Effect of phosphatidylserine on unitary conductance and Ba2+ block of the BK Ca2+-activated K+ channel: Re-examination of the surface charge hypothesis

Journal of General Physiology

Volumn 121, Issue 5, 2003, Pages 375-397

  Park, Jin Bong ^a,c   Kim, Hee Jeong ^a   Ryu, Pan Dong ^a   Moczydlowski, Edward ^b  

^a Seoul National University   (South Korea)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Chungnam National University   (South Korea)

Author keywords

Electrostatics; Gouy Chapman theory; Lipid modulation; Phospholipid; Slowpoke

Indexed keywords

BARIUM ION; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; POTASSIUM CHANNEL; POTASSIUM CHLORIDE;

ARTICLE; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; DISSOCIATION; ELECTRICITY; ENERGY TRANSFER; ION CONDUCTANCE; KINETICS; LIPID BILAYER; MOLECULAR INTERACTION; NONHUMAN; PHYSICAL CHEMISTRY; POTASSIUM CONDUCTANCE; POTASSIUM TRANSPORT; PROTEIN CONFORMATION; SURFACE CHARGE;

ALGORITHMS; ANIMALS; BARIUM; ELECTRIC CONDUCTIVITY; EXTRACELLULAR FLUID; INTRACELLULAR FLUID; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; LIPID BILAYERS; MEMBRANE POTENTIALS; MUSCLE, SKELETAL; PATCH-CLAMP TECHNIQUES; PHOSPHATIDYLSERINES; POTASSIUM; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS;

EID: 0037626076     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200208746     Document Type: Article

References (87)

1. Andersen, O.S. 1989. Kinetics of ion movement mediated by carriers and channels. Methods Enzymol. 171:62-112.
2. Andersen, O.S., C. Nielsen, A.M. Maer, J.A. Lundbaek, M. Goulian, and R.E. Koeppe. 1999. Ion channels as tools to monitor lipid-bilayer-membrane protein interactions: gramicidin channels as molecular force transducers. Methods Enzymol. 294:208-224.
3. Apell, H.-J., E. Bamberg, and P. Läuger. 1979. Effects of surface charge on the conductance of the gramicidin channel. Biochim. Biophys. Acta. 552:369-378.
4. Becker, M.D., R.E. Koeppe II, and O.S. Andersen. 1992. Amino acid substitutions and ion channel function: model dependent conclusions. Biophys. J. 62:25-27.
5. + channel of sarcoplasmic reticulum. Biophys. J. 45:279-287.
6. Ben-Tal, N., B. Honig, C. Miller, and S. McLaughlin. 1997. Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles. Biophys. J. 73:1717-1727.
7. + channel. Nature. 414:73-77.
8. Bezrukov, S.M. 2000. Functional consequences of lipid packing stress. Curr. Opin. Coll. Interface Sci. 5:237-243.
9. Bezrukov, S.M., R.P. Rand, I. Vodyanoy, and V.A. Parsegian. 1998. Lipid packing stress and polypeptide aggregation: alamethicin channel probed by proton titration of lipid charge. Faraday Discuss. 111:173-183.
10. Brelidze, T.I., X. Niu, and K.L. Magleby. 2003. Limits and contributing mechanisms for big single-channel currents in BK channels. Biophys. J. 84:92a.
11. Butler, A., S. Tsunoda, D.P. McCobb, A. Wei, and L. Salkoff. 1993. mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science. 261:221-224.
12. + channel from smooth muscle. Biophys. J. 52:707-716.
13. Chang, H.M., R. Reitstetter, and R. Gruener. 1995a. Lipid-ion channel interactions: increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior. J. Membr. Biol. 145:13-19.
14. Chang, H.M., R. Reistetter, R.P. Mason, and R. Gruener. 1995b. Attenuation of channel kinetics and conductance by cholesterol: an interpretation using structural stress as unifying concept. J. Membr. Biol. 143:51-63.
15. Chu, B., A.M. Dopico, J.R. Lemos, and S.N. Treistman. 1998. Ethanol potentiation of calcium-activated potassium channels reconstituted into planar lipid bilayers. Mol. Pharmacol. 54:397-406.
16. Ca channel activity by fatty acids and other charged lipids: structural requirements and mechanism of action. Am. J. Physiol. Cell Physiol. 283:C1441-C1453.
17. Ca channels from arterial smooth muscle cells. Am. J. Physiol. Cell Physiol. 284: C607-C619.
18. Coronado, R., and H. Affolter. 1986. Insulation of the conduction pathway of muscle transverse tubule calcium channels from the surface charge of bilayer phospholipid. J. Gen. Physiol. 87:933-953.
19. Cukierman, S. 1991. Asymmetric electrostatic effects on the gating of rat brain sodium channels in planar lipid membranes. Biophys. J. 60:845-855.
20. Cukierman, S., W.C. Zinkand, and R.J. French. 1988. Effects of membrane surface charge and calcium on the gating of rat brain sodium channels in planar bilayers. J. Gen. Physiol. 92:431-447.
21. Dowhan, W. 1997. Molecular basis of membrane phospholipid diversity: why are there so many lipids? Annu. Rev. Biochem. 66:199-232.
22. + conduction and selectivity. Science. 280:69-77.
23. Eisenberg, M., T. Gresalfi, T. Riccio, and S. McLaughlin. 1979. Adsorption of monovalent cations to bilayer membranes containing negative phospholipids. Biochemistry. 18:5213-5223.
24. Epand, R.M. 1998. Lipid polymorphism and protein-ligand interactions. Biochim. Biophys. Acta. 1376:353-368.
25. Escobar, L., M.J. Root, and R. MacKinnon. 1993. Influence of protein surface charge on the bimolecular kinetics of a potassium channel peptide inhibitor. Biochemistry. 32:6982-6987.
26. Finkelstein, A., and O.S. Andersen. 1981. The gramicidin A channel: a review of its permeability characteristics with special reference to the single-file aspect of transport. J. Membr. Biol. 59:155-171.
27. 2+ also block. J. Gen. Physiol. 98:163-181.
28. Fonseca, V., P. Daumas, L. Ranjalahy-Rasoloarijoa, F. Heitz, R. Lazaro, Y. Trudelle, and O.S. Andersen. 1992. Gramicidin channels that have no tryptophan residues. Biochemistry. 31:5340-5350.
29. Fyfe, P.K., K.E. McAuley, A.W. Roszak, N.W. Isaacs, R.J. Cogdell, and M.R. Jones. 2001. Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. Trends Biochem. Sci. 26:106-112.
30. Gil, T., J.H. Ipsen, O.G. Mouritsen, M.C. Sabra, M.M. Sperotto, and M.J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid membranes. Biochim. Biophys. Acta. 1376:245-266.
31. Girshman, J., D.V. Greathouse, R.E. Koeppe, and O.S. Andersen. 1997. Gramicidin channels in phospholipid bilayers with unsaturated acyl chains. Biophys. J. 73:1310-1319.
32. Grahame, D. 1947. The electric double layer and the theory of electrocapillarity. Chem. Rev. 41:441-501.
33. Green, W.N., and O.S. Andersen. 1991. Surface charges and ion channel function. Annu. Rev. Physiol. 53:341-359.
34. Green, W.N., L.B. Weiss, and O.S. Andersen. 1987a. Batrachotoxin-modified sodium channels in planar bilayers: ion permeation and block. J. Gen. Physiol. 89:841-872.
35. Green, W.N., L.B. Weiss, and O.S. Andersen. 1987b. Batrachotoxin-modified sodium channels in planar bilayers: characterization of saxitoxin- and tetrodotoxin-induced channel closures. J. Gen. Physiol. 89:841-872.
36. Guo, X., A. Uehara, A. Ravindran, S.H. Bryant, S. Hall, and E. Moczydlowski. 1987. Kinetic basis for insensitivity to tetrodotoxin and saxitoxin in sodium channels of canine heart and denervated rat skeletal muscle. Biochemistry. 26:7546-7556.
37. Hilgemann, D.W., S. Feng, and C. Nasuhoglu. 2001. The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE. 2001:RE19.
38. Hille, B. 2001. Ion Channels of Excitable Membranes. Sinauer, Sunderland, MA. 814 pp.
39. Honig, B., and A. Nicholls. 1995. Classical electrostatics in biology and chemistry. Science. 268:1144-1149.
40. 2 and its stabilization by Gβγ. Nature. 391:803-806.
41. Jiang, Y., and R. MacKinnon. 2000. The barium site in a potassium channel by X-ray crystallography. J. Gen. Physiol. 115:269-272.
42. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002a. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
43. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002b. The open pore conformation of potassium channels. Nature. 417:523-526.
44. Keller, S.L., S.M. Bezrukov, S.M. Gruner, M.W. Tate, I. Vodyanoy, and V.A. Parsegian. 1993. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys. J. 65:23-27.
45. Killian, J.A. 1992. Gramicidin and gramicidin-lipid interactions. Biochim. Biophys. Acta. 1113:391-425.
46. Killian, J.A. 1998. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta. 1376:401-416.
47. Latorre, R., P. Labarca, and D. Naranjo. 1992. Surface charge effects on ion conduction in ion channels. Methods Enzymol. 207: 471-501.
48. LeMasurier, M., L. Heginbotham, and C. Miller. 2001. KcsA: it's a potassium channel. J. Gen. Physiol. 118:303-313.
49. + channels. Am. J. Physiol. Cell Physiol. 280:C1130-C1139.
50. Loosley-Millman, M.E., R.P. Rand, and V.A. Parsegian. 1982. Effect of monovalent ion binding and screening and measured electrostatic forces between charged phospholipid bilayers. Biophys. J. 40:221-232.
51. Lundbaek, J.A., P. Birn, J. Girshman, A.J. Hansen, and O.S. Andersen. 1996. Membrane stiffness and channel function. Biochemistry. 35:3825-3830.
52. Lundbaek, J.A., A.M. Maer, and O.S. Andersen. 1997. Lipid bilayer electrostatic energy, curvature stress, and assembly of gramicidin channels. Biochemistry. 36:5695-5701.
53. + channel. Biochemistry. 28:8092-8099.
54. + channel by trimethyloxonium. Biochemistry. 28: 8087-8092.
55. McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces. Curr. Top. Membr. Trans. 9:71-144.
56. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
57. McLaughlin, S., N. Mulrine, T. Gresalfi, B. Vaio, and A. McLaughlin. 1981. Adsorption of divalent cations to bilayer membranes containing phosphatidylserine. J. Gen. Physiol. 77:445-473.
58. McLaughlin, S.G.A., G. Szabo, G. Eisenman, and S.M. Ciani. 1970. Surface charge and conductance of phospholipid membranes. Proc. Natl. Acad. Sci. USA. 67:1268-1275.
59. + channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), and extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc. Natl. Acad. Sci. USA. 94:14066-14071.
60. + channel in planar lipid bilayers. J. Membr. Biol. 83:273-282.
61. + selectivity filter. Nature. 414:37-42.
62. + channels. Biophys. J. 71:220-226.
63. + channel. J. Gen. Physiol. 92:569-586.
64. Nimigean, C., J. Chappie, and C. Miller. 2003. Why are BK channels so big? Biophys. J. 84:8a.
65. + channels in negatively-charged lipid membranes. Korean J. Physiol. Pharmacol. 2:529-539.
66. Popot, J.-L., and D.M. Engleman. 2000. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:881-922.
67. Ravindran, A., and E. Moczydlowski. 1989. Influence of negative surface charge on toxin binding to canine heart Na channels in planar bilayers. Biophys. J. 55:359-365.
68. + channels. J. Gen. Physiol. 97:89-115.
69. Rietveld, A., and K. Simons. 1998. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta. 1376:467-479.
70. Rohács, T., C.M.B. Lopes, T. Jin, P.P. Ramdya, Z. Molnar, and D.E. Logothetis. 2003. Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc. Natl. Acad. Sci. USA. 100:745-750.
71. Rostovtseva, T.K., V.M. Aguilella, I. Vodoyany, S. Bezrukov, and V.A. Parsegian. 1998. Membrane surface-charge titration probed by gramicidin A channel conductance. Biophys. J. 75:1783-1792.
72. ATP channels. Science. 282:1138-1141.
73. + channel from human vas deferens epithelial cells. Biophys. J. 70:1316-1325.
74. + channel vestibule. Proc. Natl. Acad. Sci. USA. 91:9509-9513.
75. + channels in goldfish saccular hair cells. J. Gen. Physiol. 111:363-379.
76. Turnheim, K., J. Gruber, C. Wachter, and V. Ruiz-Gutierrez. 1999. Membrane phospholipid composition affects function of potassium channels from rabbit colon epithelium. Am. J. Physiol. 277: C83-C90.
77. Valiyaveetil, F.I., Y. Zhou, and R. MacKinnon. 2002. Lipids in the structure, folding, and function of the KcsA channel. Biochemistry. 41:10771-10777.
78. Van Dalen, A., S. Hegger, J.A. Killian, and B. de Kruijff. 2002. Influence of lipids on assembly and stability of the potassium channel, KcsA. FEBS Lett. 525:33-38.
79. 2+ blockade. J. Gen. Physiol. 82:543-568.
80. + channel with quaternary ammonium ions. Pflugers Arch. 413:118-126.
81. Walters, F.S., M. Covarrubias, and J.S. Ellingson. 2000. Potent inhibition of the aortic smooth muscle maxi-K channel by clinical doses of ethanol. Am. J. Physiol. Cell Physiol. 279:C1107-C1115.
82. Williamson, I.M., S.J. Alvis, J.M. East, and A.G. Lee. 2002. Interactions of phospholipids with the potassium channel KcsA. Biophys. J. 83:2026-2038.
83. Woolf, T.B., and B. Roux. 1996. Structure, energetics, and dynamics of lipid-protein interactions: a molecular dynamics study of the gramicidin A channel in a DMPC bilayer. Proteins. 24:92-114.
84. Worley, J.F., R.J. French, and B.K. Krueger. 1986. Trimethyloxonium modification of single batrachotoxin-activated sodium channels in planar bilayers: changes in unit conductance and in block by saxitoxin and calcium. J. Gen. Physiol. 87:327-349.
85. Worley, J.F., R.J. French, B.A. Pailthorpe, and B.K. Krueger. 1992. Lipid surface charge does not influence conductance or calcium block of single sodium channels in planar bilayers. Biophys. J. 61: 1353-1363.
86. + channel. Cell. 111:231-239.
87. + channel-Fab complex at 2.0 Å resolution. Nature. 414:43-48.