Hydration changes implicated in the remarkable temperature-dependent membrane permeation of cyclosporin A

Biochemistry

Volumn 39, Issue 25, 2000, Pages 7621-7630

  Augustijns, Patrick F ^a   Brown, Stephen C ^b,c   Willard, Derril H ^b   Consler, Thomas G ^b   Annaert, Pieter P ^a   Hendren, R Wayne ^b   Bradshaw, Timothy P ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GLAXOSMITHKLINE   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN; CYCLOSPORIN A;

ARTICLE; CONFORMATIONAL TRANSITION; DRUG CONFORMATION; DRUG PENETRATION; HYDRATION; HYDROGEN BOND; ISOMERISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE;

CACO-2 CELLS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CYCLOSPORINE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; SOLUBILITY; TEMPERATURE; WATER;

EID: 0034720737     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9929709     Document Type: Article

References (52)

1. Lindholm A., Henricsson S., and Dahlqvist R. (1990) The Effect of Food and Bile Acid Administration on the Relative Bioavailability of Cyclosporin. Br. J. Clin. Pharmac. 29, 541-548.
2. Ptachcinski, R. J., Venkataramanan, R., and Burckart, G. J. (1986) Clinical Pharmocokinetics of Cyclosporin. Clin. Pharmacokinet. 11, 107-132.
3. Wood, A. J., Maurer, G., Niederberger, W., and Beveridge, T. (1983) Cyclosporine: Pharmacokinetics, Metabolism, and Drug Interactions. Transplant. Proc. 15, 2409-2412.
4. Tjia, J. F., Webber, I. R., and Back D. J. (1991) Cyclosporin Metabolism by the Gastrointestinal Mucosa. Br. J. Clin. Pharmac. 31, 344-346.
5. Grevel J. (1986) Absorption of Cyclosporin A After Oral Dosing. Transplant. Proc. 18, 9-15.
6. Kolars, J. C., Stetson, P. L., Rush, B. D., Ruwart, M. J., Schmiedlin-Ren, P., Duell, E. A., Vorhees, J. J., and Watkins, P. B. (1992) Cyclosporine Metabolism by P450IIIA in Rat Enterocytes-Another Determinant of Oral Bioavailability? Transplantation 53, 596-602.
7. McMillan, M. A. (1989) Clinical Pharmacokinetics of Cyclosporin. Pharmacol. Ther. 42, 135-56.
8. Ueda, C. T., Lemaire, M., Gsell, G., Misslin P., and Nussbaumer K. (1984) Apparent Dose-dependent Oral Absorption of Cyclosporin A in Rats. Biopharm. Drug Dispos. 5, 141-51.
9. Hebert, M. F., Roberts, J. P., Prueksaritanont, T., and Benet, L. Z. (1992) Bioavailability of Cydosporine with Concomitant Rifampin Administration is Markedly Less than Predicted by Hepatic Enzyme Induction. Clin. Pharmacol. Ther. 52, 453-457.
10. Hidalgo, I. J., Raub, T. J., and Borcardt, R. T. (1989) Characterization of the Human Colon Carcinoma Line (Caco-2) as a Model System for Intestinal Epithelial Permeability. Gastroenterology 96, 736-749.
11. Wilson, G., Hassan, I. F., Dix, C. J., Williamson, I., Shah, R., Mackay, M., and Artursson, P. (1990) Transport and Permeability Properties of Human Caco-2 Cells: An In Vitro Model of the Intestinal Epithelial Cell Barrier. J. Cont. Relat. 11, 25-40.
12. Augustijns, P. F., Bradshaw, T. P., Gan, L.-S. L., Hendren, R. W., and Thakker, D. R. (1993) Evidence for a Polarized Efflux System in Caco-2 Cells Capable of Modulating Cyclosporin A Transport. Biochem. Biophys. Res. Commun. 197, 360-365.
13. Wenger, R. (1983) Synthesis of Cyclosporin and Analogues: Structure, Activity, Relationships of New Cyclosporin Derivatives. Transplant. Proc. 15, 2230-2241.
14. Borel, J. F., Feurer, C., Gubler, H. U., and Stahelin, H. (1976) Biological Effects of Cyclosporin A: A New Antilymphocytic Agent. Agents Actions 6, 468-475.
15. Wenger, R. M. (1983) Synthesis of Cyclosporin. 1. Synthesis of Enantiomerically Pure (2S, 3R, 4R, 6E)-3-Hydroxy-4-methyl-2-methylamino-6-octenoic Acid Starting from Tartaric Acid. Helv. Chim. Acta 66, 2308-2321.
16. Kessler, H., Kock, M., Wein, T., and Gehrke, M. (1990) Reinvestigation of the Conformation of Cyclosporin A in Chloroform. Helv. Chim. Acta 73, 1818-1832.
17. Loosli, H.-R., Kessler, H., Oschkinat, H., Weber, H.-P., Petcher, T. J., and Widmer, A. (1985) The Conformation of Cyclosporin A in the Crystal and in Solution. Helv. Chim. Acta 68, 682-704.
18. Wenger, R. M. (1988) Methodologic Advances in Cyclosporine Measurement. Transplant. Proc. 20, 313-318.
19. Thériault, Y., Logan, T. M., Meadows, R., Yu, L., Olejniczak, E. T., Holzman, T. F., Simmer, R. L., and Fesik, S. W. (1993) Solution Structure of the Cyclosporin A/Cyclophilin Complex by NMR. Nature 361, 88-91.
20. Gallion, S., and Ringe, D. (1992) Molecular Modeling Studies of the Complex Between Cyclophilin and Cyclosporin A. Protein Eng. 5, 391-397.
21. Weber, C., Wider, G., von Freyberg, B., Traber, R., Braun, W., Widmer, H., and Wüthrich, K. (1991) The NMR Structure of Cyclosporin A Bound to Cyclophilin in Aqueous Solution. Biochemistry 30, 6563-6574.
22. Lautz, J. K., Kessler, H., Kaptein, H. R., and van Gunsteren, W. F. (1987) Molecular Dynamics Simulations of Cyclosporin A: The Crystal Structure and Dynamic Modeling of a Structure in Apolar Solution-based NMR Data. J. Comput. Aided Mol. Des. 1, 219-241.
23. Lautz, J., Kessler, H., van Gunsteren, W. F., Weber, H.-P., and Wenger, R. M. (1990) On the Dependence of Molecular Conformation on the Type of Solvent Environment: A Molecular Dynamics Study of Cyclosporin A. Biopolymers 29, 1669-1687.
24. 6 by a Combination of Homo-and Heteronuclear Two-Dimensional Techniques. Helv. Chim. Acta 68, 661-704.
25. Ko, S. Y., and Dalvit, C. (1992) Conformation of Cyclosporin A in Polar Solvents. Int. J. Pept. Protein Res. 40, 380-382.
26. Kofron, J. L., Kuzmic, P., Kisbore, V., Gemmecker, G., Fesok, S. W., and Rich, D. H. (1992) Lithium Chloride Perturbation of Cis-Trans Peptide Bond Equilibria: Effect on Conformational Equilibria in Cyclosporin A and on Time-Dependent Inhibition of Cyclophilin. J. Am. Chem. Soc. 114, 2670-2675.
27. Hsu, V. L., Heald, S. L., Harding M. W., Handschumacher, R. E., and Armitage, I. M. (1990) Structural Elements Pertinent to the Interaction of Cyclosporin A with its Specific Receptor Protein, Cyclophilin. Biochem. Pharmacol. 40, 131-140.
28. Burton, P. S., Conradi, R. A., and Hilgers, A. R. (1991) Mechanisms of Peptide and Protein Absorption. Adv. Drug Del. Rev. 7, 365-386.
29. Burton, P. S., Conradi, R. A., Hilgers, A. R., Ho, N. F. H., and Maggiora, L. L. (1992) The Relationship Between Peptide Structure and Transport Across Epithelial Cell Monolayers. J. Controlled Rel. 19, 87-98.
30. Chikhale, E. G., Ng, K.-Y., Burton, P. S., and Borchardt, R. T. (1994) Hydrogen Bonding Potential as a Determinant of the In Vitro and In Situ Blood-Brain Barrier Permeability of Peptides. Pharm. Res. 11, 412-419.
31. Conradi, R. A., Hilgers, A. R., Ho, N. F. H., and Burton, P. S. (1991) The Influence of Peptide Structure on Transport Across Caco-2 Cell. Pharm. Res. 8, 1453-1460.
32. Plateau, P., and Guéron, M. (1982) Exchangeable Proton NMR without Base-Line Distortion, Using New Strong-Pulse Sequences. J. Am. Chem. Soc. 104, 7310-7311.
33. Piotto, M., Saudek, V., and Sklenár, V. (1992) Gradient-tailored Excitation for Single-quantum NMR Spectroscopy of Aqueous Solutions. J. Biomol. NMR 2, 661-665.
34. Marquardt, D. W. (1963) An Algorithm for Least-Squares Estimation of Nonlinear Parameters. J. Soc. Indust. Appl. Math. 11, 431-441.
35. Fahr, A. (1993) Cyclosporin Clinical Pharmacokinetics. Clin. Pharmacokinet. 24, 472-495.
36. LeGrue, S. J., Friedman, A. W., and Kahan, B. D. (1983) Binding of Cyclosporin by Human Lymphocytes and Phospholipid Vesicles. J. Immumol. 131, 712-717.
37. Merker, M. M., and Handschumacher, R. E. (1984) Uptake and Nature of the Intracellular Binding of Cyclosporin A in a Murine Thymoma Cell Line, BW5147. J. Immumol. 132, 3064-3079.
38. Fricker, G., and Fahr, A. (1997) Mechanisms of Hepatic Transport of Cyclosporin A: An Explanation for its Cholestatic Action? Yale J. Biol. Med. 7, 379-390.
39. Artursson, P., and Karlsson, J. (1991) Correlation Between Oral Drug Absorption in Humans and Apparent Drug Permeability Coefficients in Human Intestinal Epithelial (Caco-2) Cells. Biochem. Biophys. Res. Commun. 175, 880-885.
40. Chong, S., Dando, S. A., Soucek, K. M., and Morrison, R. A. (1996) In Vitro Permeability Through Caco-2 Cells is not Quantitatively Predictive of In Vivo Absorption for Peptide-Like Drugs Absorbed Via the Dipeptide Transporter System. Pharm. Res. 13, 120-123.
41. Brasitus, T. A., Tall, A. R., and Schachter, D. (1980) Thermotropic Transitions in Rat Intestinal Plasma Membranes Studies by Differential Scanning Calorimetry and Fluorescence Polarization. Biochemistry 19, 1256-1261.
42. Ismailos, G., Reppas, C., Dressman, J. B., and Maceras, P. (1991) Unusual Solubility Behaviour of Cyclosporin A in Aqueous Media. J. Pharm. Pharmacol. 43, 287-289.
43. Principles of Solution and Solubility (1978) Shinoda, K., Ed.; Marcel Dekker, Inc.
44. Tanford, C. (1997) How Protein Chemists Learned About the Hydrophobic Factor. Protein Sci. 6, 1358-1366.
45. Kauzmann, W. (1959) Some factors in the interpretation of protein denaturation. Adv. Prot. Chem. 14, 1.
46. Kessler, H., Gehrke, M., Lautz, J., Kock, M., Seebach, D., and Thaler, A. (1990) Complexation and Medium Effects on the Conformation of Cyclosporin A Studied by NMR Spectroscopy and Molecular Dynamics Calculations. Biochem. Pharm. 40, 169-173.
47. Englander, S. W., and Kallenbach, N. (1984) Hydrogen Exchange and Structural Dynamics of Proteins and Nucleic Acids. Q. Rev. Biophys. 16, 521-655.
48. Eigen, M. (1964) Proton Transfer, Acid-base Catalysis and Enzymatic Hydrolysis, Part I: Elementary Processes. Angew. Chem., Int. Ed. 3, 1-72.
49. Durschlag, H. (1986) Specific Volumes of Biological Molecules and Some Other Macromolecules of Biological Interest. In Thermodynamic Data for Biochemistry and Biotechnology (Hinz, H.J., Ed.) p 45, Springer-Verlag, New York.
50. Cohn, E. J., and Edsall, J. T. (1943) Density and apparent specific volume of proteins. In Proteins, Amino Acids and Peptides as Ions and Dipolar Ions (Cohn, E. J., and Edsall, J. T., Eds.) p 157, Rheinhold, New York.
51. Gutknecht, J. (1992) Aspirin, acetaminophen and proton transport through phospholipid bilayers and mitochondrial membranes. Mol. Cell. Biochem. 114, 3-8.
52. Wang, C. X., Wan, S. Z., Xiang, Z. X., and Shi, Y. Y. (1997) Incorporating hydration force determined by boundary element method into stochastic dynamics. J. Phys. Chem. B. 101, 230-235.