Assessment of transmission, pathogenesis and adaptation of H2 subtype influenza viruses in ferrets

Virology

Volumn 477, Issue , 2015, Pages 61-71

  Pappas, Claudia ^a   Yang, Hua ^a   Carney, Paul J ^a   Pearce, Melissa B ^a   Katz, Jacqueline M ^a   Stevens, James ^a   Tumpey, Terrence M ^a  

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

Author keywords

Ferret; Hemagglutinin; Influenza; Transmission

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; MUTANT PROTEIN; POLYSACCHARIDE; PROTEIN BINDING;

ADAPTATION; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; FERRET; HA 1 GENE; INFLUENZA A; INFLUENZA A (H2N2); INFLUENZA A (H2N3); MALE; MICROARRAY ANALYSIS; NONHUMAN; RECEPTOR BINDING; VIRUS GENE; VIRUS ISOLATION; VIRUS PATHOGENESIS; VIRUS TRANSMISSION; VIRUS VIRULENCE; X RAY CRYSTALLOGRAPHY; ANIMAL; BIRD; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; INFLUENZA A VIRUS; ISOLATION AND PURIFICATION; MISSENSE MUTATION; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PIG; TRANSMISSION; VIROLOGY; VIRULENCE; VIRUS ATTACHMENT;

AVES; MAMMALIA; MUSTELA; ORTHOMYXOVIRIDAE; SUIDAE;

ADAPTATION, BIOLOGICAL; ANIMALS; BIRDS; CRYSTALLOGRAPHY, X-RAY; DISEASE MODELS, ANIMAL; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; MICROARRAY ANALYSIS; MUTANT PROTEINS; MUTATION, MISSENSE; ORTHOMYXOVIRIDAE INFECTIONS; POLYSACCHARIDES; PROTEIN BINDING; SWINE; VIRULENCE; VIRUS ATTACHMENT;

EID: 84922380594     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.01.002     Document Type: Article

References (62)

1. Adams P.D., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66(Pt 2):213-221.
2. Belser J.A., et al. Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 2013, 501(7468):556-559.
3. Bussey K.A., Bousse T.L., Desmet E.A., Kim B., Takimoto T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J. Virol. 2010, 84(9):4395-4406.
4. CCP4 The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50(Pt 5):760-763.
5. Chen G.L., et al. Evaluation of replication and cross-reactive antibody responses of H2 subtype influenza viruses in mice and ferrets. J. Virol. 2010, 84(15):7695-7702.
6. Chen L.M., et al. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 2012, 422(1):105-113.
7. Conenello G.M., Zamarin D., Perrone L.A., Tumpey T., Palese P. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog. 2007, 3(10):1414-1421.
8. Connor R.J., Kawaoka Y., Webster R.G., Paulson J.C. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 1994, 205(1):17-23.
9. Davis I.W., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35(Web Server issue):W375-W383.
10. DeLano W.L., 2002. The PyMol Molecular Graphics Systems. http://www.pymol.org.
11. Dowdle W.R. Influenza pandemic periodicity, virus recycling, and the art of risk assessment. Emerg. Infect. Dis. 2006, 12(1):34-39.
12. Driskell E.A., Jones C.A., Stallknecht D.E., Howerth E.W., Tompkins S.M. Avian influenza virus isolates from wild birds replicate and cause disease in a mouse model of infection. Virology 2010, 399(2):280-289.
13. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60(Pt 12 Pt 1):2126-2132.
14. Ferro P.J., et al. Multiyear surveillance for avian influenza virus in waterfowl from wintering grounds, Texas coast, USA. Emerg. Infect. Dis. 2010, 16(8):1224-1230.
15. Glaser L., et al. Sequence analysis and receptor specificity of the hemagglutinin of a recent influenza H2N2 virus isolated from chicken in North America. Glycoconj. J. 2006, 23(1-2):93-99.
16. Herfst S., et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012, 336(6088):1534-1541.
17. Jackson D., Hossain M.J., Hickman D., Perez D.R., Lamb R.A. A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc. Natl. Acad. Sci. USA 2008, 105(11):4381-4386.
18. Jones J.C., et al. Risk assessment of H2N2 influenza viruses from the avian reservoir. J. Virol. 2014, 88(2):1175-1188.
19. Killian M.L., Zhang Y., Panigrahy B., Trampel D., Yoon K.J. Identification and characterization of H2N3 avian influenza virus from backyard poultry and comparison with novel H2N3 swine influenza virus. Avian Dis. 2011, 55(4):611-619.
20. Kishida N, et al. H2N5 influenza virus isolates from terns in Australia: genetic reassortants between those of the Eurasian and American lineages. Virus Genes 2008, 37(1):16-21.
21. Liu J., et al. Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957. Proc. Natl. Acad. Sci. USA 2009, 106(40):17175-17180.
22. Liu J.H., et al. Interregional transmission of the internal protein genes of H2 influenza virus in migratory ducks from North America to Eurasia. Virus Genes 2004, 29(1):81-86.
23. Liu Q., et al. Combination of PB2 271A and SR polymorphism at positions 590/591 is critical for viral replication and virulence of swine influenza virus in cultured cells and in vivo. J. Virol. 2012, 86(2):1233-1237.
24. Liu S., et al. Panorama phylogenetic diversity and distribution of Type A influenza virus. PloS One 2009, 4(3):e5022.
25. Ma W., et al. Identification of H2N3 influenza A viruses from swine in the United States. Proc. Natl. Acad. Sci. USA 2007, 104(52):20949-20954.
26. Maines T.R., et al. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 2005, 79(18):11788-11800.
27. Maines T.R., et al. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc. Natl. Acad. Sci. USA 2006, 103(32):12121-12126.
28. Maines T.R., et al. Transmission and pathogenesis of swine-origin 2009A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325(5939):484-487.
29. Maines T.R., et al. Effect of receptor binding domain mutations on receptor binding and transmissibility of avian influenza H5N1 viruses. Virology 2011, 413(1):139-147.
30. Makarova N.V., Kaverin N.V., Krauss S., Senne D., Webster R.G. Transmission of Eurasian avian H2 influenza virus to shorebirds in North America. J. Gen. Virol. 1999, 80(Pt 12):3167-3171.
31. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 2005, 61(Pt 4):458-464.
32. Mehle A., Doudna J.A. Adaptive strategies of the influenza virus polymerase for replication in humans. Proc. Natl. Acad. Sci. USA 2009, 106(50):21312-21316.
33. Nabel G.J., Wei C.J., Ledgerwood J.E. Vaccinate for the next H2N2 pandemic now. Nature 2011, 471(7337):157-158.
34. Negovetich N.J., Webster R.G. Thermostability of subpopulations of H2N3 influenza virus isolates from mallard ducks. J. Virol. 2010, 84(18):9369-9376.
35. Otwinowski Z. & Minor W., 1997. Scalepack Manual.
36. Pappas C., et al. Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PloS One 2010, 5(6):e11158.
37. Pearce M.B., et al. Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets. Proc. Natl. Acad. Sci. USA 2012, 109(10):3944-3949.
38. Piaggio A.J., et al. Molecular surveillance of low pathogenic avian influenza viruses in wild birds across the United States: inferences from the hemagglutinin gene. PloS One 2012, 7(12):e50834.
39. Pyhala R. Antibody status to influenza A/Singapore/1/57(H2N2) in Finland during a period of outbreaks caused by H3N2 and H1N1 subtype viruses. J. Hyg. 1985, 95(2):437-445.
40. Ramey A.M., et al. Transmission and reassortment of avian influenza viruses at the Asian-North American interface. Virology 2010, 406(2):352-359.
41. Richmond J.Y., McKinney R.W. Biosafety in Microbiological and Biomedical Laboratories 2007, Centers for Disease Control and Prevention, Atlanta, GA. 5th Ed.
42. Richt J.A., et al. Recently emerged swine influenza A virus (H2N3) causes severe pneumonia in Cynomolgus macaques. PloS One 2012, 7(7):e39990.
43. Rogers G.N., Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127(2):361-373.
44. Rogers G.N., et al. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 1983, 304(5921):76-78.
45. Russell C.A., et al. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 2012, 336(6088):1541-1547.
46. Salomon R., et al. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J. Exp. Med. 2006, 203(3):689-697.
47. Schafer J.R., et al. Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 1993, 194(2):781-788.
48. Simonsen L., et al. Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. J. Infect. Dis. 1998, 178(1):53-60.
49. Sorrell E.M., Wan H., Araya Y., Song H., Perez D.R. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl. Acad. Sci. USA 2009, 106(18):7565-7570.
50. Stevens J., et al. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 2004, 303(5665):1866-1870.
51. Stevens J., et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 2006, 355(5):1143-1155.
52. Stevens J., et al. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 2006, 312(5772):404-410.
53. Tumpey T.M., et al. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 2007, 315(5812):655-659.
54. Van Hoeven N., et al. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc. Natl. Acad. Sci. USA 2009, 106(9):3366-3371.
55. Viswanathan K., et al. Determinants of glycan receptor specificity of H2N2 influenza A virus hemagglutinin. PloS One 2010, 5(10):e13768.
56. Webster R.G. Predictions for future human influenza pandemics. J. Infect. Dis. 1997, 176(Suppl. 1):S14-S19.
57. Winn M.D., Isupov M.N., Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 2001, 57(Pt 1):122-133.
58. World Health Organization, 2013. Influenza at the Human-Animal Interface (HAI).
59. Xu R., McBride R., Paulson J.C., Basler C.F., Wilson I.A. Structure, receptor binding, and antigenicity of influenza virus hemagglutinins from the 1957 H2N2 pandemic. J. Virol. 2010, 84(4):1715-1721.
60. Yang H., Chen L.M., Carney P.J., Donis R.O., Stevens J. Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog. 2010, 6(9):e1001081.
61. Yang H., Carney P., Stevens J. Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr. 2010, 2.
62. Yang H., Carney P.J., Donis R.O., Stevens J. Structure and receptor complexes of the hemagglutinin from a highly pathogenic H7N7 influenza virus. J. Virol. 2012, 86(16):8645-8652.