Thiazolidinedione insulin sensitizers alter lipid bilayer properties and voltage-dependent sodium channel function: Implications for drug discovery

Journal of General Physiology

Volumn 138, Issue 2, 2011, Pages 249-270

  Rusinova, Radda ^a   Herold, Karl F ^a,c   Lea Sanford, R ^a   Greathouse, Denise V ^b   Hemmings, Hugh C ^a   Andersen, Olaf S ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; CHROMAN DERIVATIVE; CIGLITAZONE; GRAMICIDIN; INSULIN; ION CHANNEL; MEMBRANE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; ROSIGLITAZONE; SODIUM CHANNEL; TROGLITAZONE;

ANIMAL; ARTICLE; CELL LINE; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECT; LIPID BILAYER; METABOLISM; METHODOLOGY; PHYSIOLOGY; RAT;

ANIMALS; CELL LINE; CELL MEMBRANE; CHROMANS; DRUG DISCOVERY; GRAMICIDIN; INSULIN; ION CHANNELS; LIPID BILAYERS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; PPAR GAMMA; RATS; SODIUM CHANNELS; THIAZOLIDINEDIONES;

EID: 79961107148     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010529     Document Type: Article

References (112)

1. Ahn, H.S., S.E. Kim, H.J. Jang, M.J. Kim, D.J. Rhie, S.H. Yoon, Y.H. Jo, M.S. Kim, K.W. Sung, S.Y. Kim, and S.J. Hahn. 2007. Open channel block of Kv1.3 by rosiglitazone and troglitazone: Kv1.3 as the pharmacological target for rosiglitazone. Naunyn Schmiedebergs Arch. Pharmacol. 374:305-309.
2. Aleo, M.D., C.M. Doshna, and K.A. Navetta. 2005. Ciglitazone-induced lenticular opacities in rats: in vivo and whole lens explant culture evaluation. J. Pharmacol. Exp. Ther. 312:1027-1033.
3. Andersen, O.S. 1983. Ion movement through gramicidin A channels. Single-channel measurements at very high potentials. Biophys. J. 41:119-133.
4. Andersen, O.S. 2008. Perspectives on how to drug an ion channel. J. Gen. Physiol. 131:395-397.
5. Andersen, O.S., and R.E. Koeppe II. 2007. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36:107-130.
6. Andersen, O.S., D.B. Sawyer, and R.E. Koeppe II. 1992. Modulation of channel function by the host bilayer. In Biomembrane Structure and Function. K.R.K. Easwaran and B. Gaber, editors. Adenine Press, Schenectady, NY. 227-244.
7. Andersen, O.S., M.J. Bruno, H. Sun, and R.E. Koeppe II. 2007. Single-molecule methods for monitoring changes in bilayer elastic properties. Methods Mol. Biol. 400:543-570.
8. 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.
9. Artigas, P., S.J. Al'aref, E.A. Hobart, L.F. Díaz, M. Sakaguchi, S. Straw, and O.S. Andersen. 2006. 2,3-butanedione monoxime affects cystic fibrosis transmembrane conductance regulator channel function through phosphorylation-dependent and phosphorylationindependent mechanisms: the role of bilayer material properties. Mol. Pharmacol. 70:2015-2026.
10. Ashrafuzzaman, M., M.A. Lampson, D.V. Greathouse, R.E. Koeppe II, and O.S. Andersen. 2006. Manipulating lipid bilayer material properties using biologically active amphipathic molecules. J. Phys. Condens. Matter. 18:S1235-S1255.
11. Avdeef, A., K.J. Box, J.E. Comer, C. Hibbert, and K.Y. Tam. 1998. pH-metric logP 10. Determination of liposomal membrane-water partition coefficients of ionizable drugs. Pharm. Res. 15:209-215.
12. Bamberg, E., and P. Läuger. 1973. Channel formation kinetics of gramicidin A in lipid bilayer membranes. J. Membr. Biol. 11:177-194.
13. Bañó, M.C., L. Braco, and C. Abad. 1992. A semi-empirical approach for the simulation of circular dichroism spectra of gramicidin A in a model membrane. Biophys. J. 63:70-77.
14. Berberan-Santos, M.N., E.N. Bodunov, and B. Valeur. 2005. Mathematical functions for the analysis of luminescence decays with underlying distributions 1. Kohlrausch decay function (stretched exponential). Chem. Phys. 315:171-182.
15. Bezanilla, F., and C.M. Armstrong. 1977. Inactivation of the sodium channel. I. Sodium current experiments. J. Gen. Physiol. 70:549-566.
16. Bruno, M.J., R.E. Koeppe II, and O.S. Andersen. 2007. Docosahexaenoic acid alters bilayer elastic properties. Proc. Natl. Acad. Sci. USA. 104:9638-9643.
17. Chen, Z., and R.P. Rand. 1998. Comparative study of the effects of several n-alkanes on phospholipid hexagonal phases. Biophys. J. 74:944-952.
18. de Dios, S.T., K.M. Hannan, R.J. Dilley, M.A. Hill, and P.J. Little. 2001. Troglitazone, but not rosiglitazone, inhibits Na/H exchange activity and proliferation of macrovascular endothelial cells. J. Diabetes Complications. 15:120-127.
19. Deisenhofer, J., O. Epp, I. Sinning, and H. Michel. 1995. Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol. 246:429-457.
20. Durkin, J.T., R.E. Koeppe II, and O.S. Andersen. 1990. Energetics of gramicidin hybrid channel formation as a test for structural equivalence. Side-chain substitutions in the native sequence. J. Mol. Biol. 211:221-234.
21. Edsall, J.T., and J. Wyman. 1958. Biophysical Chemistry. Volume 1. Academic Press, New York. 699 pp.
22. Elliott, J.R., D. Needham, J.P. Dilger, and D.A. Haydon. 1983. The effects of bilayer thickness and tension on gramicidin single-channel lifetime. Biochim. Biophys. Acta. 735:95-103.
23. Epshtein, Y., A.P. Chopra, A. Rosenhouse-Dantsker, G.B. Kowalsky, D.E. Logothetis, and I. Levitan. 2009. Identification of a C-terminus domain critical for the sensitivity of Kir2.1 to cholesterol. Proc. Natl. Acad. Sci. USA. 106:8055-8060.
24. Escher, B.I., and R.P. Schwarzenbach. 1996. Partitioning of substituted phenols in liposome-water, biomembrane-water, and octanol-water systems. Environ. Sci. Technol. 30:260-270.
25. European Medicines Agency. 2011. Avandia. http://www.ema.europa .eu/ema/index.jsp?curl=pages/medicines/human/medicines/ 000268/human_med_000662.jsp&murl=menus/medicines/medicines.jsp (accessed July 6, 2011).
26. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J. Phys. Chem. 91:4219-4228.
27. Evans, E., and W. Rawicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094-2097.
28. Evans, E.A., and S. Simon. 1975. Mechanics of electrocompression of lipid bilayer membranes. Biophys. J. 15:850-852.
29. Evans, E., W. Rawicz, and A.F. Hofmann. 1995. Lipid bilayer expansion and mechanical disruption in solutions of water-soluble bile acid. In Bile Acids in Gastroenterology: Basic and Clinical Advances. A.F. Hofmann, G. Paumgartner, and A. Stiehl, editors. Kluwer Academic Publishers, Dordrecht, Netherlands. 59-68.
30. Fattal, D.R., and A. Ben-Shaul. 1993. A molecular model for lipid-protein interaction in membranes: the role of hydrophobic mis match. Biophys. J. 65:1795-1809.
31. Fernández, J.M., R.E. Taylor, and F. Bezanilla. 1983. Induced capacitance in the squid giant axon. Lipophilic ion displacement currents. J. Gen. Physiol. 82:331-346.
32. Fernandez, J.M., A.P. Fox, and S. Krasne. 1984. Membrane patches and whole-cell membranes: a comparison of electrical properties in rat clonal pituitary (GH3) cells. J. Physiol. 356:565-585.
33. Food and Drug Administration. 2010. FDA significantly restricts access to the diabetes drug Avandia. http://www.fda.gov/Drugs/DrugSafety/PostmarketDrugSafetyInformationforPatientsand Providers/ucm226956.htm (accessed July 6, 2011).
34. Fujiwara, T., and H. Horikoshi. 2000. Troglitazone and related compounds: therapeutic potential beyond diabetes. Life Sci. 67:2405-2416.
35. Fujiwara, T., S. Yoshioka, T. Yoshioka, I. Ushiyama, and H. Horikoshi. 1988. Characterization of new oral antidiabetic agent CS-045. Studies in KK and ob/ob mice and Zucker fatty rats. Diabetes. 37:1549-1558.
36. Funk, C., C. Ponelle, G. Scheuermann, and M. Pantze. 2001. Cholestatic potential of troglitazone as a possible factor contributing to troglitazone-induced hepatotoxicity: in vivo and in vitro interaction at the canalicular bile salt export pump (Bsep) in the rat. Mol. Pharmacol. 59:627-635.
37. Galbraith, T.P., and B.A. Wallace. 1998. Phospholipid chain length alters the equilibrium between pore and channel forms of gramicidin. Faraday Discuss. 111:159-164.
38. Giaginis, C., S. Theocharis, and A. Tsantili-Kakoulidou. 2007. A consideration of PPAR-gamma ligands with respect to lipophilicity: current trends and perspectives. Expert Opin. Investig. Drugs. 16:413-417.
39. 1β2γ2S GABAA receptors in rapidly perfused whole cells and membrane patches: divergent results can be explained by pharmacokinetics. J. Gen. Physiol. 133:171-188.
40. Goulian, M., O.N. Mesquita, D.K. Fygenson, C. Nielsen, O.S. Andersen, and A. Libchaber. 1998. Gramicidin channel kinetics under tension. Biophys. J. 74:328-337.
41. Graham, D.J., R. Ouellet-Hellstrom, T.E. MaCurdy, F. Ali, C. Sholley, C. Worrall, and J.A. Kelman. 2010. Risk of acute myocardial infarction, stroke, heart failure, and death in elderly Medicare patients treated with rosiglitazone or pioglitazone. JAMA. 304:411-418.
42. Greathouse, D.V., J.F. Hinton, K.S. Kim, and R.E. Koeppe II. 1994. Gramicidin A/short-chain phospholipid dispersions: chain length dependence of gramicidin conformation and lipid organization. Biochemistry. 33:4291-4299.
43. Greathouse, D.V., R.E. Koeppe II, L.L. Providence, S. Shobana, and O.S. Andersen. 1999. Design and characterization of gramicidin channels. Methods Enzymol. 294:525-550.
44. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100.
45. Harned, H.S., and B.B. Owen. 1943. The Physical Chemistry of Electrolytic Solutions. Reinhold Publishing Corporation, New York. 611 pp.
46. He, K., S.J. Ludtke, Y. Wu, H.W. Huang, O.S. Andersen, D. Greathouse, and R.E. Koeppe II. 1994. Closed state of gramicidin channel detected by X-ray in-plane scattering. Biophys. Chem. 49:83-89.
47. Heerklotz, H., and J. Seelig. 2000. Titration calorimetry of surfactant-membrane partitioning and membrane solubilization. Biochim. Biophys. Acta. 1508:69-85.
48. Helfrich, P., and E. Jakobsson. 1990. Calculation of deformation energies and conformations in lipid membranes containing gramicidin channels. Biophys. J. 57:1075-1084.
49. Henke, B.R., S.G. Blanchard, M.F. Brackeen, K.K. Brown, J.E. Cobb, J.L. Collins, W.W. Harrington Jr., M.A. Hashim, E.A. Hull-Ryde, I. Kaldor, et al. 1998. N-(2-Benzoylphenyl)-L-tyrosine PPARgamma agonists. 1. Discovery of a novel series of potent antihyperglycemic and antihyperlipidemic agents. J. Med. Chem. 41:5020-5036.
50. Hodgkin, A.L., and A.F. Huxley. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544.
51. Huang, H.W. 1986. Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime. Biophys. J. 50:1061-1070.
52. Hulin, B., P.A. McCarthy, and E.M. Gibbs. 1996. The glitazone family of antidiabetic drugs. Curr. Pharm. Des. 2:85-102.
53. Hwang, T.C., R.E. Koeppe II, and O.S. Andersen. 2003. Genistein can modulate channel function by a phosphorylation-independent mechanism: importance of hydrophobic mismatch and bilayer mechanics. Biochemistry. 42:13646-13658.
54. Ingólfsson, H.I., and O.S. Andersen. 2010. Screening for small molecules' bilayer-modifying potential using a gramicidin-based fluorescence assay. Assay Drug Dev. Technol. 8:427-436.
55. Ingólfsson, H.I., R.E. Koeppe II, and O.S. Andersen. 2007. Curcumin is a modulator of bilayer material properties. Biochemistry. 46:10384-10391.
56. Ingólfsson, H.I., R.L. Sanford, R. Kapoor, and O.S. Andersen. 2010. Gramicidin-based fluorescence assay; for determining small molecules potential for modifying lipid bilayer properties. J. Vis. Exp. 2131.
57. Juurlink, D.N. 2010. Rosiglitazone and the case for safety over certainty. JAMA. 304:469-471.
58. Kapoor, R., J.H. Kim, H. Ingolfson, and O.S. Andersen. 2008. Preparation of artificial bilayers for electrophysiology experiments. J. Vis. Exp. 1033.
59. Katsaras, J., R.S. Prosser, R.H. Stinson, and J.H. Davis. 1992. Constant helical pitch of the gramicidin channel in phospholipid bilayers. Biophys. J. 61:827-830.
60. 2+ channels. Am. J. Physiol. Cell Physiol. 288:C389-C395.
61. Knock, G.A., S.K. Mishra, and P.I. Aaronson. 1999. Differential effects of insulin-sensitizers troglitazone and rosiglitazone on ion currents in rat vascular myocytes. Eur. J. Pharmacol. 368:103-109.
62. Le Blanc, O.H. Jr. 1969. Tetraphenylborate conductance through lipid bilayer membranes. Biochim. Biophys. Acta. 193:350-360.
63. Lee, A.G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87.
64. Lee, K., T. Ibbotson, P.J. Richardson, and P.R. Boden. 1996. Inhibition of KATP channel activity by troglitazone in CRI-G1 insulin-secreting cells. Eur. J. Pharmacol. 313:163-167.
65. Leeson, P.D., and B. Springthorpe. 2007. The influence of drug-like concepts on decision-making in medicinal chemistry. Nat. Rev. Drug Discov. 6:881-890.
66. Lipinski, C.A., F. Lombardo, B.W. Dominy, and P.J. Feeney. 2001. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46:3-26.
67. Lundbæk, J.A. 2008. Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs. J. Gen. Physiol. 131:421-429.
68. Lundbæk, J.A., and O.S. Andersen. 1994. Lysophospholipids modulate channel function by altering the mechanical properties of lipid bilayers. J. Gen. Physiol. 104:645-673.
69. Lundbæk, J.A., and O.S. Andersen. 1999. Spring constants for channel-induced lipid bilayer deformations. Estimates using gramicidin channels. Biophys. J. 76:889-895.
70. Lundbæk, J.A., P. Birn, J. Girshman, A.J. Hansen, and O.S. Andersen. 1996. Membrane stiffness and channel function. Biochemistry. 35:3825-3830.
71. Lundbæk, J.A., P. Birn, A.J. Hansen, R. Søgaard, C. Nielsen, J. Girshman, M.J. Bruno, S.E. Tape, J. Egebjerg, D.V. Greathouse, et al. 2004. Regulation of sodium channel function by bilayer elasticity: the importance of hydrophobic coupling. Effects of Micelle-forming amphiphiles and cholesterol. J. Gen. Physiol. 123:599-621.
72. Lundbæk, J.A., P. Birn, S.E. Tape, G.E. Toombes, R. Søgaard, R.E. Koeppe II, S.M. Gruner, A.J. Hansen, and O.S. Andersen. 2005. Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. Mol. Pharmacol. 68:680-689.
73. Lundbæk, J.A., S.A. Collingwood, H.I. Ingólfsson, R. Kapoor, and O.S. Andersen. 2010a. Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes. J. R. Soc. Interface. 7:373-395.
74. Lundbæk, J.A., R.E. Koeppe II, and O.S. Andersen. 2010b. Amphiphile regulation of ion channel function by changes in the bilayer spring constant. Proc. Natl. Acad. Sci. USA. 107:15427-15430.
75. Ly, H.V., and M.L. Longo. 2004. The influence of short-chain alcohols on interfacial tension, mechanical properties, area/molecule, and permeability of fluid lipid bilayers. Biophys. J. 87:1013-1033.
76. Marsh, D. 2008. Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta. 1778:1545-1575.
77. Nakamura, Y., Y. Ohya, U. Onaka, K. Fujii, I. Abe, and M. Fujishima. 1998. Inhibitory action of insulin-sensitizing agents on calcium channels in smooth muscle cells from resistance arteries of guineapig. Br. J. Pharmacol. 123:675-682.
78. Needham, D., and R.S. Nunn. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997-1009.
79. Nielsen, C., and O.S. Andersen. 2000. Inclusion-induced bilayer deformations: effects of monolayer equilibrium curvature. Biophys. J. 79:2583-2604.
80. Nielsen, C., M. Goulian, and O.S. Andersen. 1998. Energetics of inclusion-induced bilayer deformations. Biophys. J. 74:1966-1983.
81. Nissen, S.E., and K. Wolski. 2010. Rosiglitazone revisited: an updated meta-analysis of risk for myocardial infarction and cardiovascular mortality. Arch. Intern. Med. 170:1191-1201.
82. Nury, H., C. Van Renterghem, Y. Weng, A. Tran, M. Baaden, V. Dufresne, J.P. Changeux, J.M. Sonner, M. Delarue, and P.J. Corringer. 2011. X-ray structures of general anaesthetics bound to a pentameric ligand-gated ion channel. Nature. 469:428-431.
83. O'Connell, A.M., R.E. Koeppe II, and O.S. Andersen. 1990. Kinetics of gramicidin channel formation in lipid bilayers: transmembrane monomer association. Science. 250:1256-1259.
84. Partenskii, M.B., and P.C. Jordan. 2002. Membrane deformation and the elastic energy of insertion: perturbation of membrane elastic constants due to peptide insertion. J. Chem. Phys. 117:10768-10776.
85. Peitzsch, R.M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:10436-10443.
86. Preininger, K., H. Stingl, R. Englisch, C. Fürnsinn, J. Graf, W. Waldhäusl, and M. Roden. 1999. Acute troglitazone action in isolated perfused rat liver. Br. J. Pharmacol. 126:372-378.
87. Requena, J., D.A. Haydon, and S.B. Hladky. 1975. Letter: lenses and the compression of black lipid membranes by an electric field. Biophys. J. 15:77-81.
88. Rokitskaya, T.I., Y.N. Antonenko, and E.A. Kotova. 1996. Photodynamic inactivation of gramicidin channels: a flash-photolysis study. Biochim. Biophys. Acta. 1275:221-226.
89. Rossotti, F.J., and H. Rossoti. 1961. The Determination of Stability Constants and Other Equilibrium Constants in Solution. McGraw-Hill, New York. 425 pp.
90. Sarafidis, P.A. 2008. Thiazolidinedione derivatives in diabetes and cardiovascular disease: an update. Fundam. Clin. Pharmacol. 22: 247-264.
91. Scheen, A.J. 2001. Thiazolidinediones and liver toxicity. Diabetes Metab. 27:305-313.
92. Seddon, A.M., D. Casey, R.V. Law, A. Gee, R.H. Templer, and O. Ces. 2009. Drug interactions with lipid membranes. Chem. Soc. Rev. 38:2509-2519.
93. Seddon, J.M. 1990. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim. Biophys. Acta. 1031:1-69.
94. Seeman, P. 1972. The membrane actions of anesthetics and tranquilizers. Pharmacol. Rev. 24:583-655.
95. Snow, K.L., and R.H. Moseley. 2007. Effect of thiazolidinediones on bile acid transport in rat liver. Life Sci. 80:732-740.
96. Søgaard, R., T.M. Werge, C. Bertelsen, C. Lundbye, K.L. Madsen, C.H. Nielsen, and J.A. Lundbaek. 2006. GABAA receptor function is regulated by lipid bilayer elasticity. Biochemistry. 45:13118-13129.
97. Spector, A.A., and M.A. Yorek. 1985. Membrane lipid composition and cellular function. J. Lipid Res. 26:1015-1035.
98. Stowers, M.A., A.L. van Wuijckhuijse, J.C. Marijnissen, B. Scarlett, B.L. van Baar, and C.E. Kientz. 2000. Application of matrixassisted laser desorption/ionization to on-line aerosol time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 14: 829-833.
99. 5.6 helix of gramicidin A predominates in unsaturated lipid membranes. Eur. Biophys. J. 22:279-288.
100. Torii, H., K. Yoshida, T. Tsukamoto, and S. Tanayama. 1984. Disposition in rats and dogs of ciglitazone, a new antidiabetic agent. Xenobiotica. 14:259-268.
101. Turner, D.C., and S.M. Gruner. 1992. X-ray diffraction reconstruction of the inverted hexagonal (HII) phase in lipid-water systems. Biochemistry. 31:1340-1355.
102. Veatch, W.R., R. Mathies, M. Eisenberg, and L. Stryer. 1975. Simultaneous fluorescence and conductance studies of planar bilayer membranes containing a highly active and fluorescent analog of gramicidin A. J. Mol. Biol. 99:75-92.
103. Wallace, B.A., W.R. Veatch, and E.R. Blout. 1981. Conformation of gramicidin A in phospholipid vesicles: circular dichroism studies of effects of ion binding, chemical modification, and lipid structure. Biochemistry. 20:5754-5760.
104. Wendt, D.J., C.F. Starmer, and A.O. Grant. 1992. Na channel kinetics remain stable during perforated-patch recordings. Am. J. Physiol. 263:C1234-C1240.
105. Wenk, M.R., T. Alt, A. Seelig, and J. Seelig. 1997. Octyl-beta-D-glucopyranoside partitioning into lipid bilayers: thermodynamics of binding and structural changes of the bilayer. Biophys. J. 72:1719-1731.
106. White, S.H. 1974. Letter: comments on "electrical breakdown of bimolecular lipid membranes as an electromechanical instability" . Biophys. J. 14:155-158.
107. White, S.H., and T.E. Thompson. 1973. Capacitance, area, and thickness variations in thin lipid films. Biochim. Biophys. Acta. 323:7-22.
108. White, S.H., W.C. Wimley, A.S. Ladokhin, and K. Hristova. 1998. Protein folding in membranes: determining energetics of peptide-bilayer interactions. Methods Enzymol. 295:62-87.
109. Xue, Y.J., K.C. Turner, J.B. Meeker, J. Pursley, M. Arnold, and S. Unger. 2003. Quantitative determination of pioglitazone in human serum by direct-injection high-performance liquid chromatography mass spectrometry and its application to a bioequivalence study. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 795:215-226.
110. Zhelev, D.V. 1998. Material property characteristics for lipid bilayers containing lysolipid. Biophys. J. 75:321-330.
111. Zhou, Y., and R.M. Raphael. 2005. Effect of salicylate on the elasticity, bending stiffness, and strength of SOPC membranes. Biophys. J. 89:1789-1801.
112. Zingsheim, H.P., and E. Neher. 1974. The equivalence of fluctuation analysis and chemical relaxation measurements: a kinetic study of ion pore formation in thin lipid membranes. Biophys. Chem. 2:197-207.