Asparagine Substitution at PB2 Residue 701 Enhances the Replication, Pathogenicity, and Transmission of the 2009 Pandemic H1N1 Influenza A Virus

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Zhou, Bin ^a,b,c   Pearce, Melissa B ^d   Li, Yan ^b   Wang, Jieru ^e   Mason, Robert J ^e   Tumpey, Terrence M ^d   Wentworth, David E ^a,b,c  

^a J CRAIG VENTER INSTITUTE   (United States)

^b WADSWORTH CENTER   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^e DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; INTERFERON; INTERFERON LAMBDA; UNCLASSIFIED DRUG;

2009 H1N1 INFLUENZA; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; EMBRYO; FEMALE; FERRET; GENE ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS EPITHELIUM; MALE; MOUSE; NONHUMAN; PB2 701N GENE; RESIDUE ANALYSIS; VIRUS GENE; VIRUS GENOME; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; ASPARAGINE; CELL LINE, TUMOR; CYTOKINES; DOGS; FEMALE; FERRETS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; KINETICS; MALE; MICE; MICE, INBRED BALB C; PNEUMOCYTES; RNA REPLICASE; VIRAL PROTEINS; VIRUS REPLICATION;

AVES; INFLUENZA A VIRUS; MAMMALIA; MUS; MUSTELA; ORTHOMYXOVIRIDAE;

EID: 84879051825     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067616     Document Type: Article

References (45)

1. Neumann G, Noda T, Kawaoka Y, (2009) Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459: 931-939. doi:10.1038/nature08157. PubMed: 19525932.
2. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, et al. (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459: 1122-1125. doi:10.1038/nature08182. PubMed: 19516283.
3. Wang TT, Palese P, (2009) Unraveling the mystery of swine influenza virus. Cell 137: 983-985. doi:10.1016/j.cell.2009.05.032. PubMed: 19524497.
4. Jagger BW, Memoli MJ, Sheng ZM, Qi L, Hrabal RJ, et al. (2010) The PB2-E627K mutation attenuates viruses containing the 2009 H1N1 influenza pandemic polymerase. MBio 1: e00067-00010. PubMed: 20689744.
5. Zhu H, Wang J, Wang P, Song W, Zheng Z, et al. (2010) Substitution of lysine at 627 position in PB2 protein does not change virulence of the 2009 pandemic H1N1 virus in mice. Virology 401: 1-5. doi:10.1016/j.virol.2010.02.024. PubMed: 20303563.
6. Yamada S, Hatta M, Staker BL, Watanabe S, Imai M, et al. (2010) Biological and structural characterization of a host-adapting amino acid in influenza virus. PLOS Pathog 6: e1001034.
7. Herfst S, Chutinimitkul S, Ye JQ, de Wit E, Munster VJ, et al. (2010) Introduction of Virulence Markers in PB2 of Pandemic Swine-Origin Influenza Virus Does Not Result in Enhanced Virulence or Transmission. J Virol 84: 3752-3758. doi:10.1128/JVI.02634-09. PubMed: 20130063.
8. Zhou B, Li Y, Halpin R, Hine E, Spiro DJ, et al. (2011) PB2 residue 158 is a pathogenic determinant of pandemic H1N1 and H5 influenza a viruses in mice. J Virol 85: 357-365. doi:10.1128/JVI.01694-10. PubMed: 20962098.
9. Subbarao EK, London W, Murphy BR, (1993) A single amino acid in the PB2 gene of influenza A virus Is a determinant of host range. J Virol 67: 1761-1764. PubMed: 8445709.
10. Le QM, Ito M, Muramoto Y, Hoang PVM, Vuong CD, et al. (2010) Pathogenicity of highly pathogenic avian H5N1 influenza A viruses isolated from humans between 2003 and 2008 in northern Vietnam. J Gen Virol 91: 2485-2490. doi:10.1099/vir.0.021659-0. PubMed: 20592108.
11. Munster VJ, de Wit E, van Riel D, Beyer WE, Rimmelzwaan GF, et al. (2007) The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 196: 258-265. doi:10.1086/518792. PubMed: 17570113.
12. Steel J, Lowen AC, Mubareka S, Palese P, (2009) Transmission of Influenza Virus in a Mammalian Host Is Increased by PB2 Amino Acids 627K or 627E/701N. PLOS Pathog 5: e1000252. PubMed: 19119420.
13. Hatta M, Gao P, Halfmann P, Kawaoka Y, (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293: 1840-1842. doi:10.1126/science.1062882. PubMed: 11546875.
14. Mehle A, Doudna JA, (2009) Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A 106: 21312-21316. doi:10.1073/pnas.0911915106. PubMed: 19995968.
15. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJD, et al. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12: 1203-1207. doi:10.1038/nm1477. PubMed: 16964257.
16. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, et al. (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102: 18590-18595. doi:10.1073/pnas.0507415102. PubMed: 16339318.
17. Le QM, Sakai-Tagawa Y, Ozawa M, Ito M, Kawaoka Y, (2009) Selection of H5N1 influenza virus PB2 during replication in humans. J Virol 83: 5278-5281. doi:10.1128/JVI.00063-09. PubMed: 19264775.
18. Zhou B, Li Y, Speer SD, Subba A, Lin X, et al. (2012) Engineering temperature sensitive live attenuated influenza vaccines from emerging viruses. Vaccine 30: 3691-3702. doi:10.1016/j.vaccine.2012.03.025. PubMed: 22449422.
19. Zhou B, Jerzak G, Scholes DT, Donnelly ME, Li Y, et al. (2011) Reverse genetics plasmid for cloning unstable influenza A virus gene segments. J Virol Methods 173: 378-383. doi:10.1016/j.jviromet.2011.01.021. PubMed: 21295611.
20. Zhou B, Donnelly ME, Scholes DT, St George K, Hatta M, et al. (2009) Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol 83: 10309-10313. doi:10.1128/JVI.01109-09. PubMed: 19605485.
21. Zhou B, Li Y, Belser JA, Pearce MB, Schmolke M, et al. (2010) NS-based live attenuated H1N1 pandemic vaccines protect mice and ferrets. Vaccine 28: 8015-8025. doi:10.1016/j.vaccine.2010.08.106. PubMed: 20934458.
22. Quinlivan M, Zamarin D, García-Sastre A, Cullinane A, Chambers T, et al. (2005) Attenuation of equine influenza viruses through truncations of the NS1 protein. J Virol 79: 8431-8439. doi:10.1128/JVI.79.13.8431-8439.2005. PubMed: 15956587.
23. Wang J, Edeen K, Manzer R, Chang Y, Wang S, et al. (2007) Differentiated human alveolar epithelial cells and reversibility of their phenotype in vitro. Am J Respir Cell Mol Biol 36: 661-668. doi:10.1165/rcmb.2006-0410OC. PubMed: 17255555.
24. Wang J, Wang S, Manzer R, McConville G, Mason RJ, (2006) Ozone induces oxidative stress in rat alveolar type II and type I-like cells. Free Radic Biol Med 40: 1914-1928. doi:10.1016/j.freeradbiomed.2006.01.017. PubMed: 16716893.
25. Wang J, Nikrad MP, Travanty EA, Zhou B, Phang T, et al. (2012) Innate immune response of human alveolar macrophages during influenza A infection. PLOS ONE 7: e29879. doi:10.1371/journal.pone.0029879. PubMed: 22396727.
26. Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T, et al. (2006) Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103: 12121-12126. doi:10.1073/pnas.0605134103. PubMed: 16880383.
27. Pearce MB, Jayaraman A, Pappas C, Belser JA, Zeng H, et al. (2012) Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets. Proc Natl Acad Sci U S A 109: 3944-3949. doi:10.1073/pnas.1119945109. PubMed: 22355116.
28. Li Z, Chen H, Jiao P, Deng G, Tian G, et al. (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79: 12058-12064. doi:10.1128/JVI.79.18.12058-12064.2005. PubMed: 16140781.
29. Mason RJ, (2006) Biology of alveolar type II cells. Respirology 11 (Suppl):: S12-S15. doi:10.1111/j.1440-1843.2006.00800.x. PubMed: 16423262.
30. Wang J, Nikrad MP, Phang T, Gao B, Alford T, et al. (2011) Innate immune response to influenza A virus in differentiated human alveolar type II cells. Am J Respir Cell Mol Biol 45: 582-591. doi:10.1165/rcmb.2010-0108OC. PubMed: 21239608.
31. Yu WC, Chan RW, Wang J, Travanty EA, Nicholls JM, et al. (2011) Viral replication and innate host responses in primary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J Virol 85: 6844-6855. doi:10.1128/JVI.02200-10. PubMed: 21543489.
32. Wang J, Oberley-Deegan R, Wang S, Nikrad M, Funk CJ, et al. (2009) Differentiated human alveolar type II cells secrete antiviral IL-29 (IFN-lambda 1) in response to influenza A infection. J Immunol 182: 1296-1304. PubMed: 19155475.
33. Maines TR, Jayaraman A, Belser JA, Wadford DA, Pappas C, et al. (2009) Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325: 484-487. PubMed: 19574347.
34. Belser JA, Jayaraman A, Raman R, Pappas C, Zeng H, et al. (2011) Effect of D222G mutation in the hemagglutinin protein on receptor binding, pathogenesis and transmissibility of the 2009 pandemic H1N1 influenza virus. PLOS ONE 6: e25091. doi:10.1371/journal.pone.0025091. PubMed: 21966421.
35. Jayaraman A, Pappas C, Raman R, Belser JA, Viswanathan K, et al. (2011) A single base-pair change in 2009 H1N1 hemagglutinin increases human receptor affinity and leads to efficient airborne viral transmission in ferrets. PLOS ONE 6: e17616. doi:10.1371/journal.pone.0017616. PubMed: 21407805.
36. Gabriel G, Herwig A, Klenk HD, (2008) Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLOS Pathog 4: e11. doi:10.1371/journal.ppat.0040011. PubMed: 18248089.
37. Gabriel G, Klingel K, Otte A, Thiele S, Hudjetz B, et al. (2011) Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat Commun 2: 156. doi:10.1038/ncomms1158. PubMed: 21245837.
38. Tarendeau F, Boudet J, Guilligay D, Mas PJ, Bougault CMet al. (2007) Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14: 229-233. doi:10.1038/nsmb1212. PubMed: 17310249.
39. Gao Y, Zhang Y, Shinya K, Deng G, Jiang Y, et al. (2009) Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLOS Pathog 5: e1000709.
40. Squires RB, Noronha J, Hunt V, Garcia-Sastre A, Macken C, et al. (2012) Influenza Research Database: an integrated bioinformatics resource for influenza research and surveillance. Influenza Other Respi Viruses 6(6):: 404-416.
41. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, et al. (2008) The influenza virus resource at the National Center for Biotechnology Information. J Virol 82: 596-601. doi:10.1128/JVI.02005-07. PubMed: 17942553.
42. Bogner P, Capua I, Lipman DJ, Cox NJ, others (2006) A global initiative on sharing avian flu data. Nature 442: 981-981.
43. Dawood FS, Iuliano AD, Reed C, Meltzer MI, Shay DK, et al. (2012) Estimated global mortality associated witih the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 12(9):: 687-695.
44. Graef KM, Vreede FT, Lau YF, McCall AW, Carr SM, et al. (2010) The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol 84: 8433-8445. doi:10.1128/JVI.00879-10. PubMed: 20538852.
45. Ozawa M, Basnet S, Burley LM, Neumann G, Hatta M, et al. (2011) Impact of amino acid mutations in PB2, PB1-F2, and NS1 on the replication and pathogenicity of pandemic (H1N1) 2009 influenza viruses. J Virol 85: 4596-4601. doi:10.1128/JVI.00029-11. PubMed: 21325408.