Detection of proton movement directly across viral membranes to identify novel influenza virus M2 inhibitors

Journal of Virology

Volumn 87, Issue 19, 2013, Pages 10679-10686

  Sulli, Chidananda ^a   Banik, Soma S R ^a   Schilling, Justin ^a   Moser, Allan ^a   Xiang, Xiaoxiao ^a   Payne, Riley ^a   Wanless, Antony ^a   Willis, Sharon H ^a   Paes, Cheryl ^a   Rucker, Joseph B ^a   Doranz, Benjamin J ^a  

^a Integral Molecular Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; ION CHANNEL; PROTEIN INHIBITOR; PROTEIN M2; PROTEIN M2 INHIBITOR; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG DISTRIBUTION; DRUG IDENTIFICATION; DRUG SPECIFICITY; HIGH THROUGHPUT SCREENING; INFLUENZA VIRUS; ION PERMEABILITY; LIPID BILAYER; MEMBRANE CONDUCTANCE; MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; PROTON TRANSPORT; TOXICITY TESTING; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS LIKE AGENT;

ANTIVIRAL AGENTS; APOPTOSIS; CELL MEMBRANE; HEK293 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS; INFLUENZA, HUMAN; ION CHANNELS; LIPID BILAYERS; PROTONS; SMALL MOLECULE LIBRARIES; VIRAL MATRIX PROTEINS; VIRION;

EID: 84886031052     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01190-13     Document Type: Article

References (46)

1. Pinto LH, Lamb RA. 2006. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281:8997-9000.
2. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.
3. Helenius A. 1992. Unpacking the incoming influenza virus. Cell 69:577-578.
4. Martin K, Helenius A. 1991. Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol. 65:232-244.
5. Iwatsuki-Horimoto K, Horimoto T, Noda T, Kiso M, Maeda J, Watanabe S, Muramoto Y, Fujii K, Kawaoka Y. 2006. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J. Virol. 80:5233-5240.
6. McCown MF, Pekosz A. 2005. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J. Virol. 79:3595-3605.
7. Sakaguchi T, Leser GP, Lamb RA. 1996. The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J. Cell Biol. 133:733-747.
8. Davies WL, Grunert RR, Haff RF, McGahen JW, Neumayer EM, Paulshock M, Watts JC, Wood TR, Hermann EC, Hoffmann CE. 1964. Antiviral activity of 1-adamantanamine (amantadine). Science 144:862-863.
9. Govorkova EA, Baranovich T, Seiler P, Armstrong J, Burnham A, Guan Y, Peiris M, Webby RJ, Webster RG. 2013. Antiviral resistance among highly pathogenic influenza A (H5N1) viruses isolated worldwide in 2002-2012 shows need for continued monitoring. Antiviral Res. 98:297-304.
10. Trampuz A, Prabhu RM, Smith TF, Baddour LM. 2004. Avian influenza: a new pandemic threat?. Mayo Clin. Proc. 79:523-530.
11. Ilyinskii PO, Gabai VL, Sunyaev SR, Thoidis G, Shneider AM. 2007. Toxicity of influenza A virus matrix protein 2 for mammalian cells is associated with its intrinsic proton-channeling activity. Cell Cycle 6:2043-2047.
12. Moffat JC, Vijayvergiya V, Gao PF, Cross TA, Woodbury DJ, Busath DD. 2008. Proton transport through influenza A virus M2 protein reconstituted in vesicles. Biophys. J. 94:434-445.
13. Zheng W, Spencer RH, Kiss L. 2004. High throughput assay technologies for ion channel drug discovery. Assay Drug Dev. Technol. 2:543-552.
14. Hoffman TL, Canziani G, Jia L, Rucker J, Doms RW. 2000. A biosensor assay for studying ligand-membrane receptor interactions: binding of antibodies and HIV-1 Env to chemokine receptors. Proc. Natl. Acad. Sci. U.S.A. 97:11215-11220.
15. Willis S, Davidoff C, Schilling J, Wanless A, Doranz BJ, Rucker J. 2008. Virus-like particles as quantitative probes of membrane protein interactions. Biochemistry 47:6988-6990.
16. Mattia K, Puffer BA, Williams KL, Gonzalez R, Murray M, Sluzas E, Pagano D, Ajith S, Bower M, Berdougo E, Harris E, Doranz BJ. 2011. Dengue reporter virus particles for measuring neutralizing antibodies against each of the four dengue serotypes. PLoS One 6:e27252. doi:10.1371 /journal.pone.0027252.
17. Balliet JW, Bates P. 1998. Efficient infection mediated by viral receptors incorporated into retroviral particles. J. Virol. 72:671-676.
18. Endres MJ, Jaffer S, Haggarty B, Turner JD, Doranz BJ, O'Brien PJ, Kolson DL, Hoxie JA. 1997. Targeting of HIV-and SIV-infected cells by CD4-chemokine receptor pseudotypes. Science 278:1462-1464.
19. Davidoff C, Payne RJ, Willis SH, Doranz BJ, Rucker JB. 2012. Maturation of the Gag core decreases the stability of retroviral lipid membranes. Virology 433:401-409.
20. Baxter DF, Kirk M, Garcia AF, Raimondi A, Holmqvist MH, Flint KK, Bojanic D, Distefano PS, Curtis R, Xie Y. 2002. A novel membrane potential-sensitive fluorescent dye improves cell-based assays for ion channels. J. Biomol. Screen. 7:79-85.
21. Benz R, McLaughlin S. 1983. The molecular mechanism of action of the proton ionophore FCCP (carbonylcyanide p-trifluoromethoxyphenylhydrazone). Biophys. J. 41:381-398.
22. Rossman JS, Jing X, Leser GP, Lamb RA. 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902-913.
23. Nguyen DH, Liao Z, Buckley JT, Hildreth JE. 1999. The channelforming toxin aerolysin neutralizes human immunodeficiency virus type 1. Mol. Microbiol. 33:659-666.
24. Frolov VA, Dunina-Barkovskaya AY, Samsonov AV, Zimmerberg J. 2003. Membrane permeability changes at early stages of influenza hemagglutinin-mediated fusion. Biophys. J. 85:1725-1733.
25. Markosyan RM, Cohen FS. 2010. Negative potentials across biological membranes promote fusion by class II and class III viral proteins. Mol. Biol. Cell 21:2001-2012.
26. Schmidtke M, Schnittler U, Jahn B, Dahse H, Stelzner A. 2001. A rapid assay for evaluation of antiviral activity against coxsackie virus B3, influenza virus A, and herpes simplex virus type 1. J. Virol. Methods 95:133-143.
27. Takeda M, Pekosz A, Shuck K, Pinto LH, Lamb RA. 2002. Influenza A virus M2 ion channel activity is essential for efficient replication in tissue culture. J. Virol. 76:1391-1399.
28. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH. 1985. The molecular basis of the specific anti-influenza action of amantadine.EMBOJ. 7:3021-3024.
29. Hu W, Zeng S, Li C, Li C, Jei Y, Li Z, Chen L. 2010. Identification of hits as matrix-2 protein inhibitors through the focused screening of a small primary amine library. J. Med. Chem. 53:3831-3834.
30. Balannik V, Wang J, Ohigashi Y, Jing X, Magavern E, Lamb RA, Degrado WF, Pinto LH. 2009. Design and pharmacological characterization of inhibitors of amantadine-resistant mutants of the M2 ion channel of influenza A virus. Biochemistry 48:11872-11882.
31. Duque MD, Ma C, Torres E, Wang J, Naesens L, Juárez-Jiménez J, Camps P, Luque FJ, DeGrado WF, Lamb RA, Pinto LH, Vázquez S. 2011. Exploring the size limit of templates for inhibitors of the M2 ion channel of influenza A virus. J. Med. Chem. 54:2646-2657.
32. Wang J, Ma C, Balannik V, Pinto LH, Lamb RA, DeGrado WF. 2011. Exploring the requirements for the hydrophobic scaffold and polar amine in inhibitors of M2 from influenza A virus. ACS Med. Chem. Lett. 2:307-312.
33. Wang J, Ma C, Fiorin G, Carnevale V, Wang T, Hu F, Lamb RA, Pinto LH, Hong M, Klein ML, DeGrado WF. 2011. Molecular dynamics simulation directed rational design of inhibitors targeting drug-resistant mutants of influenza A virus M2. J. Am. Chem. Soc. 133:12834-12841.
34. Zhao X, Li C, Zeng S, Hu W. 2011. Discovery of highly potent agents against influenza A virus. Eur. J. Med. Chem. 46:52-57.
35. Wang J, Ma C, Wang J, Jo H, Canturk B, Fiorin G, Pinto LH, Lamb RA, Klein ML, DeGrado WF. 2013. Discovery of novel dual inhibitors of the wild-type and the most prevalent drug-resistant mutant, S31N, of the M2 proton channel from influenza A virus. J. Med. Chem. 56:2804-2812.
36. Wang J, Wu Y, Ma C, Fiorin G, Wang J, Pinto LH, Lamb RA, Klein ML, Degrado WF. 2013. Structure and inhibition of the drug-resistant S31N mutant of the M2 ion channel of influenza A virus. Proc. Natl. Acad. Sci. U.S.A. 110:1315-1320.
37. Vigant F, Lee J, Hollmann A, Tanner LB, Akyol Ataman Z, Yun T, Shui G, Aguilar HC, Zhang D, Meriwether D, Roman-Sosa G, Robinson LR, Juelich TL, Buczkowski H, Chou S, Castanho MA, Wolf MC, Smith JK, Banyard A, Kielian M, Reddy S, Wenk MR, Selke M, Santos NC, Freiberg AN, Jung ME, Lee B. 2013. A mechanistic paradigm for broadspectrum antivirals that target virus-cell fusion. PLoS Pathog. 9:e1003297. doi:10.1371/journal.ppat.1003297.
38. Wolf MC, Freiberg AN, Zhang T, Akyol-Ataman Z, Grock A, Hong PW, Li J, Watson NF, Fang AQ, Aguilar HC, Porotto M, Honko AN, Damoiseaux R, Miller JP, Woodson SE, Chantasirivisal S, Fontanes V, Negrete OA, Krogstad P, Dasgupta A, Moscona A, Hensley LE, Whelan SP, Faull KF, Holbrook MR, Jung ME, Lee B. 2010. A broad-spectrum antiviral targeting entry of enveloped viruses. Proc. Natl. Acad. Sci. U.S.A. 107:3157-3162.
39. Ivanovic T, Rozendaal R, Floyd DL, Popovic M, van Oijen AM, Harrison SC. 2012. Kinetics of proton transport into influenza virions by the viralM2channel. PLoS One 7:e31566. doi:10.1371/journal.pone.0031566.
40. Birch PJ, Dekker LV, James IF, Southan A, Cronk D. 2004. Strategies to identify ion channel modulators: current and novel approaches to target neuropathic pain. Drug Discov. Today 9:410-418.
41. Dunlop J, Bowlby M, Peri R, Vasilyev D, Arias R. 2008. Highthroughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat. Rev. Drug Discov. 7:358-368.
42. Johnson ID, Life T, Spence MTZ, Haugland RP. 2010. The molecular probes handbook: a guide to fluorescent probes and labeling technologies, 11th ed. Life Technologies, Eugene, OR.
43. Plasek J, Sigler K. 1996. Slow fluorescent indicators of membrane potential: a survey of different approaches to probe response analysis. J. Photochem. Photobiol. B 33:101-124.
44. Smith JC. 1990. Potential-sensitive molecular probes in membranes of bioenergetic relevance. Biochim. Biophys. Acta 1016:1-28.
45. Nicholls DG, Ward MW. 2000. Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts. Trends Neurosci. 23:166-174.
46. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.