A novel activation mechanism of avian influenza virus H9N2 by furin

Journal of Virology

Volumn 88, Issue 3, 2014, Pages 1673-1683

  Tse, Longping V ^a,b   Hamilton, Alice M ^a   Friling, Tamar ^a   Whittaker, Gary R ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FURIN; INFLUENZA VIRUS HEMAGGLUTININ; PROTEINASE;

AMINO ACID SEQUENCE; ARTICLE; CLEAVAGE SITE; ENZYME ACTIVATION; GLYCOSYLATION; HUMAN; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H7N1; INFLUENZA VIRUS A H9N2; MORBIDITY; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; RESTRICTION SITE; VIRUS ACTIVATION; VIRUS VIRULENCE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHICKENS; FURIN; GLYCOSYLATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; POULTRY DISEASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ALIGNMENT;

EID: 84892475040     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02648-13     Document Type: Article

References (55)

1. Homme PJ, Easterday BC. 1970. Avian influenza virus infections. I. Characteristics of influenza A/turkey/Wisconsin/1966 virus. Avian Dis. 14:66-74.
2. Capua I, Alexander DJ. 2009. Avian influenza infection in birds: a challenge and opportunity for the poultry veterinarian. Poult. Sci. 88:842-846. http://dx.doi.org/10.3382/ps.2008-00289.
3. Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP, Norwood M, Shortridge KF, Webster RG, Guan Y. 2000. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 267:279-288. http://dx.doi.org/10.1006/viro .1999.0115.
4. Negovetich NJ, Feeroz MM, Jones-Engel L, Walker D, Alam SM, Hasan K, Seiler P, Ferguson A, Friedman K, Barman S, Franks J, Turner J, Krauss S, Webby RJ, Webster RG. 2011. Live bird markets of Bangladesh: H9N2 viruses and the near absence of highly pathogenic H5N1 influenza. PLoS One 6:e19311. http://dx.doi.org/10.1371/journal.pone.0019311.
5. Alexander DJ. 2003. Report on avian influenza in the eastern hemisphere during 1997-2002. Avian Dis. 47:792-797. http://dx.doi.org/10.1637/0005-2086-47.s3.792.
6. Brown IH, Banks J, Manvell RJ, Essen SC, Shell W, Slomka M, Londt B, Alexander DJ. 2006. Recent epidemiology and ecology of influenza A viruses in avian species in Europe and the Middle East. Dev. Biol. (Basel) 124:45-50.
7. Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF. 1999. Human infection with influenza H9N2. Lancet 354: 916-917. http://dx.doi.org/10.1016/S0140-6736(99)03311-5.
8. Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS, Guan Y. 2005. Human infection with an avian H9N2 influenzaAvirus in Hong Kong in 2003. J. Clin. Microbiol. 43:5760-5767. http://dx.doi.org/10.1128/JCM.43.11.5760-5767.2005.
9. World Organization for Animal Health. 2008. Manual of diagnostic tests and vaccines for terrestrial animals, 6th ed. World Health Organization/ OIE, Geneva, Switzerland.
10. Lee CW, Song CS, Lee YJ, Mo IP, Garcia M, Suarez DL, Kim SJ. 2000. Sequence analysis of the hemagglutinin gene of H9N2 Korean avian influenza viruses and assessment of the pathogenic potential of isolate MS96. Avian Dis. 44:527-535. http://dx.doi.org/10.2307/1593091.
11. Banet-Noach C, Perk S, Simanov L, Grebenyuk N, Rozenblut E, Pokamunski S, Pirak M, Tendler Y, Panshin A. 2007. H9N2 influenza viruses from Israeli poultry: a five-year outbreak. Avian Dis. 51:290-296. http://dx.doi.org/10.1637/7590-040206R1.1.
12. Nili H, Asasi K. 2003. Avian influenza (H9N2) outbreak in Iran. Avian Dis. 47:828-831. http://dx.doi.org/10.1637/0005-2086-47.s3.828.
13. Xu KM, Li KS, Smith GJ, Li JW, Tai H, Zhang JX, Webster RG, Peiris JS, Chen H, Guan Y. 2007. Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. J. Virol. 81:2635-2645. http://dx.doi.org/10.1128/JVI.02316-06.
14. Lin YP, Shaw M, Gregory V, Cameron K, Lim W, Klimov A, Subbarao K, Guan Y, Krauss S, Shortridge K, Webster R, Cox N, Hay A. 2000. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc. Natl. Acad. Sci. U.S.A. 97:9654-9658. http://dx.doi.org/10.1073/pnas.160270697.
15. Zhang P, Tang Y, Liu X, Liu W, Zhang X, Liu H, Peng D, Gao S, Wu Y, Zhang L, Lu S. 2009. A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in eastern China since 1998. J. Virol. 83:8428-8438. http://dx.doi.org/10 .1128/JVI.00659-09.
16. Matrosovich MN, Krauss S, Webster RG. 2001. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281:156-162. http://dx.doi.org/10.1006/viro.2000.0799.
17. Abdel-Moneim AS, Afifi MA, El-Kady MF. 2012. Isolation and mutation trend analysis of influenza A virus subtype H9N2 in Egypt. Virol. J. 9:173. http://dx.doi.org/10.1186/1743-422X-9-173.
18. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569. http://dx.doi.org/10.1146/annurev.biochem.69.1.531.
19. Steinhauer DA. 1999. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258:1-20. http://dx.doi.org/10.1006/viro .1999.9716.
20. Klenk H-D, Garten W. 1994. Activation cleavage of viral spike proteins by host proteases, p 241-280. In Wimmer E (ed), Cellular receptors for animal viruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Kawaoka Y, Webster RG. 1988. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 85:324-328. http://dx.doi.org/10.1073/pnas .85.2.324.
22. Lee CW, Lee YJ, Senne DA, Suarez DL. 2006. Pathogenic potential of North American H7N2 avian influenza virus: a mutagenesis study using reverse genetics. Virology 353:388-395. http://dx.doi.org/10.1016/j.virol .2006.06.003.
23. Seidah NG, Mayer G, Zaid A, Rousselet E, Nassoury N, Poirier S, Essalmani R, Prat A. 2008. The activation and physiological functions of the proprotein convertases. Int. J. Biochem. Cell Biol. 40:1111-1125. http://dx.doi.org/10.1016/j.biocel.2008.01.030.
24. Shapiro J, Sciaky N, Lee J, Bosshart H, Angeletti RH, Bonifacino JS. 1997. Localization of endogenous furin in cultured cell lines. J. Histochem. Cytochem. 45:3-12. http://dx.doi.org/10.1177/002215549704500102.
25. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 101:6062-6067. http://dx.doi .org/10.1073/pnas.0400782101.
26. Werth N, Beerlage C, Rosenberger C, Yazdi AS, Edelmann M, Amr A, Bernhardt W, von Eiff C, Becker K, Schafer A, Peschel A, Kempf VA. 2010. Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS One 5:e11576. http://dx.doi.org/10.1371/journal.pone.0011576.
27. McMahon S, Grondin F, McDonald PP, Richard DE, Dubois CM. 2005. Hypoxia-enhanced expression of the proprotein convertase furin is mediated by hypoxia-inducible factor 1: impact on the bioactivation of proproteins. J. Biol. Chem. 280:6561-6569. http://dx.doi.org/10.1074/jbc.M413248200.
28. Izidoro MA, Gouvea IE, Santos JA, Assis DM, Oliveira V, Judice WA, Juliano MA, Lindberg I, Juliano L. 2009. A study of human furin specificity using synthetic peptides derived from natural substrates, and effects of potassium ions. Arch. Biochem. Biophys. 487:105-114. http://dx.doi .org/10.1016/j.abb.2009.05.013.
29. Thomas G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell. Biol. 3:753-766. http://dx .doi.org/10.1038/nrm934.
30. Krysan DJ, Rockwell NC, Fuller RS. 1999. Quantitative characterization of furin specificity. Energetics of substrate discrimination using an internally consistent set of hexapeptidyl methylcoumarinamides. J. Biol. Chem. 274:23229-23234.
31. Baron J, Tarnow C, Mayoli-Nussle D, Schilling E, Meyer D, Hammami M, Schwalm F, Steinmetzer T, Guan Y, Garten W, Klenk HD, Bottcher-Friebertshauser E. 2012. Matriptase, HAT, and TMPRSS2 activate the hemagglutinin of H9N2 influenza A viruses. J. Virol. 87:1811-1820. http://dx.doi.org/10.1128/JVI.02320-12.
32. Gohrbandt S, Veits J, Breithaupt A, Hundt J, Teifke JP, Stech O, Mettenleiter TC, Stech J. 2011. H9 avian influenza reassortant with engineered polybasic cleavage site displays a highly pathogenic phenotype in chicken. J. Gen. Virol. 92:1843-1853. http://dx.doi.org/10.1099/vir.0.031591-0.
33. Kawaoka Y, Naeve CW, Webster RG. 1984. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139:303-316. http://dx.doi.org/10.1016/0042-6822(84)90376-3.
34. Gibson CA, Daniels RS, Oxford JS, McCauley JW. 1992. Sequence analysis of the equine H7 influenza virus hemagglutinin gene. Virus Res. 22:93-106. http://dx.doi.org/10.1016/0168-1702(92)90037-A.
35. Hamilton BS, Sun X, Chung C, Whittaker GR. 2012. Acquisition of a novel eleven amino acid insertion directly N-terminal to a tetrabasic cleavage site confers intracellular cleavage of an H7N7 influenza virus hemagglutinin. Virology 434:88-95. http://dx.doi.org/10.1016/j.virol.2012.09 .004.
36. Spandidos A, Wang X, Wang H, Seed B. 2010. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 38:D792-D799. http://dx.doi.org/10 .1093/nar/gkp1005.
37. Spandidos A, Wang X, Wang H, Dragnev S, Thurber T, Seed B. 2008. A comprehensive collection of experimentally validated primers for polymerase chain reaction quantitation of murine transcript abundance.BMC Genomics 9:633. http://dx.doi.org/10.1186/1471-2164-9-633.
38. Wang X, Seed B. 2003. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 31:e154. http://dx.doi.org/10.1093/nar/gng154.
39. -ΔΔCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
40. Tian S, Huajun W, Wu J. 2012. Computational prediction of furin cleavage sites by a hybrid method and understanding mechanism underlying diseases. Sci. Rep. 2:261.
41. Golender N, Panshin A, Banet-Noach C, Nagar S, Pokamunski S, Pirak M, Tendler Y, Davidson I, Garcia M, Perk S. 2008. Genetic characterization of avian influenza viruses isolated in Israel during 2000-2006. Virus Genes 37:289-297. http://dx.doi.org/10.1007/s11262-008-0272-7.
42. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22:195-201. http://dx.doi.org/10.1093/bioinformatics/bti770.
43. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. 2009. The SWISSMODEL Repository and associated resources. Nucleic Acids Res. 37: D387-D392. http://dx.doi.org/10.1093/nar/gkn750.
44. Brown EG, Liu H, Kit LC, Baird S, Nesrallah M. 2001. Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc. Natl. Acad. Sci. U.S.A. 98:6883-6888. http://dx.doi.org/10.1073/pnas .111165798.
45. Pasick J, Handel K, Robinson J, Copps J, Ridd D, Hills K, Kehler H, Cottam-Birt C, Neufeld J, Berhane Y, Czub S. 2005. Intersegmental recombination between the haemagglutinin and matrix genes was responsible for the emergence of a highly pathogenic H7N3 avian influenza virus in British Columbia. J. Gen. Virol. 86:727-731. http://dx.doi.org/10.1099/vir.0.80478-0.
46. Perk S, Panshin A, Shihmanter E, Gissin I, Pokamunski S, Pirak M, Lipkind M. 2006. Ecology and molecular epidemiology of H9N2 avian influenza viruses isolated in Israel during 2000-2004 epizootic. Dev. Biol. (Basel) 124:201-209.
47. Tay FP, Huang M, Wang L, Yamada Y, Liu DX. 2012. Characterization of cellular furin content as a potential factor determining the susceptibility of cultured human and animal cells to coronavirus infectious bronchitis virus infection. Virology 433:421-430. http://dx.doi.org/10.1016/j.virol .2012.08.037.
48. Silvestri L, Pagani A, Camaschella C. 2008. Furin-mediated release of soluble hemojuvelin: a new link between hypoxia and iron homeostasis. Blood 111:924-931. http://dx.doi.org/10.1182/blood-2007-07-100677.
49. Tolnay AE, Baskin CR, Tumpey TM, Sabourin PJ, Sabourin CL, Long JP, Pyles JA, Albrecht RA, Garcia-Sastre A, Katze MG, Bielefeldt-Ohmann H. 2010. Extrapulmonary tissue responses in cynomolgus macaques (Macaca fascicularis) infected with highly pathogenic avian influenza A (H5N1) virus. Arch. Virol. 155:905-914. http://dx.doi.org/10.1007/s00705-010-0662-8.
50. Beerlage C, Greb J, Kretschmer D, Assaggaf M, Trackman PC, Hansmann ML, Bonin M, Eble JA, Peschel A, Brune B, Kempf VA. 2013. Hypoxia-inducible factor 1-regulated lysyl oxidase is involved in Staphylococcus aureus abscess formation. Infect. Immun. 81:2562-2573. http://dx.doi.org/10.1128/IAI.00302-13.
51. Kirienko NV, Kirienko DR, Larkins-Ford J, Wahlby C, Ruvkun G, Ausubel FM. 2013. Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death. Cell Host Microbe 13:406-416. http://dx.doi.org/10.1016/j.chom.2013.03.003.
52. Mosleh N, Dadras H, Mohammadi A. 2009. Molecular quantitation of H9N2 avian influenza virus in various organs of broiler chickens using TaqMan real-time PCR. J. Mol. Genet. Med. 3:152-157.
53. Hadipour MM, Farjadian SH, Azad F, Kamravan M, Dehghan A. 2011. Nephropathogenicity of H9N2 avian influenza virus in commercial broiler chickens following intratracheal inoculation. J. Anim. Vet. Adv. 10:1706-1710. http://dx.doi.org/10.3923/javaa.2011.1706.1710.
54. Pazani J, Marandi MV, Ashrafihelan J, Marjanmehr SH, Ghods F. 2008. Pathological studies of A/chicken/Tehran/ZMT-173/99 (H9N2) influenza virus in commercial broiler chickens of Iran. Int. J. Poult. Sci. 5:502-510.
55. Soda K, Asakura S, Okamatsu M, Sakoda Y, Kida H. 2011. H9N2 influenza virus acquires intravenous pathogenicity on the introduction of a pair of di-basic amino acid residues at the cleavage site of the hemagglutinin and consecutive passages in chickens. Virol. J. 8:64. http://dx.doi.org/10.1186/1743-422X-8-64.