Generation and characterization of a new panel of broadly reactive anti-NS1 mabs for detection of influenza A virus

Journal of General Virology

Volumn 94, Issue PART3, 2013, Pages 593-605

  Rahim, Md Niaz ^a,b   Selman, Mohammed ^c   Sauder, Patricia J ^b   Forbes, Nicole E ^c   Stecho, William ^c   Xu, Wanhong ^a,b,e   Lebar, Mark ^a,b   Brown, Earl G ^c   Coombs, Kevin M ^a,b,d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

^d John Buhler Research Centre   (Canada)

^e Public Health Agency of Canada   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 3;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL NUCLEUS; CLONE; CONTROLLED STUDY; CYTOPLASM; EPITOPE MAPPING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYBRIDOMA; IMMUNIZATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLUENZA VIRUS A; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SCREENING TEST; VIRUS CHARACTERIZATION; VIRUS REPLICATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; CELL LINE; DOGS; EPITOPE MAPPING; HUMANS; INFLUENZA A VIRUS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN CONFORMATION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84874065424     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.046649-0     Document Type: Article

References (48)

1. Ayllon, J., Hale, B. G. & García-Sastre, A. (2012). Strain-specific contribution of NS1-activated phosphoinositide 3-kinase signaling to influenza A virus replication and virulence. J Virol 86, 5366-5370.
2. Bao, Y. M., Bolotov, P., Dernovoy, D., Kiryutin, B., Zaslavsky, L., Tatusova, T., Ostell, J. & Lipman, D. (2008). The influenza virus resource at the National Center for Biotechnology Information. J Virol 82, 596-601.
3. Bergmann, M., Garcia-Sastre, A., Carnero, E., Pehamberger, H., Wolff, K., Palese, P. & Muster, T. (2000). Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J Virol 74, 6203-6206.
4. Bornholdt, Z. A. & Prasad, B. V. V. (2008). X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature 456, 985-988.
5. Brown, E. G. (1990). Increased virulence of a mouse-adapted variant of influenza A/FM/1/47 virus is controlled by mutations in genome segments 4, 5, 7, and 8. J Virol 64, 4523-4533.
6. Brown, L. E., Hinshaw, V. S. & Webster, R. G. (1983). Antigenic variation in the influenza A virus nonstructural protein, NS1. Virology 130, 134-143.
7. Chen, Z., Li, Y. & Krug, R. M. (1999). Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 39-end processing machinery. EMBO J 18, 2273-2283.
8. Dundon, W. G. (2012). Variability among the neuraminidase, non- structural 1 and PB1-F2 proteins in the influenza A virus genome. Virus Genes 44, 363-373.
9. Egorov, A., Brandt, S., Sereinig, S., Romanova, J., Ferko, B., Katinger, D., Grassauer, A., Alexandrova, G., Katinger, H. & Muster, T. (1998). Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol 72, 6437-6441.
10. Forbes, N. E., Ping, J., Dankar, S. K., Jia, J.-J., Selman, M., Keleta, L., Zhou, Y. & Brown, E. G. (2012). Multifunctional adaptive NS1 mutations are selected upon human influenza virus evolution in the mouse. PLoS ONE 7, e31839.
11. Fortes, P., Beloso, A. & Ortín, J. (1994). Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J 13, 704-712.
12. Gack, M. U., Albrecht, R. A., Urano, T., Inn, K.-S., Huang, I.-C., Carnero, E., Farzan, M., Inoue, S., Jung, J. U. & García-Sastre, A. (2009). Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5, 439-449.
13. Garaigorta, U. & Ortín, J. (2007). Mutation analysis of a recombinant NS replicon shows that influenza virus NS1 protein blocks the splicing and nucleo-cytoplasmic transport of its own viral mRNA. Nucleic Acids Res 35, 4573-4582.
14. García-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D. E., Durbin, J. E., Palese, P. & Muster, T. (1998). Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252, 324-330.
15. Greenspan, D., Palese, P. & Krystal, M. (1988). Two nuclear location signals in the influenza virus NS1 nonstructural protein. J Virol 62, 3020-3026.
16. Guo, Z., Chen, L.-M., Zeng, H., Gomez, J. A., Plowden, J., Fujita, T., Katz, J. M., Donis, R. O. & Sambhara, S. (2007). NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am J Respir Cell Mol Biol 36, 263-269.
17. Hale, B. G., Randall, R. E., Ortín, J. & Jackson, D. (2008). The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89, 2359-2376.
18. Harlow, E. & Lane, D. (1988). Antibodies: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
19. Hatada, E. & Fukuda, R. (1992). Binding of influenza A virus NS1 protein to dsRNA in vitro. J Gen Virol 73, 3325-3329.
20. Hatada, E., Takizawa, T. & Fukuda, R. (1992). Specific binding of influenza A virus NS1 protein to the virus minus-sense RNA in vitro. J Gen Virol 73, 17-25.
21. Jagger, B. W., Wise, H. M., Kash, J. C., Walters, K. A., Wills, N. M., Xiao, Y.-L., Dunfee, R. L., Schwartzman, L. M., Ozinsky, A. & other authors (2012). An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337, 199-204.
22. Jia, D. L., Rahbar, R., Chan, R. W. Y., Lee, S. M. Y., Chan, M. C. W., Wang, B. X. H., Baker, D. P., Sun, B., Peiris, J. S. M. & other authors (2010). Influenza virus non-structural protein 1 (NS1) disrupts interferon signaling. PLoS ONE 5, e13927.
23. Kochs, G., García-Sastre, A. & Martínez-Sobrido, L. (2007a). Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81, 7011-7021.
24. Kochs, G., Koerner, I., Thiel, L., Kothlow, S., Kaspers, B., Ruggli, N., Summerfield, A., Pavlovic, J., Stech, J. & Staeheli, P. (2007b). Properties of H7N7 influenza A virus strain SC35M lacking interferon antagonist NS1 in mice and chickens. J Gen Virol 88, 1403-1409.
25. Krug, R. M. & Etkind, P. R. (1973). Cytoplasmic and nuclear virus- specific proteins in influenza virus-infected MDCK cells. Virology 56, 334-348.
26. Li, Y., Yamakita, Y. & Krug, R. M. (1998). Regulation of a nuclear export signal by an adjacent inhibitory sequence: the effector domain of the influenza virus NS1 protein. Proc Natl Acad Sci U S A 95, 4864-4869.
27. Lindstrom, S. E., Hiromoto, Y., Nerome, R., Omoe, K., Sugita, S., Yamazaki, Y., Takahashi, T. & Nerome, K. (1998). Phylogenetic analysis of the entire genome of influenza A (H3N2) viruses from Japan: evidence for genetic reassortment of the six internal genes. J Virol 72, 8021-8031.
28. Ludwig, S., Schultz, U., Mandler, J., Fitch, W. M. & Scholtissek, C. (1991). Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses. Virology 183, 566-577.
29. Mibayashi, M., Martínez-Sobrido, L., Loo, Y.-M., Cárdenas, W. B., Gale, M., Jr & García-Sastre, A. (2007). Inhibition of retinoic acid- inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81, 514-524.
30. Nemeroff, M. E., Barabino, S. M. L., Li, Y., Keller, W. & Krug, R. M. (1998). Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 39 end formation of cellular pre- mRNAs. Mol Cell 1, 991-1000.
31. Newby, C. M., Sabin, L. & Pekosz, A. (2007). The RNA binding domain of influenza A virus NS1 protein affects secretion of tumor necrosis factor alpha, interleukin-6, and interferon in primary murine tracheal epithelial cells. J Virol 81, 9469-9480.
32. Noronha, J. M., Liu, M., Squires, R. B., Pickett, B. E., Hale, B. G., Air, G. M., Galloway, S. E., Takimoto, T., Schmolke, M. & other authors (2012). Influenza virus sequence feature variant type analysis: evidence of a role for NS1 in influenza virus host range restriction. J Virol 86, 5857-5866.
33. Opitz, B., Rejaibi, A., Dauber, B., Eckhard, J., Vinzing, M., Schmeck, B., Hippenstiel, S., Suttorp, N. & Wolff, T. (2007). IFNb induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 9, 930-938.
34. Palese, P. & Shaw, M. L. (2007). Orthomyxoviridae: the viruses and their replication. In Fields Virology, 5th edn, pp. 1647-1689. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
35. Ping, J. H., Keleta, L., Forbes, N. E., Dankar, S., Stecho, W., Tyler, S., Zhou, Y., Babiuk, L., Weingartl, H. & other authors (2011). Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS ONE 6, e21740.
36. Rai, M., Bhatia, S., Malik, Y. P. S. & Dubey, S. C. (2010). Production and characterization of monoclonal antibodies against NS1 protein of H5N1 avian influenza virus. Hybridoma (Larchmt) 29, 183-186.
37. Robb, N. C., Chase, G., Bier, K., Vreede, F. T., Shaw, P. C., Naffakh, N., Schwemmle, M. & Fodor, E. (2011). The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. J Virol 85, 5228-5231.
38. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
39. Sato, Y., Yoshioka, K., Suzuki, C., Awashima, S., Hosaka, Y., Yewdell, J. & Kuroda, K. (2003). Localization of influenza virus proteins to nuclear dot 10 structures in influenza virus-infected cells. Virology 310, 29-40.
40. Satterly, N., Tsai, P.-L., van Deursen, J., Nussenzveig, D. R., Wang, Y. M., Faria, P. A., Levay, A., Levy, D. E. & Fontoura, B. M. A. (2007). Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104, 1853-1858.
41. Selman, M., Dankar, S. K., Forbes, N. E., Jia, J.-J. & Brown, E. G. (2012). Adaptive mutation in influenza A virus non-structural gene is linked to host switching and induces a novel protein by alternative splicing. Emerg Microbes Infect 1, e42.
42. Slootstra, J. W., Puijk, W. C., Ligtvoet, G. J., Langeveld, J. P. M. & Meloen, R. H. (1996). Structural aspects of antibody-antigen interaction revealed through small random peptide libraries. Mol Divers 1, 87-96.
43. Squires, R. B., Noronha, J., Hunt, V., García-Sastre, A., Macken, C., Baumgarth, N., Suarez, D., Pickett, B. E., Zhang, Y. & other authors (2012). Influenza research database: an integrated bioinformatics resource for influenza research and surveillance. Influenza Other Respir Viruses 6, 404-416.
44. Suzuki, K., Bose, P., Leong-Quong, R. Y., Fujita, D. J. & Riabowol, K. (2010). REAP: A two minute cell fractionation method. BMC Res Notes 3, 294.
45. Tan, Z. H., Akerstrom, S., Wee, B. Y., Lal, S. K., Mirazimi, A. & Tan, Y.- J. (2010). A new panel of NS1 antibodies for easy detection and titration of influenza A virus. J Med Virol 82, 467-475.
46. Tong, S. X., Li, Y., Rivailler, P., Conrardy, C., Castillo, D. A. A., Chen, L.-M., Recuenco, S., Ellison, J. A., Davis, C. T. & other authors (2012). A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A109,4269-4274.
47. Treanor, J. J., Snyder, M. H., London, W. T. & Murphy, B. R. (1989). The B allele of the NS gene of avian influenza viruses, but not the A allele, attenuates a human influenza A virus for squirrel monkeys. Virology 171, 1-9.
48. Wright, P. F., Neumann, G. & Kawaoka, Y. (2007). Orthomyxoviruses. In Fields Virology, 5th edn, pp. 1691-1740. Edited by D. Knipe & P. M. Howley. Philadelphia: Lippincott Williams and Wilkins.