Recent developments and prospects for influenza M2 ion channel inhibitors that circumvent amantadine resistance

Current Bioinformatics

Volumn 7, Issue 4, 2012, Pages 366-373

  Mitrasinovic, Petar M ^a  

^a Belgrade Institute of Science and Technology   (Serbia)

Author keywords

Amantadine; Influenza A virus; Inhibitor; M2 ion channel; Mutant; Resistance

Indexed keywords

AMINES; ANTIVIRAL AGENTS;

AMANTADINE; INFLUENZA A; INFLUENZA A VIRUS; INHIBITOR; ION CHANNEL; ION-CHANNEL INHIBITORS; M2 CHANNEL; M2 ION CHANNEL; MUTANT; RESISTANCE;

VIRUSES;

2 AMINO ADAMANTANE; 2 ETHYL 2 AMINO ADAMANTANE; 2 METHYL 2 AMINO ADAMANTANE; 2 METHYL 2 FLUORO ADAMANTANE; 2 METHYL 2 HYDROXYL ADAMANTANE; 2 N PROPYL 2 AMINO ADAMANTANE; 2 N PROPYL 2 HYDROXYL ADAMANTANE; ADAMANTANE DERIVATIVE; AIMANTADINE; AMANTADINE; ANTIVIRUS AGENT; ION CHANNEL; M2 ION CHANNEL INHIBITOR; OSELTAMIVIR; PROTEIN M2; RIMANTADINE; SPIRO(PIPERIDINE 2,2' ADAMANTAN); SPIRO(PYRROLIDINE 2,2' ADAMANTANE); UNCLASSIFIED DRUG;

BINDING AFFINITY; DRUG BINDING; DRUG STRUCTURE; FUNGAL STRAIN; GENE MUTATION; HUMAN; INFLUENZA; INFLUENZA VIRUS A; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; VIRUS REPLICATION; X RAY CRYSTALLOGRAPHY;

EID: 84874830894     PISSN: 15748936     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (55)

1. Chizhmakov IV, Geraghty FM, Ogden DC, Hayhurst A, Antoniou M, Hay AJ. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J Physiol 1996; 494(Pt 2): 329-36.
2. Mould JA, Paterson RG, Takeda M, et al. Influenza B virus BM2 protein has ion channel activity that conducts protons across membranes. Dev Cell 2003; 5(1): 175-84.
3. Pinto LH, Lamb RA. The M2 proton channels of influenza A and B viruses. J Biol Chem 2006; 281(14): 8997-9000.
4. Hay AJ. The action of adamantanamines against influenza A viruses: Inhibition of the M2 ion channel protein. Semin Virol 1992; 3: 21-30.
5. Martin K, Helenius A. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 1991; 67(1): 117-30.
6. Pinto LH, Lamb RA. Controlling influenza virus replication by inhibiting its proton channel. Mol Biosyst 2007; 3(1): 18-23.
7. Sugrue RJ, Bahadur G, Zambon MC, Hall-Smith M, Douglas AR, Hay AJ. Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J 1990; 9(11): 3469-76.
8. Steinhauer DA, Wharton SA, Skehel JJ, Wiley DC, Hay AJ. Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: Evidence for virus-specific regulation of the pH of glycoprotein transport vesicles. Proc Natl Acad Sci USA 1991; 88(24): 11525-9.
9. Dolin R, Reichman RC, Madore HP, Maynard R, Linton PN, Webber-Jones J. A controlled trial of amantadine and rimantadine in the prophylaxis of influenza A infection. N Engl J Med 1982; 307(10): 580-4.
10. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH. The molecular basis of the specific anti-influenza action of amantadine. EMBO J 1985; 4(11): 3021-4.
11. Hurt AC, Selleck P, Komadina N, Shaw R, Brown L, Barr IG. Susceptibility of highly pathogenic A (H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res 2007; 73(3): 228-31.
12. Ilyushina NA, Govorkova EA, Webster RG. Detection of amantadine-resistant variants among avian influenza viruses isolated in North America and Asia. Virology 2005; 341(1): 102-6.
13. Bai G-R, Chittaganpitch M, Kanai Y, et al. Amantadine-and oseltamivir-resistant variants of influenza A viruses in Thailand. Biochem Biophys Res Commun 2009; 390(3): 897-901.
14. Krumbholz A, Schmidtke M, Bergmann S, et al. High prevalence of amantadine resistance among circulating European porcine influenza A viruses. J Gen Virol 2009; 90(Pt 4): 900-8.
15. Abed Y, Goyette N, Boivin G. Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob Agents Chemother 2005; 49(2): 556-9.
16. Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell 1992; 69(3): 517-28.
17. Astrahan P, Kass I, Cooper MA, Arkin IT. A novel method of resistance for influenza against a channel-blocking antiviral drug. Proteins 2004; 55(2): 251-7.
18. Zhong, Q, Newns DM, Pattnaik P, Lear JD, Klein ML. Two possible conducting states of the influenza A virus M2 ion channel. FEBS Lett 2000; 473(2): 195-8.
19. Hu J, Fu R, Nishimura K, et al. Histidines, heart of the hydrogen ion channel from influenza A virus: Toward an understanding of conductance and proton selectivity. Proc Natl Acad Sci USA 2006; 103(18): 6865-70.
20. Kass I, Arkin IT. How pH opens a H channel: The gating mechanism of influenza a M2. Structure 2005; 13(12): 1789-98.
21. Chen H, Wu Y, Voth GA. Proton transport behavior through the influenza A M2 channel: Insights from molecular simulation. Biophys J 2007; 93(10): 3470-9.
22. Intharathep P, Laohpongspaisan C, Rungrotmongkol T, et al. How amantadine and rimantadine inhibit proton transport in the M2 protein channel. J Mol Graph Model 2008; 27(3): 342-8.
23. Stouffer AL, Acharya R, Salom D, et al. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 2008; 451(7178): 596-9.
24. Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 2008; 451(7178): 591-5.
25. Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 2010; 463(7281): 689-92.
26. Jing X, Ma C, Ohigashi Y, et al. Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel. Proc Natl Acad Sci USA 2008; 105(31): 10967-72.
27. Ohigashi Y, Ma C, Jing X, Balannick V, Pinto LH, Lamb RA. An amantadine-sensitive chimeric BM2 ion channel of influenza B virus has implications for the mechanism of drug inhibition. Proc Natl Acad Sci USA 2009; 106(44): 18775-9.
28. Stouffer AL, Ma C, Cristian L, et al. The interplay of functional tuning, drug resistance, and thermodynamic stability in the evolution of the M2 proton channel from the influenza A virus. Structure 2008; 16(7): 1067-76.
29. Pielak R, Schnell J, Chou J. Mechanism of drug inhibition and drug resistance of influenza A M2 channel. Proc Natl Acad Sci USA 2009; 106(18): 7379-84.
30. Huang R-B, Du Q-S, Wang C-H, Chou K-C. An in-depth analysis of the biological functional studies based on the NMR M2 channel structure of influenza A virus. Biochem Biophys Res Commun 2008; 377(4): 1243-7.
31. Cady SD, Hong M. Amantadine-induced conformational and dynamical changes of the influenza M2 transmembrane proton channel. Proc Natl Acad Sci USA 2008; 105(5): 1483-8.
32. 31 in amantadine binding. J Mol Biol 2009; 385(4): 1127-41.
33. Luo W, Cady SD, Hong M. Immobilization of the influenza A M2 transmembrane peptide in virus envelope-mimetic lipid membranes: a solid-state NMR investigation. Biochemistry 2009; 48(27): 6361-8.
34. Yi M, Cross TA, Zhou H-X. Conformational heterogeneity of the M2 proton channel and a structural model for channel activation. Proc Natl Acad Sci USA 2009; 106(32): 13311-6.
35. Khurana E, Peraro MD, DeVane R, Vemparala A, DeGrado WF, Klein ML. Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus. Proc Natl Acad Sci USA 2009; 106(4): 1069-74.
36. Ma C, Polishchuk AL, Ohigashi Y, et al. Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel. Proc Natl Acad Sci USA 2009; 106(30): 12283-8.
37. Laohpongspaisan C, Rungrotmongkol T, Intharathep P, et al. Why amantadine loses its function in influenza M2 mutants: MD simulations. J Chem Inf Model 2009; 49(4): 847-52.
38. World Health Organization. Press Release: Swine Influenza Frequently Asked Questions. http://www.scribd.com/doc/14705-127/World-Health-Organization-Swine-Flu-FAQ-April-26-2009 (Accessed January 29, 2011).
39. Mitrasinovic PM, Ed. Global view of the fight against influenza. New York: Nova Science Publishers Inc. 2009.
40. Yen HL, Ilyushina NA, Salomon R, Hoffmann E, Webster RG, Govorkova EA. Neuraminidase inhibitor-resistant recombinant A/Vietnam/1203/04 (H5N1) influenza viruses retain their replication efficiency and pathogenicity in vitro and in vivo. J Virol 2007; 81(22): 12418-26.
41. Wang SQ, Du QS, Huang RB, Zhang DW, Chou KC. Insights from investigating the interaction of oseltamivir (Tamiflu) with neuraminidase of the 2009 H1N1 swine flu virus. Biochem Biophys Res Commun 2009; 386(3): 432-6.
42. Garten RJ, Davis CT, Russell CA, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009; 325(5937): 197-201.
43. Cheung C-L, Rayner JM, Smith GJ, et al. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis 2006; 193(12): 1626-9.
44. Wang J-F, Wei D-Q, Chou K-C. Insights from investigating the interactions of adamantane-based drugs with the M2 proton channel from the H1N1 swine virus. Biochem Biophys Res Commun 2009; 388(2): 413-7.
45. Rungrotmongkol T, Intharathep P, Malaisree M, et al. Susceptibility of antiviral drugs against 2009 influenza A (H1N1) virus. Biochem Biophys Res Commun 2009; 385(3): 390-4.
46. Tataridis D, Fytas G, Kolocouris A, et al. Influence of an additional 2-amino substituent of the 1-aminoethyl pharmacophore group on the potency of rimantadine against influenza virus A. Bioorg Med Chem Lett 2007; 17(3): 692-6.
47. Du Q-S, Huang R-B, Wang S-Q, Chou K-C. Designing inhibitors of M2 proton channel against H1N1 swine influenza virus. PLoS ONE 2010; 5(2): e9388.
48. Kolocouris A. In: Burger's Medicinal Chemistry, Wolff ME, Ed. John Wiley & Sons: New York 1997; 4: pp. 590-1.
49. Kolocouris N, Foscolos GB, Kolocouris A, et al. Synthesis and antiviral activity of some aminoadamantane derivatives. J Med Chem 1994; 37(18): 2896-902.
50. Kolocouris N, Kolocouris A, Foscolos GB, et al. Synthesis and antiviral activity evaluation of some new aminoadamantane derivatives. J Med Chem 1996; 39(17): 3307-18.
51. Kolocouris A, Spearpoint P, Martin SR, et al. Comparisons of the influenza virus A M2 channel binding affinities, anti-influenza virus potencies and NMDA antagonistic activities of 2-alkyl-2-aminoadamantanes and analogues. Bioorg Med Chem Lett 2008; 18(23): 6156-60.
52. Kolocouris A. The effect of spiroadamantane substitution on the conformational preferences of N-Me pyrrolidine and N-Me piperidine: A description based on dynamic NMR spectroscopy and ab initio correlated calculations. Tetrahedron 2009; 65(45): 9428-35.
53. Wang J, Cady SD, Balannik V, Pinto LH, DeGrado WF, Hong M. Discovery of spiro-piperidine inhibitors and their modulation of the dynamics of the M2 proton channel from influenza A virus. J Am Chem Soc 2009; 131(23): 8066-76.
54. Hu W, Zeng S, Li C, Jie Y, Li Z, Chen L. Identification of hits as matrix-2 protein inhibitors through the focused screening of a small primary amine library. J Med Chem 2010; 53(9): 3831-4.
55. Balannik V, Wang J, Ohigashi Y, et al. Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus. Biochemistry 2009; 48(50): 11872-82.