Solid-state NMR and MD simulations of the antiviral drug amantadine solubilized in DMPC bilayers

Biophysical Journal

Volumn 94, Issue 4, 2008, Pages 1295-1302

  Li, Conggang ^a,b   Yi, Myunggi ^a,c   Hu, Jun ^a,b   Zhou, Huan Xiang ^a,c   Cross, Timothy A ^a,b,c  

^a Department of Chemistry and Biochemistry ^*  (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; ANTIVIRUS AGENT; DIMYRISTOYLPHOSPHATIDYLCHOLINE;

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE FLUIDITY; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POROSITY; SOLUBILITY;

AMANTADINE; ANTIVIRAL AGENTS; COMPUTER SIMULATION; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HYDROPHOBICITY; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; POROSITY; SOLUBILITY;

EID: 38949181061     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.112482     Document Type: Article

References (49)

1. Rhodes, D. G., J. G. Sarmiento, and L. G. Herbette. 1985. Kinetics of binding of membrane-active drugs to receptor sites. Diffusion-limited rates for a membrane bilayer approach of 1,4-dihydropyridine calcium channel antagonists to their active site. Mol. Pharmacol. 27:612-623.
2. Pawlikowska-Pawlega, B., W. I. Gruszecki, L. E. Misiak, and A. Gawron. 2003. The study of the quercetin action on human erythrocyte membranes. Biochem. Pharmacol. 66:605-612.
3. Makriyannis, A., X. Tian, and J. Guo. 2005. How lipophilic cannabinergic ligands reach their receptor sites. Prostaglandins Other Lipid Mediat. 77:210-218.
4. Zhou, H. X., and A. Szabo. 2004. Enhancement of association rates by nonspecific binding to DNA and cell membranes. Phys. Rev. Lett. 93:178101.
5. Holsinger, L. J., and R. A. Lamb. 1991. Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology. 183:32-43.
6. Takeda, M., A. Pekosz, K. Shuck, L. H. Pinto, and R. A. Lamb. 2002. Influenza A virus M2 ion channel activity is essential for efficient replication in tissue culture. J. Virol. 76:1391-1399.
7. Pinto, L. H., L. J. Holsinger, and R. A. Lamb. 1992. Influenza virus M2 protein has ion channel activity. Cell. 69:517-528.
8. Chizhmakov, I. V., F. M. Geraghty, D. C. Ogden, A. Hayhurst, M. Antoniou, and A. J. Hay. 1996. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. 494:329-336.
9. Vijayvergiya, V., R. Wilson, A. Chorak, P. F. Gao, T. A. Cross, and D. D. Busath. 2004. Proton conductance of influenza virus M2 protein in planar lipid bilayers. Biophys. J. 87:1697-1704.
10. Wang, C., K. Takeuchi, L. H. Pinto, and R. A. Lamb. 1993. Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J. Virol. 67:5585-5594.
11. Skehel, J. J. 1992. Influenza virus. Amantadine blocks the channel. Nature. 358:110-111.
12. Duff, K. C., and R. H. Ashley. 1992. The transmembrane domain of influenza-A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology. 190:485-489.
13. Hu,J.,R.Fu,K.Nishimura,L.Zhang,H.X.Zhou,D.D.Busath,V. Vijayvergiya, and T. A. Cross. 2006. Histidines, heart of the hydrogen ion channel from influenza A virus: toward an understanding of conductance and proton selectivity. Proc. Natl. Acad. Sci. USA. 103:6865-6870.
14. Hu, J., T. M. Asbury, S. Achuthan, C. Li, R. Bertram, J. R. Quine, R. Fu, and T. A. Cross. 2007. Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92:4335-4343.
15. Fieschi, C., M. Nardini, M. Casacchia, and M. E. Tedone. 1970. Amantadine for Parkinson's disease. Lancet. 1:945-946.
16. Blanchet, P. J., L. V. Metman, and T. N. Chase. 2003. Renaissance of amantadine in the treatment of Parkinson's disease. Adv. Neurol. 91: 251-257.
17. Duff, K. C., A. J. Cudmore, and J. P. Bradshaw. 1993. The location of amantadine hydrochloride and free base within phospholipid multilayersa neutron and x-ray-diffraction study. Biochim. Biophys. Acta. 1145:149-156.
18. Wang, J. F., J. R. Schnell, and J. J. Chou. 2004. Amantadine partition and localization in phospholipid membrane: a solution NMR study. Biochem. Biophys. Res. Commun. 324:212-217.
19. Subczynski, W. K., J. Wojas, V. Pezeshk, and A. Pezeshk. 1998. Partitioning and localization of spin-labeled amantadine in lipid bilayers: An EPR study. J. Pharm. Sci. 87:1249-1254.
20. Stetter, H., J. Mayer, M. Schwarz, and K. Wulff. 1960. Uber Verbindungen Mit Urotropin-Struktur. 16. Beitrage Zur Chemie Der Adamantyl-(1)-Derivate. Chemische Berichte-Recueil. 93:226-230.
21. Davis, J. H., K. R. Jeffrey, M. Bloom, M. I. Valic, and T. P. Higgs. 1976. Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42:390-394.
22. Case, D. A., T. A. Darden, T. E. I. Cheatham, C. L. Simmerling, J. Wang, R. E. Duke, R. Luo, K. M. Merz, B. Wang, D. A. Pearlman, M. Crowley, S. Brozell, V. Tsui, H. Gohlke, J. Mogan, V. Hornak, G. Cui, P. Beroza, C. Schafmeister, J. W. Caldwell, W. S. Ross, and P. A. Kollman. 2004. AMBER 8. University of California, San Francisco.
23. Feller, S. E., and A. D. MacKerell. 2000. An improved empirical potential energy function for molecular simulations of phospholipids. J. Phys. Chem. B. 104:7510-7515.
24. Frisch, M. J. T. G. W., H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, J. Montgomery, J. A.; T. Vreven, K. N. Kudin, J. C. Burant, J. M. Millam, S. S. Iyengar, J. Tomasi, V. Barone, B. Mennucci, M. Cossi, G. Scalmani, N. Rega, G. A. Petersson, H. Nakatsuji, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, M. Klene, X. Li, J. E. Knox, H. P. Hratchian, J. B. Cross, V. Bakken,C.Adamo,J. Jaramillo,R.Gomperts,R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, P. Y. Ayala, K. Morokuma, G. A. Voth, P. Salvador, J. J. Dannenberg, V. G. Zakrzewski, S. Dapprich, A. D. Daniels, M. C. Strain, O. Farkas, D. K. Malick, A. D. Rabuck, K. Raghavachari, J. B. Foresman,J. V.Ortiz,Q.Cui,A.G.Baboul,S. Clifford,J.Cioslowski, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. L. Martin,D.J.Fox,T. Keith,M. A. Al-Laham, C. Y. Peng, A. Nanayakkara, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, C. Gonzalez, and J. A. and Pople. 2004. Gaussian 03, Revision C.02. Gaussian, Wallingford, CT.
25. Wang, J. M., P. Cieplak, and P. A. Kollman. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21:1049-1074.
26. Wang, J. M., R. M. Wolf, J. W. Caldwell, P. A. Kollman, and D. A. Case. 2004. Development and testing of a general amber force field. J. Comput. Chem. 25:1157-1174.
27. Berendsen, H. J. C., J. P. M. Postma, W. F. Vangunsteren, A. Dinola, and J. R. Haak. 1984. Molecular-Dynamics with Coupling to an External Bath. J. Chem. Phys. 81:3684-3690.
28. Darden, T., D. York, and L. Pedersen. 1993. Particle Mesh Ewald - an N.Log(N) Method for Ewald Sums in Large Systems. J. Chem. Phys. 98:10089-10092.
29. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A Smooth Particle Mesh Ewald Method. J. Chem. Phys. 103:8577-8593.
30. Toukmaji, A., C. Sagui, J. Board, and T. Darden. 2000. Efficient particle-mesh Ewald based approach to fixed and induced dipolar interactions. J. Chem. Phys. 113:10913-10927.
31. Miyamoto, S., and P. A. Kollman. 1992. Settle - an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models. J. Comput. Chem. 13:952-962.
32. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical-integration of Cartesian equations of motion of a system with constraints-molecular-dynamics of N-alkanes. J. Comput. Phys. 23: 327-341.
33. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 79:926-935.
34. Bastug, T., and S. Kuyucak. 2005. Test of molecular dynamics force fields in gramicidin A. Eur. Biophys. J. 34:377-382.
35. Lindstrom, F., P. T. Williamson, and G. Grobner. 2005. Molecular insight into the electrostatic membrane surface potential by 14n/31p MAS NMR spectroscopy: nociceptin-lipid association. J. Am. Chem. Soc. 127:6610-6616.
36. Santos, J. S., D. K. Lee, and A. Ramamoorthy. 2004. Effects of anti-depressants on the conformation of phospholipid headgroups studied by solid-state NMR. Magn. Reson. Chem. 42:105-114.
37. Rothgeb, T. M., and E. Oldfield. 1981. Nitrogen-14 nuclear magnetic resonance spectroscopy as a probe of lipid bilayer headgroup structure. J. Biol. Chem. 256:6004-6009.
38. 2+. Biophys. J. 85:2363-2373.
39. 2+ ion. Biophys. J. 81:425-434.
40. 13C hetero-nuclear chemical shift correlation spectroscopy of lipid bilayers. Biophys. J. 55:355-358.
41. Petrache, H. I., S. Tristram-Nagle, and J. F. Nagle. 1998. Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids. 95:83-94.
42. Koenig, B. W., H. H. Strey, and K. Gawrisch. 1997. Membrane lateral compressibility determined by NMR and x-ray diffraction: Effect of acyl chain polyunsaturation. Biophys. J. 73:1954-1966.
43. Pasenkiewicz-Gierula, M., Y. Takaoka, H. Miyagawa, K. Kitamura, and A. Kusumi. 1999. Charge pairing of headgroups in phosphatidyl- choline membranes: A molecular dynamics simulation study. Biophys. J. 76:1228-1240.
44. Hu, W., K. C. Lee, and T. A. Cross. 1993. Tryptophans in membrane proteins: indole ring orientations and functional implications in the gramicidin channel. Biochemistry. 32:7035-7047.
45. Gaede, H. C., W. M. Yau, and K. Gawrisch. 2005. Electrostatic contributions to indole-lipid interactions. J. Phys. Chem. B. 109:13014-13023.
46. Spector, R. 1988. Transport of amantadine and rimantadine through the blood-brain barrier. J. Pharmacol. Exp. Ther. 244:516-519.
47. Cabral, D. J., J. A. Hamilton, and D. M. Small. 1986. The ionization behavior of bile acids in different aqueous environments. J. Lipid Res. 27:334-343.
48. Urry, D. W., S. Q. Peng, and T. M. Parker. 1992. Hydrophobicity- induced pK shifts in elastin protein-based polymers. Biopolymers. 32:373-379.
49. Epand, R. M., R. F. Epand, and R. C. McKenzie. 1987. Effects of viral chemotherapeutic agents on membrane properties. Studies of cyclo-sporin A, benzyloxycarbonyl-D-Phe-L-Phe-Gly and amantadine. J. Biol. Chem. 262:1526-1529.