Identification of a Novel Splice Variant Form of the Influenza A Virus M2 Ion Channel with an Antigenically Distinct Ectodomain

PLoS Pathogens

Volumn 8, Issue 11, 2012, Pages

  Wise, Helen M ^a,b   Hutchinson, Edward C ^a,d   Jagger, Brett W ^a,c   Stuart, Amanda D ^a   Kang, Zi H ^a   Robb, Nicole ^d   Schwartzman, Louis M ^c   Kash, John C ^c   Fodor, Ervin ^d   Firth, Andrew E ^a   Gog, Julia R ^a   Taubenberger, Jeffery K ^c   Digard, Paul ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; MESSENGER RNA; MESSENGER RNA2; MESSENGER RNA4; PROTEIN M2; PROTEIN M42; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; INFLUENZA VIRUS A; LIFE CYCLE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERTANT; UPREGULATION; VIRUS REPLICATION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; BIRDS; CELL LINE, TUMOR; DISEASE OUTBREAKS; DOGS; HUMANS; INFLUENZA A VIRUS, H5N2 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MICE; MICE, INBRED BALB C; NORTH AMERICA; RNA, MESSENGER; RNA, VIRAL; VIRAL MATRIX PROTEINS;

AVIAN INFLUENZA VIRUS; INFLUENZA A VIRUS; MUS;

EID: 84870834635     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002998     Document Type: Article

References (62)

1. Salomon R, Webster RG, (2009) The influenza virus enigma. Cell 136: 402-410.
2. Du L, Zhou Y, Jiang S, (2010) Research and development of universal influenza vaccines. Microbes Infect 12: 280-286.
3. Fiers W, De Filette M, El Bakkouri K, Schepens B, Roose K, et al. (2009) M2e-based universal influenza A vaccine. Vaccine 27: 6280-6283.
4. Wise HM, Foeglein A, Sun J, Dalton RM, Patel S, et al. (2009) A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 83: 8021-8031.
5. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, et al. (2012) An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337: 199-204.
6. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, et al. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7: 1306-1312.
7. Wise HM, Barbezange C, Jagger BW, Dalton RM, Gog JR, et al. (2011) Overlapping signals for translational regulation and packaging of influenza A virus segment 2. Nucleic Acids Res 39: 7775-7790.
8. Inglis SC, Gething MJ, Brown CM, (1980) Relationship between the messenger RNAs transcribed from two overlapping genes of influenza virus. Nucleic Acids Res 8: 3575-3589.
9. Lamb RA, Lai CJ, (1980) Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for the two overlapping nonstructural proteins of influenza virus. Cell 21: 475-485.
10. Inglis SC, Brown CM, (1981) Spliced and unspliced RNAs encoded by virion RNA segment 7 of influenza virus. Nucleic Acids Res 9: 2727-2740.
11. Lamb RA, Lai CJ, Choppin PW, (1981) Sequences of mRNAs derived from genome RNA segment 7 of influenza virus: colinear and interrupted mRNAs code for overlapping proteins. Proc Natl Acad Sci U S A 78: 4170-4174.
12. Shih SR, Suen PC, Chen YS, Chang SC, (1998) A novel spliced transcript of influenza A/WSN/33 virus. Virus Genes 17: 179-183.
13. Lamb RA, Choppin PW, (1981) Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 112: 729-737.
14. Shih SR, Nemeroff ME, Krug RM, (1995) The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci U S A 92: 6324-6328.
15. Chiang C, Chen GW, Shih SR, (2008) Mutations at alternative 5′ splice sites of M1 mRNA negatively affect influenza A virus viability and growth rate. J Virol 82: 10873-10886.
16. Jackson D, Lamb RA, (2008) The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J Gen Virol 89: 3097-3101.
17. Robb NC, Fodor E, (2011) The accumulation of influenza A virus segment 7 spliced mRNAs is regulated by the NS1 protein. J Gen Virol In press.
18. Holsinger LJ, Lamb RA, (1991) Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183: 32-43.
19. Sugrue RJ, Hay AJ, (1991) Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180: 617-624.
20. Schnell JR, Chou JJ, (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451: 591-595.
21. Pielak RM, Chou JJ, (2011) Influenza M2 proton channels. Biochim Biophys Acta 1808: 522-529.
22. 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.
23. Pinto LH, Holsinger LJ, Lamb RA, (1992) Influenza virus M2 protein has ion channel activity. Cell 69: 517-528.
24. Bukrinskaya AG, Vorkunova NK, Pushkarskaya NL, (1982) Uncoating of a rimantadine-resistant variant of influenza virus in the presence of rimantadine. J Gen Virol 60: 61-66.
25. Sugrue RJ, Bahadur G, Zambon MC, Hall-Smith M, Douglas AR, et al. (1990) Specific structural alteration of the influenza haemagglutinin by amantadine. EMBO J 9: 3469-3476.
26. Chen BJ, Leser GP, Jackson D, Lamb RA, (2008) The influenza virus M2 protein cytoplasmic tail interacts with the M1 protein and influences virus assembly at the site of virus budding. J Virol 82: 10059-10070.
27. Grantham ML, Stewart SM, Lalime EN, Pekosz A, (2010) Tyrosines in the influenza A virus M2 protein cytoplasmic tail are critical for production of infectious virus particles. J Virol 84: 8765-8776.
28. Iwatsuki-Horimoto K, Horimoto T, Noda T, Kiso M, Maeda J, et al. (2006) The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J Virol 80: 5233-5240.
29. 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.
30. McCown MF, Pekosz A, (2006) Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J Virol 80: 8178-8189.
31. Rossman JS, Jing X, Leser GP, Balannik V, Pinto LH, et al. (2010) Influenza virus m2 ion channel protein is necessary for filamentous virion formation. J Virol 84: 5078-5088.
32. Rossman JS, Jing X, Leser GP, Lamb RA, (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142: 902-913.
33. Parks GD, Hull JD, Lamb RA, (1989) Transposition of domains between the M2 and HN viral membrane proteins results in polypeptides which can adopt more than one membrane orientation. J Cell Biol 109: 2023-2032.
34. Parks GD, Lamb RA, (1991) Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain. Cell 64: 777-787.
35. Park EK, Castrucci MR, Portner A, Kawaoka Y, (1998) The M2 ectodomain is important for its incorporation into influenza A virions. J Virol 72: 2449-2455.
36. Cheung TK, Guan Y, Ng SS, Chen H, Wong CH, et al. (2005) Generation of recombinant influenza A virus without M2 ion-channel protein by introduction of a point mutation at the 5′ end of the viral intron. J Gen Virol 86: 1447-1454.
37. Hutchinson EC, Curran MD, Read EK, Gog JR, Digard P, (2008) Mutational analysis of cis-acting RNA signals in segment 7 of influenza A virus. J Virol 82: 11869-11879.
38. Watanabe T, Watanabe S, Ito H, Kida H, Kawaoka Y, (2001) Influenza A virus can undergo multiple cycles of replication without M2 ion channel activity. J Virol 75: 5656-5662.
39. 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.
40. Wang R, Song A, Levin J, Dennis D, Zhang NJ, et al. (2008) Therapeutic potential of a fully human monoclonal antibody against influenza A virus M2 protein. Antiviral Res 80: 168-177.
41. Zebedee SL, Lamb RA, (1988) Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol 62: 2762-2772.
42. Zhang M, Zharikova D, Mozdzanowska K, Otvos L, Gerhard W, (2006) Fine specificity and sequence of antibodies directed against the ectodomain of matrix protein 2 of influenza A virus. Mol Immunol 43: 2195-2206.
43. Zhirnov OP, Konakova TE, Wolff T, Klenk HD, (2002) NS1 protein of influenza A virus down-regulates apoptosis. J Virol 76: 1617-1625.
44. Hughey PG, Compans RW, Zebedee SL, Lamb RA, (1992) Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J Virol 66: 5542-5552.
45. Jackson IJ, (1991) A reappraisal of non-consensus mRNA splice sites. Nucleic Acids Res 19: 3795-3798.
46. Kozak M, (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292.
47. de Wit E, Spronken MI, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, et al. (2004) Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res 103: 155-161.
48. De Filette M, Ysenbaert T, Roose K, Schotsaert M, Roels S, et al. (2011) Antiserum against the conserved nine amino acid N-terminal peptide of influenza A virus matrix protein 2 is not immunoprotective. J Gen Virol 92: 301-306.
49. Suarez DL, Senne DA, (2000) Sequence analysis of related low-pathogenic and highly pathogenic H5N2 avian influenza isolates from United States live bird markets and poultry farms from 1983 to 1989. Avian Dis 44: 356-364.
50. Lupiani B, Reddy SM, (2009) The history of avian influenza. Comp Immunol Microbiol Infect Dis 32: 311-323.
51. Ohuchi M, Cramer A, Vey M, Ohuchi R, Garten W, et al. (1994) Rescue of vector-expressed fowl plague virus hemagglutinin in biologically active form by acidotropic agents and coexpressed M2 protein. J Virol 68: 920-926.
52. Blencowe BJ, Ahmad S, Lee LJ, (2009) Current-generation high-throughput sequencing: deepening insights into mammalian transcriptomes. Genes Dev 23: 1379-1386.
53. Amorim MJ, Bruce EA, Read EK, Foeglein A, Mahen R, et al. (2011) A Rab11- and microtubule-dependent mechanism for cytoplasmic transport of influenza A virus viral RNA. J Virol 85: 4143-4156.
54. Roberts PC, Lamb RA, Compans RW, (1998) The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240: 127-137.
55. Amorim MJ, Read EK, Dalton RM, Medcalf L, Digard P, (2007) Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity. Traffic 8: 1-11.
56. Noton SL, Medcalf E, Fisher D, Mullin AE, Elton D, et al. (2007) Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 88: 2280-2290.
57. Matrosovich M, Matrosovich T, Garten W, Klenk HD, (2006) New low-viscosity overlay medium for viral plaque assays. Virol J 3: 63.
58. Abramoff MD, Magelhaes PJ, Ram SJ, (1996) Image processing with ImageJ. Biophotonics International 11: 36-42.
59. Robb NC, Jackson D, Vreede FT, Fodor E, (2010) Splicing of influenza A virus NS1 mRNA is independent of the viral NS1 protein. J Gen Virol 91: 2331-2340.
60. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, et al. (2001) Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75: 408-419.
61. Zebedee SL, Lamb RA, (1989) Growth restriction of influenza A virus by M2 protein antibody is genetically linked to the M1 protein. Proc Natl Acad Sci U S A 86: 1061-1065.
62. Shih SR, Krug RM, (1996) Novel exploitation of a nuclear function by influenza virus: the cellular SF2/ASF splicing factor controls the amount of the essential viral M2 ion channel protein in infected cells. Embo J 15: 5415-5427.