changing the lipid-water potential difference only influences channel conduction if the rate-limiting step takes place well inside the channel constriction. We find that either mouth dipoles or mouth charges can act as powerful ion attractors increasing either cation or anion concentration near the channel entrance to many times its bulk value, especially at low ionic strengths. The effects are sufficient to reconcile the apparently contradictory properties of high selectivity and high conductivity, observed for a number of K+ channel systems. We find that localizing the electrical sources closer to the constriction entrance substantially increases their effectiveness as ion attractors; this phenomenon is especially marked for dipolar distributions. An approximate treatment of electrolyte shielding is used to discriminate between the various mechanisms for increasing ionic concentration near the constriction entrance. Dipolar potentials are far less sensitive to ionic strength variation than potentials due to fixed charges. We suggest that the K+ channel from sarcoplasmic reticulum does not have a fixed negative charge near the constriction entrance; we suggest further that the Ca+2-activated K+ channel from transverse tubule does have such a charge.

MeSH Terms
Cell Membrane Permeability Gramicidin Ion Channels/physiology Kinetics Mathematics Membrane Potentials Models, Biological Osmolar Concentration Surface Properties
Chemicals
Ion Channels Gramicidin
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Jordan P C
References (32)
32 references, click to expand
  1. Single channels of 9, 11, 13, 15-destryptophyl-phenylalanyl-gramicidin A.
    Biophys J. 1982 Oct;40(1):87-9 PMID: 6182929
  2. Effect of phloretin on the permeability of thin lipid membranes.
    J Gen Physiol. 1976 Jun;67(6):749-71 PMID: 946975
  3. Single-channel parameters of gramicidin A,B, and C.
    Biochim Biophys Acta. 1976 Jan 21;419(2):223-8 PMID: 55275
  4. The membrane dipole potential in a total membrane potential model. Applications to hydrophobic ion interactions with membranes.
    Biophys J. 1986 Feb;49(2):541-52 PMID: 3955184
  5. Structure and dynamics of ion transport through gramicidin A.
    Biophys J. 1984 Aug;46(2):229-48 PMID: 6206901
  6. Potassium channels as multi-ion single-file pores.
    J Gen Physiol. 1978 Oct;72(4):409-42 PMID: 722275
  7. Ionic selectivity, saturation, and block in a K+-selective channel from sarcoplasmic reticulum.
    J Gen Physiol. 1980 Oct;76(4):425-46 PMID: 6255062
  8. Effect of phospholipid surface charge on the conductance and gating of a Ca2+-activated K+ channel in planar lipid bilayers.
    J Membr Biol. 1985;83(3):273-82 PMID: 2582128
  9. Shortened analog of the gramicidin A channel argues for the doubly occupied channel as the dominant conducting state.
    Biochim Biophys Acta. 1984 Aug 8;775(1):115-9 PMID: 6205694
  10. Nature of the charge distribution in proteins.
    Nature. 1981 Oct 29;293(5835):757-8 PMID: 7290210
  11. Single channels of various gramicidins: voltage effects.
    Biophys J. 1984 Jan;45(1):97-9 PMID: 19431582
  12. Effect of pore structure on energy barriers and applied voltage profiles. I. Symmetrical channels.
    Biophys J. 1984 Jun;45(6):1091-100 PMID: 6331539
  13. Electrical capacity of black lipid films and of lipid bilayers made from monolayers.
    Biochim Biophys Acta. 1975 Jul 3;394(3):323-34 PMID: 1131368
  14. Electrostatic modeling of ion pores. II. Effects attributable to the membrane dipole potential.
    Biophys J. 1983 Feb;41(2):189-95 PMID: 6188503
  15. Ion movement through gramicidin A channels. Studies on the diffusion-controlled association step.
    Biophys J. 1983 Feb;41(2):147-65 PMID: 6188502
  16. The role of the alpha-helix dipole in protein function and structure.
    Prog Biophys Mol Biol. 1985;45(3):149-95 PMID: 3892583
  17. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle.
    Proc Natl Acad Sci U S A. 1982 Feb;79(3):805-9 PMID: 6278496
  18. The gramicidin A transmembrane channel: a proposed pi(L,D) helix.
    Proc Natl Acad Sci U S A. 1971 Mar;68(3):672-6 PMID: 5276779
  19. Structure of gramicidin A.
    Biophys J. 1986 Jan;49(1):295-306 PMID: 2420381
  20. Bis-quaternary ammonium blockers as structural probes of the sarcoplasmic reticulum K+ channel.
    J Gen Physiol. 1982 May;79(5):869-91 PMID: 6284862
  21. Molecular dynamics simulation of cation motion in water-filled gramicidinlike pores.
    Biophys J. 1984 Dec;46(6):805-19 PMID: 6083812
  22. Effects of phospholipid surface charge on ion conduction in the K+ channel of sarcoplasmic reticulum.
    Biophys J. 1984 Jan;45(1):279-87 PMID: 6324908
  23. The alpha-helix as an electric macro-dipole.
    Adv Biophys. 1976;:1-63 PMID: 797240
  24. Helical channels in crystals of gramicidin A and of a cesium--gramicidin A complex: an x-ray diffraction study.
    J Mol Biol. 1978 May 5;121(1):41-54 PMID: 77905
  25. Diffusion-limited ion flow through pores.
    Biochim Biophys Acta. 1976 Dec 2;455(2):493-509 PMID: 999924
  26. Electrostatic modeling of ion pores. Energy barriers and electric field profiles.
    Biophys J. 1982 Aug;39(2):157-64 PMID: 6288132
  27. Conduction, Blockade and Gating in a Ca -activated K Channel Incorporated into Planar Lipid Bilayers.
    Biophys J. 1984 Jan;45(1):73-6 PMID: 19431572
  28. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems.
    Nature. 1969 Mar 1;221(5183):844-6 PMID: 5765058
  29. Electrostatic calculations for an ion channel. I. Energy and potential profiles and interactions between ions.
    Biophys J. 1978 May;22(2):209-19 PMID: 656542
  30. Strong electrolyte continuum theory solution for equilibrium profiles, diffusion limitation, and conductance in charged ion channels.
    Biophys J. 1985 Jul;48(1):19-31 PMID: 2410048
  31. Crystalline arrays of membrane-bound acetylcholine receptor.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3678-82 PMID: 6943572
  32. Dielectric behaviour of dry synthetic polypeptides.
    Biochim Biophys Acta. 1976 Aug 4;443(1):137-42 PMID: 953011
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1987-02-00
Pages
297-311
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1329891
Subset
IM
Grants
NIGMS NIH HHS · GM-28643 · 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: [email protected]