Abstract
Malonyl gramicidin is incorporated into lysolecithin micelles in a manner which satisfies a number of previously demonstrated criteria for the formation of the transmembrane channel structure. By means of sodium-23 nuclear magnetic resonance, two binding sites are observed: a tight site and a weak site with binding constants of approximately 100 M-1 and 1 M-1 respectively. In addition, off-rate constants from the two sites were estimated from NMR analyses to be kofft congruent to 3 X 10(5)/sec and koffw congruent to 2 X 10(7)/sec giving, with the binding constants, the on-rate constants, kont congruent to 3 X 10(7)/Msec and konw congruent to 2 X 10(7)/Msec. Five different multiple occupancy models with NMR-restricted energy profiles were considered for the purpose of calculating single-channel currents as a function of voltage and concentration utilizing the four NMR-derived rate constants (and an NMR-limit placed on a fifth rate constant for intrachannel ion translocation) in combination with Eyring rate theory for the introduction of voltage dependence. Using the X-ray diffraction results of Koeppe et al. (1979) for limiting the positions of the tight sites, the two-site model and a three-site model in which the weak sites occur after the tight site is filled were found to satisfactorily calculate the experimental currents (also reported here) and to fit the experimental currents extraordinarily well when the experimentally derived values were allowed to vary to a least squares best fit. Surprisingly the "best fit" values differed by only about a factor of two from the NMR-derived values, a variation that is well within the estimated experimental error of the rate constants. These results demonstrate the utility of ion nuclear magnetic resonance to determine rate constants relevant to transport through the gramicidin channel and of the Eyring rate theory to introduce voltage dependence.
MeSH Terms
Colloids
Gramicidin
Ion Channels/metabolism
Lysophosphatidylcholines
Magnetic Resonance Spectroscopy
Mathematics
Micelles
Models, Biological
Models, Molecular
Molecular Conformation
Chemicals
Colloids
Ion Channels
Lysophosphatidylcholines
Micelles
Gramicidin
malonyl gramicidin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Urry D W
Venkatachalam C M
Spisni A
Bradley R J
Trapane T L
Prasad K U
References (24)
24 references, click to expand
-
Relaxation studies on complex formation of macrocyclic and open chain antibiotics with monovalent cations.
Biophys Chem. 1977 Apr;6(3):239-51
PMID: 880340
-
Development of K+-Na+ discrimination in experimental bimolecular lipid membranes by macrocyclic antibiotics.
Biochem Biophys Res Commun. 1967 Feb 21;26(4):398-404
PMID: 6033739
-
23Na nuclear magnetic resonance relaxation studies of sodium ion interaction with soluble RNA.
Proc Natl Acad Sci U S A. 1969 Mar;62(3):644-9
PMID: 5256995
-
The kinetics of ion movements in the gramicidin channel.
Fed Proc. 1978 Oct;37(12):2628-32
PMID: 81148
-
Interactions in cation permeation through the gramicidin channel. Cs, Rb, K, Na, Li, Tl, H, and effects of anion binding.
Biophys J. 1978 May;22(2):307-40
PMID: 77689
-
Rate theory calculation of gramicidin single-channel currents using NMR-derived rate constants.
Proc Natl Acad Sci U S A. 1980 Apr;77(4):2028-32
PMID: 6154942
-
Sodium binding sites of gramicidin A: sodium-23 nuclear magnetic resonance study.
Biochemistry. 1979 May 15;18(10):2004-7
PMID: 86363
-
Correlation analysis of electrical noise in lipid bilayer membranes: kinetics of gramicidin A channels.
J Membr Biol. 1975;20(1-2):133-54
PMID: 47397
-
Synthetic peptide K+ carrier with Ca2+ inhibition.
Arch Biochem Biophys. 1977 Jan 30;178(2):468-74
PMID: 836044
-
Structure of the gramicidin A channel: discrimination between the piL,D and the beta helix by electrical measurements with lipid bilayer membranes.
Proc Natl Acad Sci U S A. 1977 Jun;74(6):2402-6
PMID: 70038
-
Ionic selectivity, saturation and block in gramicidin A channels: I. Theory for the electrical properties of ion selective channels having two pairs of binding sites and multiple conductance states.
J Membr Biol. 1977 Mar 23;31(4):383-47
PMID: 66317
-
Sodium and calcium binding to Panulirus interruptus hemocyanin as studied by 23Na nuclear magnetic resonance.
Eur J Biochem. 1979 Aug 1;98(2):591-5
PMID: 488113
-
Multi-site, multi-barrier, multi-occupancy models for the electrical behavior of single filing channels like those of gramicidin.
Brain Res Bull. 1979 Jan-Feb;4(1):154-8
PMID: 89003
-
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
-
Gramicidin A crystals contain two cation binding sites per channel.
Nature. 1979 Jun 21;279(5715):723-5
PMID: 88018
-
Characterization of micellar-packaged gramicidin A channels.
Biochem Biophys Res Commun. 1979 Jun 13;88(3):940-9
PMID: 88942
-
Temperature-dependent properties of gramicidin A channels.
Biochim Biophys Acta. 1974 Oct 29;367(2):127-33
PMID: 4138938
-
Conformation and molecular mechanisms of carriers and channels.
Ann N Y Acad Sci. 1975 Dec 30;264:203-20
PMID: 56911
-
The action of a carbonsuboxide dimerized gramicidin A on lipid bilayer membranes.
Biochim Biophys Acta. 1977 Mar 17;465(3):486-99
PMID: 65181
-
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
-
Channel structures of gramicidin: characterization of succinyl derivatives.
Science. 1978 Apr 28;200(4340):435-7
PMID: 77040
-
Pulsed nuclear magnetic resonance studies on 23 Na, 7 Li and 35 Cl binding to human oxy- and carbon monoxyhaemoglobin.
J Mol Biol. 1973 Jan 10;73(2):251-9
PMID: 4689950
-
Basic aspects of calcium chemistry and membrane interaction: on the messenger role of calcium.
Ann N Y Acad Sci. 1978 Apr 28;307:3-27
PMID: 81649
-
Conformation of gramicidin A channel in phospholipid vesicles: a 13C and 19F nuclear magnetic resonance study.
Proc Natl Acad Sci U S A. 1979 Sep;76(9):4230-4
PMID: 92025