Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses

English version České info

Of the Orthomyxoviridae family of viruses, only influenza A viruses are thought to exist as multiple subtypes and has non-human maintenance hosts. In April 2011, nasal swabs were collected for virus isolation from pigs exhibiting influenza-like illness. Subsequent electron microscopic, biochemical, and genetic studies identified an orthomyxovirus with seven RNA segments exhibiting approximately 50% overall amino acid identity to human influenza C virus. Based on its genetic organizational similarities to influenza C viruses this virus has been provisionally designated C/Oklahoma/1334/2011 (C/OK). Phylogenetic analysis of the predicted viral proteins found that the divergence between C/OK and human influenza C viruses was similar to that observed between influenza A and B viruses. No cross reactivity was observed between C/OK and human influenza C viruses using hemagglutination inhibition (HI) assays. Additionally, screening of pig and human serum samples found that 9.5% and 1.3%, respectively, of individuals had measurable HI antibody titers to C/OK virus. C/OK virus was able to infect both ferrets and pigs and transmit to naive animals by direct contact. Cell culture studies showed that C/OK virus displayed a broader cellular tropism than a human influenza C virus. The observed difference in cellular tropism was further supported by structural analysis showing that hemagglutinin esterase (HE) proteins between two viruses have conserved enzymatic but divergent receptor-binding sites. These results suggest that C/OK virus represents a new subtype of influenza C viruses that currently circulates in pigs that has not been recognized previously. The presence of multiple subtypes of co-circulating influenza C viruses raises the possibility of reassortment and antigenic shift as mechanisms of influenza C virus evolution.

Vyšlo v časopise: Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses. PLoS Pathog 9(2): e32767. doi:10.1371/journal.ppat.1003176
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003176

Souhrn

Zdroje

1. Palese P, Shaw ML (2007) Orthomyxoviridae: The viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology, Fifth Edition. Philadelphia: Lippincott Williams & Wilkins. pp. 1647–1690.

2. MatsuzakiY, KatsushimaN, NagaiY, ShojiM, ItagakiT, et al. (2006) Clinical features of influenza C virus infection in children. J Infect Dis 193: 1229–1235.

3. GouarinS, VabretA, DinaJ, PetitjeanJ, BrouardJ, et al. (2008) Study of influenza C virus infection in France. J Med Virol 80: 1441–1446.

4. AntόnA, MarcosMA, CodonerFM, de MolinaP, MartinezA, et al. (2011) Influenza C virus surveillance during the first influenza A (H1N1) 2009 pandemic wave in Catalonia, Spain. Diagn Microbiol Infect Dis 69: 419–427.

5. MatsuzakiY, AbikoC, MizutaK, SugawaraK, TakashitaE, et al. (2007) A nationwide epidemic of influenza C virus infection in Japan in 2004. J Clin Microbiol 45: 783–788.

6. MatsuzakiY, MizutaK, SugawaraK, TsuchiyaE, MurakiY, et al. (2003) Frequent reassortment among influenza C viruses. J Virol 77: 871–881.

7. MurakiY, HongoS, SugawaraK, KitameF, NakamuraK (1996) Evolution of the hemagglutinin esterase gene of influenza C. J Gen Virol 77: 673–679.

8. TscherneDM, García-SastreA (2011) Virulence determinants of pandemic influenza viruses. J Clin Med 121: 6–12.

9. WebsterR, BeanWJ, GormanOT, ChambersTM, KawaokaY (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56: 152–179.

10. TongS, LiY, RivaillerP, ConrardyC, Alvarez CastilloDA, et al. (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 109: 4269–4274.

11. GuoYJ, FengenGJ, PingW, MinW, JimingZ (1983) Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus. J Gen Virol 64: 177–182.

12. KimuraH, AbikoC, PengG, MurakiY, SugawaraK, et al. (1997) Interspecies transmission of influenza C virus between humans and pigs. Virus Res 48: 71–79.

13. YuanjiG, DesselbergerU (1984) Genome analysis of influenza C viruses isolated in 1981/82 from pigs in China. J Gen Virol 65: 1857–1872.

14. YamaokaM, HottaH, ItohM, HommaM (1991) Prevalence of antibody to influenza C virus among pigs in Hyogo prefecture Japan. J Gen Virol 72: 711–714.

15. BrownIH, HarrisPA, AlexanderDJ (1995) Serological studies of influenza viruses in pigs in Great Britain 1991–2. Epidemiol Infect 114: 511–520.

16. HarmonK, BowerL, KimWI, PentellaM, YoonKJ (2010) A matrix gene-based multiplex real-time PCR for detection and differentiation of 2009 pandemic H1N1 and other influenza A viruses in North America. Influenza Other Respi Viruses 4: 405–410.

17. CoirasMT, Pérez-BrenaP, GarcíaML, CasasI (2003) Simultaneous detection of influenza A, B, and C viruses, respiratory syncytial virus and adenoviruses in clinical samples by multiplex reverse transcription nested-PCR assay. J Med Virol 69: 132–144.

18. YamashitaM, KrystalM, PaleseP (1989) Comparison of the three large polymerase proteins of influenza A, B, and C viruses. Virology 171: 458–466.

19. YamashitaM, KrystalM, PaleseP (1988) Evidence that the matrix protein of influenza C virus is coded for by a spliced mRNA. J Virol 62: 3348–3355.

20. SugawaraK, NishimuraH, HongoS, KitameF, NakamuraK (1991) Antigenic characterization of the nucleoprotein and matrix protein of influenza C virus with monoclonal antibodies. J Gen Virol 72: 103–109.

21. MurakiY, HongoS (2010) The molecular virology and reverse genetics of influenza C virus. Jpn J Infect Dis 63: 157–165.

22. DesselbergerU, RacanielloVR, ZazraJJ, PaleseP (1980) The 3′ and 5′-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8: 315–328.

23. ZhengH, PaleseP, García-SastreA (1996) Nonconserved nucleotides at the 3′ and 5′ ends of an influenza A virus RNA play an important role in viral RNA replication. Virology 217: 242–251.

24. LeeY-S, SeongBL (1998) Nucleotides in the panhandle structure of the influenza B virus virion RNA are involved in the specificity between influenza A and B viruses. J Gen Virol 79: 673–681.

25. HsuMT, ParvinJD, GuptaS, KrystalM, PaleseP (1987) Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci USA 84: 8140–8144.

26. GaoQ, PaleseP (2009) Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci USA 106: 15891–15896.

27. Crescenzo-ChaigneB, BarbezangeC, van der WerfS (2008) Non coding extremities of the seven influenza virus type C vRNA segments: effects on transcription and replication by the type C and type A polymerase complexes. Virol J 5: 132.

28. MatsuzakiY, MurakiY, SugawaraK, HongoS, NishimuraH, et al. (1994) Cocirculation of two distinct groups of influenza C virus in Yamagata City, Japan. Virology 202: 796–802.

29. MatsuzakiY, TakaoS, ShimadaS, MizutaK, SugawaraK, et al. (2004) Characterization of antigenically and genetically similar influenza C viruses isolated in Japan during the 1999–2000 season. Epidemiol Infect 132: 709–720.

30. PengG, HongoS, KimuraH, MurakiY, SugawaraK, et al. (1996) Frequent occurrence of genetic reassortment between influenza C virus strains in nature. J Gen Virol 77: 1489–1492.

31. MarcelinG, BlandHM, NegovetichNJ, SandbulteMR, EllebedyAH, et al. (2010) Inactivated seasonal influenza vaccines increase serum antibodies to the neuraminidase of pandemic influenza A(H1N1) 2009 virus in an age-dependent manner. J Infect Dis 202: 1634–1638.

32. ManuguerraJ-C, HannounC, SaenzMDC, VillarE, CabezasJA (1994) Sero-epidemiological survey of influenza C virus infection in Spain. Eur J Epidemiol 10: 91–94.

33. RiserBL, MaassabHF (1990) Differential interaction of virulent and attenuated influenza virus strains with ferret alveolar macrophages: possible role in pathogenicity. J Infect Dis 161: 699–705.

34. Crescenzo-ChaigneB, van der WerfS (2007) Rescue of influenza C virus from recombinant DNA. J Virol 81: 11282–11289.

35. RogersGN, HerrlerG, PaulsonJC, KlenkHD (1986) Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J Biol Chem 261: 5947–5951.

36. RosenthalPB, ZhangX, FormanowskiF, FitzW, WongCH, et al. (1998) Structure of the hemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396: 92–96.

37. HerrlerGR, RottR, KlenkHD, MullerHP, ShuklaK, et al. (1985) The receptor-destroying enzyme of influenza C virus is a neuraminidase-O-acetylesterase. EMBO 4: 1503–1506.

38. MainesTR, JayaramanA, BelserJA, WadfordDA, PappasC, et al. (2009) Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325: 484–487.

39. ScholtissekC, BürgerH, KistnerO, ShortridgeKF (1985) The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147: 287–294.

40. WangQ, ChengF, LuM, TianX, MaJ (2008) Crystal structure of unaligned influenza B virus hemagglutinin. J Virol 82: 3011–3020.

41. WangQ, TianX, ChenX, MaJ (2007) Structural basis for receptor specificity of influenza B virus hemagglutinin. Proc Natl Acad Sci 104: 16874–16879.

42. ZengQH, LangereisMA, van VlietALW, HuizingaEG, de GrootRJ (2008) Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci USA 105: 9065–9069.

43. LangereisMA, ZengQH, HeestersB, HuizingaEG, de GrootRJ (2012) The murine coronavirus hemagglutinin-esterase receptor binding site: A major shift in ligand specificity through modest changes in architecture. PLoS Pathog 8(1): e1002492.

44. HensleySE, DasSR, BaileyAL, SchmidtLM, HickmanHD, et al. (2009) Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326: 734–736.

45. BuonagurioDA, NakadaS, FitchWM, PaleseP (1986) Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology 153: 12–21.

46. BuonagurioDA, NakadaS, DesselbergerU, KrystalM, PaleseP (1985) Noncumulative sequence changes in the hemagglutinin genes of influenza C virus isolates. Virology 146: 221–232.

47. GathererD (2010) Tempo and mode in the molecular evolution of influenza C. PLoS Curr 2: RRN1199.

48. YamashitaM, KrystalM, FitchWM, PaleseP (1988) Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology 163: 112–122.

49. Kawaoka Y, Cox NJ, Haller O, et al.. (2005) Infectious salmon anemia virus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, editors. Virus Taxonomy. Classification and Nomenclature of Viruses: Eighth Report of the International Committee on Taxonomy of Viruses. New York: Elsevier, Academic Press. pp. 681–693.

50. PrestiRM, ZhaoG, BeattyWL, MihindukulasuriyaKA, da RosaAP, et al. (2009) Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol 83: 11599–11606.

51. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Bio Evol 28: 2731–2739.

52. WHO (2002) WHO Manual on Animal Influenza Diagnosis and Surveillance, 2002. Available: http://whqlibdoc.who.int/hq/2002/WHO_CDS_CSR_NCS_2002.5.pdf.

53. ReumanPD, KeelyS, SchiffGM (1989) Assessment of signs of influenza illness in the ferret model. J Virol Methods 24: 27–34.

54. EswarN, WebbB, Marti-RenomMA, MadhusudhanMS, EramianD, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5.6.

55. EisenbergD, LuthyR, BowieJU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277: 396–404.

56. BakerNA, SeptD, JosephS, HolstMJ, McCammonJA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037–10041.

57. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

58. BuchanDW, WardSM, LobleyAE, NugentTC, BrysonK, et al. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res 38: W563–W568.