Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus

Biochemistry

Volumn 48, Issue 50, 2009, Pages 11872-11882

  Balannik, Victoria ^a   Wang, Jun ^b   Ohigashi, Yuki ^a   Jing, Xianghong ^a   Magavern, Emma ^b   Lamb, Robert A ^a   DeGrado, William F ^b   Pinto, Lawrence H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; CHANNEL PORE; CHARGED GROUPS; IN-VITRO; INFLUENZA A VIRUS; INHIBITION KINETICS; ION CHANNEL; M2 CHANNEL; N-TERMINALS; NATURALLY OCCURRING; PHARMACOLOGICAL CHARACTERIZATION; PROTON CHANNELS; RESISTANT MUTANTS; RIMANTADINE; SELECTIVITY FILTER; TRANSMEMBRANE POTENTIALS; WILD TYPES;

BINDING ENERGY; BINDING SITES; BIOELECTRIC POTENTIALS; FLUORINE CONTAINING POLYMERS; LEAD COMPOUNDS;

AMINES;

AMANTADINE; BL 1743; IMIDAZOLE; ION CHANNEL; M2 CHANNEL; MUTANT PROTEIN; RIMANTADINE; SPIRO COMPOUND; SPIRO[5.5]UNDECAN 3 AMINE; TRIAZOLE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DRUG BINDING; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG STRUCTURE; IN VITRO STUDY; INFLUENZA VIRUS A; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

AMANTADINE; ANIMALS; ANTIVIRAL AGENTS; BINDING, COMPETITIVE; CELL LINE; DOGS; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, VIRAL; IMIDAZOLES; INFLUENZA A VIRUS; ION CHANNELS; OOCYTES; POINT MUTATION; SPIRO COMPOUNDS; VIRAL MATRIX PROTEINS; XENOPUS;

INFLUENZA A VIRUS;

EID: 72449187005     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9014488     Document Type: Article

References (38)

1. Cox, N. J., and Subbarao, K. (1999) Influenza. Lancet 354, 1277-1282.
2. Lagoja, I. M., and De Clercq, E. (2008) Anti-influenza virus agents: Synthesis and mode of action. Med. Res. Rev. 28, 1-38.
3. Deyde, V. M., Xu, X., Bright, R. A., Shaw, M., Smith, C. B., Zhang, Y., Shu, Y., Gubareva, L. V., Cox, N. J., and Klimov, A. I. (2007) Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis. 196, 249-257.
4. Hay, A. J., Wolstenholme, A. J., Skehel, J. J., and Smith, M. H. (1985) The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4, 3021-3024.
5. Garten, R. J., Davis, C. T., Russell, C. A., Shu, B., Lindstrom, S., Balish, A., Sessions, W. M., Xu, X., Skepner, E., Deyde, V., Okomo-Adhiambo, M., Gubareva, L., Barnes, J., Smith, C. B., Emery, S. L., Hillman, M. J., Rivailler, P., Smagala, J., de Graaf, M., Burke, D. F., Fouchier, R. A., Pappas, C., Alpuche-Aranda, C. M., Lopez-Gatell, H., Olivera, H., Lopez, I., Myers, C. A., Faix, D., Blair, P. J., Yu, C., Keene, K. M., Dotson, P. D., Boxrud, D., Sambol, A. R., Abid, S. H., St George, K., Bannerman, T., Moore, A. L., Stringer, D. J., Blevins, P., Demmler-Harrison, G. J., Ginsberg, M., Kriner, P., Waterman, S., Smole, S., Guevara, H. F., Belongia, E. A., Clark, P. A., Beatrice, S. T., Donis, R., Katz, J., Finelli, L., Bridges, C. B., Shaw, M., Jernigan, D. B., Uyeki, T. M., Smith, D. J., Klimov, A. I., and Cox, N. J. (2009) Antigenic and Genetic Characteristics of Swine-Origin 2009 A(H1N1) Influenza Viruses Circulating in Humans. Science 325, 197-201.
6. Pinto, L. H., and Lamb, R. A. (2007) Controlling influenza virus replication by inhibiting its proton channel. Mol. Biosyst. 3, 18-23.
7. Pinto, L. H., and Lamb, R. A. (2006) The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281, 8997-9000.
8. Hu, J., Fu, R., Nishimura, K., Zhang, L., Zhou, H. X., Busath, D. D., Vijayvergiya, V., and Cross, T. A. (2006) Histidines, heart of the hydrogen ion channel from influenza A virus: Toward an understanding of conductance and proton selectivity. Proc. Natl. Acad. Sci. U.S.A. 103, 6865-6870.
9. Tu, Q., Pinto, L. H., Luo, G., Shaughnessy, M. A., Mullaney, D., Kurtz, S., Krystal, M., and Lamb, R. A. (1996) Characterization of inhibition of M2 ion channel activity by BL-1743, an inhibitor of influenza A virus. J. Virol. 70, 4246-4252. (Pubitemid 26191137)
10. Wang, J., Cady, S. D., Balannik, V., Pinto, L. H., DeGrado, W. F., and Hong, M. (2009) Discovery of spiro-piperidine inhibitors and their modulation of the dynamics of the M2 proton channel from influenza A virus. J. Am. Chem. Soc. 131, 8066-8076.
11. Bright, R. A., Shay, D. K., Shu, B., Cox, N. J., and Klimov, A. I. (2006) Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA, J. Am. Med. Assoc. 295, 891-894. (Pubitemid 43295823)
12. Cady, S. D., Mishanina, T. V., and Hong, M. (2009) Structure of amantadine-bound M2 transmembrane peptide of influenza A in lipid bilayers from magic-angle-spinning solid-state NMR: The role of Ser31 in amantadine binding. J. Mol. Biol. 385, 1127-1141.
13. Furuse, Y., Suzuki, A., and Oshitani, H. (2009) Large-Scale Sequence Analysis of M Gene of Influenza A Viruses from Different Species: Mechanisms for Emergence and Spread of Amantadine Resistance. Antimicrob. Agents Chemother. 53, 4457-4463.
14. Duff, K. C., Gilchrist, P. J., Saxena, A. M., and Bradshaw, J. P. (1994) Neutron diffraction reveals the site of amantadine blockade in the influenza A M2 ion channel. Virology 202, 287-293.
15. Stouffer, A. L., Acharya, R., Salom, D., Levine, A. S., Di Costanzo, L., Soto, C. S., Tereshko, V., Nanda, V., Stayrook, S., and DeGrado, W. F. (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451, 596-599. (Pubitemid 351186271)
16. Yi, M., Cross, T. A., and Zhou, H. X. (2008) A secondary gate as a mechanism for inhibition of the M2 proton channel by amantadine. J. Phys. Chem. B 112, 7977-7979.
17. Chen, H., Wu, Y., and Voth, G. A. (2007) Proton transport behavior through the influenza AM2 channel: Insights from molecular simulation. Biophys. J. 93, 3470-3479. (Pubitemid 350190810)
18. Khurana, E., Dal Peraro, M., DeVane, R., Vemparala, S., DeGrado, W. F., and Klein, M. L. (2009) Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus. Proc. Natl. Acad. Sci. U.S.A. 106, 1069-1074.
19. Bright, R. A., Medina, M. J., Xu, X., Perez-Oronoz, G., Wallis, T. R., Davis, X. M., Povinelli, L., Cox, N. J., and Klimov, A. I. (2005) Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: A cause for concern. Lancet 366, 1175-1181. (Pubitemid 41393595)
20. Saito, R., Sakai, T., Sato, I., Sano, Y., Oshitani, H., Sato, M., and Suzuki, H. (2003) Frequency of amantadine-resistant influenza A viruses during two seasons featuring cocirculation of H1N1 and H3N2. J. Clin. Microbiol. 41, 2164-2165.
21. Schnell, J. R., and Chou, J. J. (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451, 591-595. (Pubitemid 351186272)
22. Pielak, R. M., Schnell, J. R., and Chou, J. J. (2009) Mechanism of drug inhibition and drug resistance of influenza AM2 channel. Proc. Natl. Acad. Sci. U.S.A. 106, 7379-7384.
23. Jing, X., Ma, C., Ohigashi, Y., Oliveira, F. A., Jardetzky, T. S., Pinto, L. H., and Lamb, R. A. (2008) Functional studies indicate amantadine binds to the pore of the influenza A virus M2 protonselective ion channel. Proc. Natl. Acad. Sci. U.S.A. 105, 10967-10972.
24. Gandhi, C. S., Shuck, K., Lear, J. D., Dieckmann, G. R., DeGrado, W. F., Lamb, R. A., and Pinto, L. H. (1999) Cu(II) inhibition of the proton translocation machinery of the influenza A virus M2 protein. J. Biol. Chem. 274, 5474-5482.
25. Wang, C., Takeuchi, K., Pinto, L. H., and Lamb, R. A. (1993) Ion channel activity of influenza A virus M2 protein: Characterization of the amantadine block. J. Virol. 67, 5585-5594. (Pubitemid 23241395)
26. Flaugh, M. E., Crowell, T. A., and Farlow, D. S. (1980) Acidcatalyzed annelation of α-alkylaldehydes and α,β-unsaturated ketones. A one-pot synthesis of 4,4-dimethyl-2-cyclohexen-1-one. J. Org. Chem. 45, 5399-5400.
27. Chan, Y., and Epstein, W. W. (1988) 4,4-Dimethyl-2-cyclohexen-1- one. Org. Synth. 50, 496-498.
28. Turner, R. M., Lindell, S. D., and Lay, S. V. (1991) A Facile Route to Imidazol-4-yl Anions and Their Reaction with Carbonyl Compounds. J. Org. Chem. 56, 5739-5740.
29. Balannik, V., Lamb, R. A., and Pinto, L. H. (2008) The oligomeric state of the active BM2 ion channel protein of influenza B virus. J. Biol. Chem. 283, 4895-4904.
30. Shimbo, K., Brassard, D. L., Lamb, R. A., and Pinto, L. H. (1996) Ion selectivity and activation of the M2 ion channel of influenza virus. Biophys. J. 70, 1335-1346. (Pubitemid 26073046)
31. Takeda, M., Pekosz, A., Shuck, K., Pinto, L. H., and Lamb, R. A. (2002) Influenza a virus M2 ion channel activity is essential for efficient replication in tissue culture. J. Virol. 76, 1391-1399. (Pubitemid 34070633)
32. Li, D., Saito, R., Suzuki, Y., Sato, I., Zaraket, H., Dapat, C., Caperig- Dapat, I. M., and Suzuki, H. (2009) In vivo and in vitro alterations in influenza A/H3N2 virus M2 and hemagglutinin genes: Effect of passage in MDCK-SIAT1 cells and conventional MDCK cells. J. Clin. Microbiol. 47, 466-468.
33. Stouffer, A. L., Nanda, V., Lear, J. D., and DeGrado, W. F. (2005) Sequence determinants of a transmembrane proton channel: An inverse relationship between stability and function. J. Mol. Biol. 347, 169-179.
34. Stouffer, A. L., Ma, C., Cristian, L., Ohigashi, Y., Lamb, R. A., Lear, J. D., Pinto, L. H., and DeGrado, W. F. (2008) The interplay of functional tuning, drug resistance, and thermodynamic stability in the evolution of the M2 proton channel from the influenza A virus. Structure 16, 1067-1076. (Pubitemid 351899295)
35. Pinto, L. H., Dieckmann, G. R., Gandhi, C. S., Papworth, C. G., Braman, J., Shaughnessy, M. A., Lear, J. D., Lamb, R. A., and DeGrado, W. F. (1997) A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. U.S.A. 94, 11301-11306.
36. Hu, J., Asbury, T., Achuthan, S., Li, C., Bertram, R., Quine, J. R., Fu, R., and Cross, T. A. (2007) Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92, 4335-4343. (Pubitemid 46915327)
37. Tang, Y., Venkataraman, P., Knopman, J., Lamb, R. A., and Pinto, L. H. (2005) The M2 proteins of Influenza A and B viruses are single-pass proton channels. In Viral Membrane Proteins: Structure, Function and Drug Design (Fischer, W. B., Ed.) pp 101-111, Kluwer Academic/Plenum Publishers, New York.
38. Li, C., Yi, M., Hu, J., Zhou, H. X., and Cross, T. A. (2008) Solid-state NMR and MD simulations of the antiviral drug amantadine solubilized in DMPC bilayers. Biophys. J. 94, 1295-1302.