Abstract
We have recently shown (Chang et al., 1995) that lipid-channel interactions, exemplified by the effects of cholesterol on the calcium-activated potassium (BK) channel, profoundly affect channel properties. The present study further explores such interactions by monitoring changes in BK channel behavior after reconstitution into bilayers where the size of phospholipid (PL) headgroups is increased and where the freedom of motion (inverse order) of fatty acid chains is incremented. Increasing the PL headgroup cross-sectional area, from that of N-meth-DOPE to that of DOPC (an increase from ca. 60 to 70 Å2), is associated with a doubling of the channel mean opentime. Channel conductance, however, was unaffected. Increasing the order of the fatty acid chains, from that of DOPE to POPE and to that of DEPE, had no significant effect on channel properties (at 22°C). We interpret the changes reported here to reflect lipid-protein interactions through the induction of structural stress related to the headgroup structures of phospholipids.
Similar content being viewed by others
References
Chang, H.-M., Reitstetter, R., Mason, R.P., Gruener, R. 1995. Attentuation of channel kinetics and conductance by cholesterol: an interpretation using structural stress as a unifying concept. J. Membrane Biol. 143:51–63
Chong, P.L.-G., Fortes, P.A.G., Jameson, D.M. 1985. Mechanisms of inhibition of (Na,K)-ATPase by hydrostatic pressure studied with fluorescent probes. J. Biol. Chem. 260:14484–11490
Colquhoun, D., Sigworth, F.J. 1983. Chapter 11. In: Single-Channel Recording. B. Sakmann and E. Neher, editors. pp. 191–263. Plenum, New York
Evans, E., Needham, D. 1987. Physical properties of surfactant bilayer membranes: thermal transition, elasticity, rigidity, cohesion and colloidal interactions. J. Phys. Chem. 91:4219–4228
Fong, T.M., McNamee, M.G. 1986. Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25:830–840
Gibson, N.J., Brown, M.F. 1993. Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes. Biochemistry 32:2438–2454
Gruner, S.M. 1985. Curvature hypothesis: does the intrinsic curvature determine biomembrane lipid composition. A role for non-bilayer lipids. Proc. Natl. Acad. Sci. USA 82:3665–3669
Gruner, S.M. 1992. Nonlamellar lipid phases. Chap. 5. In: The structure of biological membranes. P. Yeagle, editors. pp. 211–250. CRC, Boca Raton, Florida
Gruner, S.M., Tate, M.W., Kirk, G.L., So, P.T.C., Turner, D.C., Keane, D.T., Tilcock, C.P.S., Cullis, P.R. 1988. X-ray diffraction study of the polymorphic behavior of N-methylated dioleoylphosphatidylethanolamine. Biochemistry 27:2853–2866
Helfrich, W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. 28c:693–703
Israelachvili, J. 1991. Chap. 14. In: Intermolecular and surface forces, 2nd ed., pp 288–311. Academic, New York
Keller, S., Bezrukov, M., Gruner, S.M., Tate, M.W., Vodyanoy, I., Parsegian, V.A. 1993. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys. J. 65:23–27
Krueger, B.K., Worley, J.F., French, R.J. 1983. Single sodium channel from rat brain incorporated into planar lipid bilayers. Nature 303:172–175
Labarca, P., Coronado, R., Miller, C. 1980. Thermodynamic and kinetic studies of the gating behavior of a potassium-selective channel from the sarcoplasmic reticulum membrane. J. Gen. Physiol. 76:397–424
Lewis, R.N.A.H., Mannock, D.A., McElhaney, R.N., Turner, D.C., Gruner, S.M. 1989. Effect of fatty acyl chain length and structure on the lamellar gel to liquid-crystalline and lamellar to reversed hexagonal phase transitions of aqueous phosphatidylethanolamine dispersions. Biochemistry 28:541
Marsh, D. 1990a. Section II. 14 In: Handbook of lipid bilayers pp. 265–273. CRC, Boca Raton, Florida
Marsh, D. 1990b. Section II. 7 In: Handbook of lipid bilayers p. 151. CRC, Boca Raton, Florida
Marsh, D. 1990c. Section II. 8 In: Handbook of lipid bilayers pp. 163–183. CRC, Boca Raton, Florida
McElhaney, R.N. 1989. The influence of membrane lipid composition on physical properties of membrane structure and function in Achole-plasma laidlail. CRC Crit. Rev. Microbiol 17:1–32
Methfessel, C., Boheim, C. 1982. The gating of single calcium-dependent potassium channels is described by an activation-blockage mechanism. Biophys. Struct. Mech. 9:35–60
Moczydlowski, E., Latorre, R. 1983. Gating kinetics of Ca2+-activated K+ channels from rat muscle incorporated into planar lipid bailers: evidence for two voltage-dependent Ca2+-binding reactions. J. Gen. Physiol. 82:511–542
Needham, D., Evans, E. 1988. Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20°C below to 10°C above the liquid crystal-crystalline phase transition at 24°C. Biochemistry 27:8261–8269
Needham, D., Nunn, R.S. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997–1009
Rand, R.P., Parsegian, V.A. 1992. Chap. 6, In: The structure of biological membranes P. Yeagle, editors. pp. 251–306. CRC, Boca Raton, Florida
Reinhart, P.M., Chung, S., Martin, B.L., Brautigan, D.L., Levitan, I.B. 1991. Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J. Neurosci. 11:1627–1635
Seddon, J.M. 1990. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transition of lipids. Biochim. Biophys. Acta 1031:1–69
Starling, A.P., East, J.M., Lee, A.G. 1993. Effects of phosphatidylcholine fatty acyl chain length on calcium binding and other functions of the (Ca2+-Mg2+)-ATPase. Biochemistry 32:1593–1600
Tate, M.W., Shyamsunder, E., Gruner, S.M., D'Amico, K.L. 1992. Kinetics of the lamellar-inverse hexagonal phase transition determined by time-resolved x-ray diffraction. Biochemistry 31:1081–1092
Toro, L., Vaca, L., Stefani, E. 1991. Calcium-activated potassium channels from coronary smooth muscle reconstituted in lipid bilayers. Am. J. Physiol. 260:H1779–1789
Trave, G., Quignard, J.F., Lionne, C., Sri Widada, J., Liautard, J.P. 1994. Interdependence of phospholipid specificity and calcium binding in annexin I as shown by site-directed mutagenesis. Biochim. Biophys. Acta 1025:215–222
Whitesell, R.R., Regen, D.M., Beth, A.H., Pelletier, D.K., Abumrad, N.A. 1989. Activation energy of the slowest step in the glucose carrier cycle: break at 23°C and correlation with membrane lipid fluidity. Biochemistry 28:5618–5625
Author information
Authors and Affiliations
Additional information
This research was funded in part by a grant (82–2687) from the Arizona Disease Control Research Commission, and a BRSG grant (to R.G.). R.R. was supported by National Institutes of Health Training grant HL-07249.
Rights and permissions
About this article
Cite this article
Chang, H.M., Reitstetter, R. & Gruener, R. Lipid-ion channel interactions: Increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior. J. Membarin Biol. 145, 13–19 (1995). https://doi.org/10.1007/BF00233303
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00233303