New strategy for high throughput screening of anti-influenza virus M2 ion channel inhibitors

Current Pharmaceutical Design

Volumn 19, Issue 28, 2013, Pages 5146-5155

  Li, Chufang ^a   Long, Yan ^b   Lin, Zuoxian ^b   Jie, Yanling ^b   Xiao, Yajuan ^b   Yang, Lingzhi ^b,c   Sun, Juanjuan ^b   Ren, Yizhong ^b,c   Chen, Ling ^a,b,c   Li, Zhiyuan ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

EGFP; High throughput assay; Influenza; M2 ion channel; Virus

Indexed keywords

3 ISOPINOCAMPHEYLAMINE; AMANTADINE; GREEN FLUORESCENT PROTEIN; M2 ION CHANNEL INHIBITOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN M2;

ARTICLE; AVIAN INFLUENZA; CONTROLLED STUDY; DRUG STRUCTURE; HIGH THROUGHPUT SCREENING; NONHUMAN; PATCH CLAMP; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SWINE INFLUENZA;

AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; AZABICYCLO COMPOUNDS; DRUG DISCOVERY; DRUG RESISTANCE, VIRAL; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; MEMBRANE POTENTIALS; MEMBRANE TRANSPORT MODULATORS; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PATCH-CLAMP TECHNIQUES; RECOMBINANT PROTEINS; VIRAL MATRIX PROTEINS;

EID: 84881357494     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990001     Document Type: Article

References (43)

1. Yuen KY, Wong SS. Human infection by avian influenza A H5N1. Hong Kong Med J 2005; 11: 189-99.
2. Guan Y, Poon LL, Cheung CY, et al. H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci USA 2004; 101: 8156-61.
3. Butler D. Swine flu goes global. Nature 2009; 458: 1082-3.
4. Michaelis M, Doerr HW, Cinatl J, Jr. Novel swine-origin influenza A virus in humans: another pandemic knocking at the door. Med Microbiol Immunol 2009; 198: 175-83.
5. de Jong MD, Tran TT, Truong HK, et al. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J Med 2005; 353: 2667-72.
6. Suzuki Y, Taira K, Saito R, et al. Epidemiologic study of influenza infection in Okinawa, Japan, from 2001 to 2007: changing patterns of seasonality and prevalence of amantadine-resistant influenza A virus. J Clin Microbiol 2009; 47: 623-9.
7. Tamura D, Mitamura K, Yamazaki M, et al. Oseltamivir-resistant influenza a viruses circulating in Japan. J Clin Microbiol 2009; 47: 1424-7.
8. Bright RA, Shay DK, Shu B, Cox NJ, Klimov AI. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 2006; 295: 891-4.
9. Deyde VM, Xu X, Bright RA, et al. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J Infect Dis 2007; 196: 249-57.
10. He G, Qiao J, Dong C, He C, Zhao L, Tian Y. Amantadineresistance among H5N1 avian influenza viruses isolated in Northern China. Antiviral Res 2008; 77: 72-6.
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: 228-31.
12. Weinstock DM, Gubareva LV, Zuccotti G. Prolonged shedding of multidrug-resistant influenza A virus in an immunocompromised patient. N Engl J Med 2003; 348: 867-8.
13. Pinto LH, Lamb RA. The M2 proton channels of influenza A and B viruses. J Biol Chem 2006; 281: 8997-9000.
14. Bright RA, Medina MJ, Xu X, et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 2005; 366: 1175-81.
15. De Clercq E. Antiviral agents active against influenza A viruses. Nat Rev Drug Discov 2006; 5: 1015-25.
16. Vijayvergiya V, Wilson R, Chorak A, Gao PF, Cross TA, Busath DD. Proton conductance of influenza virus M2 protein in planar lipid bilayers. Biophys J 2004; 87: 1697-704.
17. Rungrotmongkol T, Intharathep P, Malaisree M, et al. Susceptibility of antiviral drugs against 2009 influenza A (H1N1) virus. Biochem Biophys Res Commun 2009; 385: 390-4.
18. Beigel J, Bray M. Current and future antiviral therapy of severe seasonal and avian influenza. Antiviral Res 2008; 78: 91-102.
19. Pinto LH, Dieckmann GR, Gandhi CS, et al. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc Natl Acad Sci USA 1997; 94: 11301-6.
20. Witter R, Nozirov F, Sternberg U, Cross TA, Ulrich AS, Fu R. Solid-state 19F NMR spectroscopy reveals that Trp41 participates in the gating mechanism of the M2 proton channel of influenza A virus. J Am Chem Soc 2008; 130: 918-24.
21. Mao L, Wang J, DeGrado WF, Inouye M. An assay suitable for high throughput screening of anti-influenza drugs. PLoS One 2013; 8: e54070.
22. Kurtz S, Luo G, Hahnenberger KM, et al. Growth impairment resulting from expression of influenza virus M2 protein in Saccharomyces cerevisiae: identification of a novel inhibitor of influenza virus. Antimicrob Agents Chemother 1995; 39: 2204-9.
23. Black RA, Rota PA, Gorodkova N, Klenk HD, Kendal AP. Antibody response to the M2 protein of influenza A virus expressed in insect cells. J Gen Virol 1993; 74 (Pt 1): 143-6.
24. Mould JA, Drury JE, Frings SM, et al. Permeation and activation of the M2 ion channel of influenza A virus. J Biol Chem 2000; 275: 31038-50.
25. Ilyinskii PO, Gabai VL, Sunyaev SR, Thoidis G, Shneider AM. Toxicity of influenza A virus matrix protein 2 for mammalian cells is associated with its intrinsic proton-channeling activity. Cell Cycle 2007; 6: 2043-7.
26. Xu J, Wang X, Ensign B, Li M, Wu L, Guia A. Ion-channel assay technologies: quo vadis? Drug Discov Today 2001; 6: 1278-1287.
27. Lippincott-Schwartz J, Patterson GH. Development and use of fluorescent protein markers in living cells. Science 2003; 300: 87-91.
28. Plautz JD, Day RN, Dailey GM, et al. Green fluorescent protein and its derivatives as versatile markers for gene expression in living Drosophila melanogaster, plant and mammalian cells. Gene 1996; 173: 83-7.
29. Hanson GT, McAnaney TB, Park ES, et al. Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminary application. Biochemistry 2002; 41: 15477-88.
30. Kneen M, Farinas J, Li Y, Verkman AS. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys J 1998; 74: 1591-9.
31. Nehrke K. Intracellular pH measurements in vivo using green fluorescent protein variants. Methods Mol Biol 2006; 351: 223-39.
32. 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: 6865-70.
33. Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell 1992; 69: 517-28.
34. Stewart SM, Pekosz A. The influenza C virus CM2 protein can alter intracellular pH, and its transmembrane domain can substitute for that of the influenza A virus M2 protein and support infectious virus production. J Virol 2012; 86: 1277-81.
35. Sun J, Li C, Xu W, Li Z, Liu J, Chen L. [Establish stable cell line to express M2 ion channel of influenza A virus H5N1]. Sheng Wu Gong Cheng Xue Bao 2008; 24: 1902-6.
36. Li Z, Migita K, Samways DS, Voigt MM, Egan TM. Gain and loss of channel function by alanine substitutions in the transmembrane segments of the rat ATP-gated P2X2 receptor. J Neurosci 2004; 24: 7378-86.
37. Bizzarri R, Arcangeli C, Arosio D, et al. Development of a novel GFP-based ratiometric excitation and emission pH indicator for intracellular studies. Biophys J 2006; 90: 3300-14.
38. Zhang JH, Chung TD, Oldenburg KR. A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 1999; 4: 67-73.
39. 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: 3831-4.
40. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 2002; 20: 87-90.
41. Franck P, Petitipain N, Cherlet M, et al. Measurement of intracellular pH in cultured cells by flow cytometry with BCECFAM. J Biotechnol 1996; 46: 187-95.
42. Patterson G, Day RN, Piston D. Fluorescent protein spectra. J Cell Sci 2001; 114: 837-8.
43. Ozkan P, Mutharasan R. A rapid method for measuring intracellular pH using BCECF-AM. Biochim Biophys Acta 2002; 1572: 143-8.