Solid-supported membrane technology for the investigation of the influenza A virus M2 channel activity

Pflugers Archiv European Journal of Physiology

Volumn 459, Issue 4, 2010, Pages 593-605

  Balannik, Victoria ^a   Obrdlik, Petr ^b   Inayat, Samsoon ^c   Steensen, Catrin ^b   Wang, Jun ^d   Rausch, Joshua M ^a,e   Degrado, William F ^d   Kelety, Bela ^b   Pinto, Lawrence H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b IonGate Biosciences   (Germany)

^c Northwestern University   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e ELMHURST COLLEGE   (United States)

Author keywords

A M2 channel; Influenza a virus; Proton channel; SSM based electrophysiology; SURFE2R; Technology

Indexed keywords

AMANTADINE; MEGLUMINE; MUTANT PROTEIN; PROTEIN M2;

ANIMAL CELL; ARTICLE; BIOSENSOR; CELL MEMBRANE; CELL STRAIN; CHO K1 CELL; CONTROLLED STUDY; DRUG SENSITIVITY; ELECTROPHYSIOLOGY; INFLUENZA VIRUS A; MEMBRANE CURRENT; MEMBRANE TECHNOLOGY; NONHUMAN; PATCH CLAMP; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLID SUPPORTED MEMBRANE TECHNOLOGY; TRANSIENT EXPRESSION; WILD TYPE;

AMANTADINE; ANIMALS; ANTIVIRAL AGENTS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; DRUG RESISTANCE, VIRAL; ELECTROPHYSIOLOGY; HUMANS; INFLUENZA A VIRUS; MICROBIAL SENSITIVITY TESTS; REPRODUCIBILITY OF RESULTS; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

EID: 77950931384     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-009-0760-1     Document Type: Article

References (44)

1. Cox NJ, Subbarao K (1999) Influenza. Lancet 354:1277-1282
2. Lamb RA, Zebedee SL, Richardson CD (1985) Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627-633
3. Lamb RA, Holsinger LJ, Pinto LH (1994) The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. In: Wimmer E (ed) Receptor-mediated virus entry into cells. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 303-321
4. Tang Y, Venkataraman P, Knopman J, Lamb RA, Pinto LH (2005) The M2 proteins of Influenza A and B viruses are single-pass proton channels. In: Fischer WB (ed) Viral membrane proteins: structure, function and drug design, Kluwer Academic/Plenum. Publisher, New York, pp 101-111
5. Pinto LH, Lamb RA (2007) Controlling influenza virus replication by inhibiting its proton channel. Mol. Biosyst 3:18-23
6. Pinto LH, Lamb RA (2006) The M2 proton channels of influenza A and B viruses. J Biol Chem 281:8997-9000
7. Hu J, Fu R, Nishimura K, Zhang L, Zhou HX, Busath DD, Vijayvergiya V, Cross TA (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
8. Bright RA, Shay DK, Shu. B, Cox NJ, Klimov AI (2006) Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 295:891-894
9. Deyde VM, Xu X, Bright RA, Shaw M, Smith CB, Zhang Y, Shu Y, Gubareva LV, Cox NJ, Klimov Al (2007) Surveillance of resistance to adamantanes among influenza A(H3N2) and A (H1N1) viruses isolated worldwide. J Infect Dis 196:249-257
10. Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH (1985) The molecular basis of the specific anti-influenza action, of amantadine. EMBO J 4:3021-3024
11. Cady SD, Mishanina TV, 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
12. Bright RA, Medina MJ, Xu X, Perez-Oronoz G, Wallis TR, Davis XM, Povinelli L, Cox NJ, Klimov AI (2005) Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366:1175-1181
13. Saito R, Sakai T, Sato I, Sano Y, Oshitani H, Sato M, 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
14. Mould JA, Paterson RG, Takeda M, Ohigashi Y, Venkataraman P, Lamb RA, Pinto LH (2003) Influenza B virus BM2 protein has ion channel activity that conducts protons across membranes. Dev Cell 5:175-184
15. 15. Shimbo K, Brassard DL, Lamb RA, Pinto LH (1996) Ion selectivity and activation of the M2 ion channel, of influenza virus. Biophys J 70:1335-1346 (Pubitemid 26073046)
16. Wang J, Cady SD, Balannik V, Pinto LH, DeGrado WF, 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
17. Pintschovius J, Fendler K (1999) Charge translocation by the Na+/K+-ATPase investigated on solid supported membranes: rapid solution exchange with a new technique. Biophys J 76:814-826
18. Schulz P, Garcia-Celma JJ, Fendler K (2008) SSM-based electrophysiology. Methods 46:97-103
19. Ganea C, Fendler K (2009) Bacterial transporters: charge translocation and mechanism. Biochim. Biophys Acta 1787 (6):706-713
20. Garcia-Celma JJ, Smimova IN, Kaback HR, Fendler K (2009) Electrophysiological characterization of LacY. Proc Natl Acad Sci USA 106:7373-7378
21. Kelety B, Diekert K, Tobien J, Watzke N, Domer W, Obrdlik P, Fendler K (2006) Transporter assays using solid supported membranes: a novel screening platform for drug discovery. Assay Drug Dev Technol 4:575-582
22. Krause R, Watzke N, Kelety B, Dorner W, Fendler K (2009) An automatic electrophysiological assay for the neuronal glutamate transporter mEAAC1. J Neurosci Methods 177:131-141
23. Weitz D, Harder D, Casagrande F, Fotiadis D, Obrdlik P, Kelety B, Daniel H (2007) Functional and structural characterization of a prokaryotic peptide transporter with features similar to mammalian PEPT1. J Biol Chem. 282:2832-2839
24. Schulz P, Dueck B, Mourot A, Hatahet L, Fendia K (2009) Measuring ion channels on solid supported membranes. Biophys J 97:388-396
25. Jing X, Ma C, Ohigashi Y, Oliveira FA, Jardetzky TS, Pinto LH, Lamb RA (2008) Functional studies indicate amantadine binds to the pore of the influenza A. virus M2 proton-selective ion channel. Proc Natl Acad Sci USA 105:10967-10972
26. Gandhi CS, Shuck K, Lear JD, Dieckmann GR, DeGrado WF, Lamb RA, Pinto LH (1999) Cu(II) inhibition of the proton translocation machinery of the influenza A virus M2 protein. J Biol Chem 274:5474-5482
27. 27. Chizhmakov IV, Geraghty FM, Ogden DC, Hayhurst A, Antoniou M, Hay AJ (1996) Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J Physiol 494(Pt 2):329-336 (Pubitemid 26318773)
28. Wang C, Takeuchi K, Pinto LH, Lamb RA (1993) Ion channel activity of influenza A. virus M2 protein: characterization of the amantadine block. J Virol 67:5585-5594
29. Lin TI, Schroeder C (2001) Definitive assignment of proton selectivity and attoampere unitary current to the M2 ion channel protein, of influenza A virus. J Virol 75:3647-3656
30. Schroeder C, Ford CM, Wharton SA, Hay AJ (1994) Functional reconstitution in lipid vesicles of influenza virus M2 protein expressed by baculovirus: evidence for proton transfer activity. J Gen Virol 75(Pt 12):3477-3484
31. Skehel. JJ, Hay AJ, Armstrong JA (1978) On the mechanism of inhibition of influenza virus replication by amantadine hydrochloride. J Gen Virol 38:97-110
32. Stouffer AL, Ma C, Cristian L, Ohigashi Y, Lamb RA, Lear JD, Pinto LH, DeGrado WF (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
33. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195
34. Balannik V, Wang J, 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 (in press)
35. Tu Q, Pinto LH, Luo G, Shaughnessy MA, Mullaney D, Kurtz S, Krystal M, Lamb RA (1996) Characterization of inhibition of M2 ion channel, activity by BL-1743, an inhibitor of influenza A virus. J Virol 70:4246-4252
36. Kolocouris A, Spearpoint P, Martin SR, Hay AJ, Lopez-Querol M, Sureda FX, Padalko E, Neyts J, De Clercq E (2008) Comparisons of the influenza virus A M2 channel, binding affinities, antiinfluenza virus potencies and NMDA antagonistic activities of 2alkyl-2-aminoadamantanes and analogues. Bioorg Med Chem Lett 18:6156-6160
37. Goldstein S, Czapski G (1986) The role and mechanism of metal ions and their complexes in enhancing damage in biological systems or in protecting these systems from the toxicity of 02. J Free Radic Biol Med 2:3-11
38. Schnell JR, Chou JJ (2008) Structure and mechanism of the M2 proton, channel of influenza A virus. Nature 451:591-595
39. Stouffer AL, Acharya R, Saiom D, Levine AS, Di Costanzo L, Soto CS, Tereshko V, Nanda V, Stayrook S, DeGrado WF (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596-599
40. Li C, Qin H, Gao FP, Cross TA (2007) Solid-state NMR characterization of conformational plasticity within the transmembrane domain of the influenza A M2 proton channel. Biochim Biophys Acta 1768:3162-3170
41. Yi M, Cross TA, Zhou HX (2008) A secondary gate as a mechanism for inhibition of the M2 proton channel by amantadine. J Phys Chem B 112:7977-7979
42. Yi M, Cross TA, Zhou HX (2009) Conformational heterogeneity of the M2 proton channel and a structural model for channel activation. Proc Natl Acad Sci USA 106:13311-13316
43. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with, a novel eukaryotic vector. Gene 108:193-199
44. Balannik V, Lamb RA, Pinto LH (2008) The oligomeric state of the active BM2 ion channel protein of influenza B virus. J Biol Chem 283:4895-4904