Novel flu viruses in bats and cattle: "Pushing the envelope" of influenza infection

Veterinary Sciences

Volumn 5, Issue 3, 2018, Pages

  Kuchipudi, Suresh V ^a   Nissly, Ruth H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Bats; Cattle; Influenza viruses; Orthomyxoviridae

Indexed keywords

EID: 85053615826     PISSN: None     EISSN: 23067381     Source Type: Journal    
DOI: 10.3390/vetsci5030071     Document Type: Review

References (76)

1. Potter, C.W. A history of influenza. J. Appl. Microbiol. 2001, 91, 572-579
2. Taubenberger, J.K.; Morens, D.M. 1918 Influenza: The mother of all pandemics. Emerg. Infect. Dis. 2006, 12, 15-22. [PubMed
3. Taubenberger, J.K. The origin and virulence of the 1918 'Spanish' influenza virus. Proc. Am. Philos. Soc. 2006, 150, 86-112
4. Paules, C.; Subbarao, K. Influenza. Lancet 2017, 390, 697-708
5. Saunders-Hastings, P.R.; Krewski, D. Reviewing the History of Pandemic Influenza: Understanding Patterns of Emergence and Transmission. Pathogens 2016, 5, 66
6. Crescenzo-Chaigne, B.; Barbezange, C.; van der Werf, S. Non coding extremities of the seven influenza virus type C vRNA segments: Effect on transcription and replication by the type C and type A polymerase complexes. Virol. J. 2008, 5, 132
7. Ran, Z.; Shen, H.; Lang, Y.; Kolb, E.A.; Turan, N.; Zhu, L.; Ma, J.; Bawa, B.; Liu, Q.; Liu, H.; et al. Domestic pigs are susceptible to infection with influenza B viruses. J. Virol. 2015, 89, 4818-4826
8. Zambon, M.C. Epidemiology and pathogenesis of influenza. J. Antimicrob. Chemother. 1999, 44 (Suppl. B), 3-9
9. Webster, R.G.; Hinshaw, V.S.; Laver, W.G. Selection and analysis of antigenic variants of the neuraminidase of N2 influenza viruses with monoclonal antibodies. Virology 1982, 117, 93-104
10. Garten, R.J.; Davis, C.T.; Russell, C.A.; Shu, B.; Lindstrom, S.; Balish, A.; Sessions, W.M.; Xu, X.; Skepner, E.; Deyde, V.; et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325, 197-201
11. Kawaoka, Y.; Krauss, S.; Webster, R.G. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J. Virol. 1989, 63, 4603-4608
12. Li, C.; Hatta, M.;Watanabe, S.; Neumann, G.; Kawaoka, Y. Compatibility among polymerase subunit proteins is a restricting factor in reassortment between equine H7N7 and human H3N2 influenza viruses. J. Virol. 2008, 82, 11880-11888
13. Gerber, M.; Isel, C.; Moules, V.; Marquet, R. Selective packaging of the influenza A genome and consequences for genetic reassortment. Trends Microbiol. 2014, 22, 446-455
14. Goto, H.; Muramoto, Y.; Noda, T.; Kawaoka, Y. The genome-packaging signal of the influenza A virus genome comprises a genome incorporation signal and a genome-bundling signal. J. Virol. 2013, 87, 11316-11322
15. Fournier, E.; Moules, V.; Essere, B.; Paillart, J.C.; Sirbat, J.D.; Cavalier, A.; Rolland, J.P.; Thomas, D.; Lina, B.; Isel, C.; et al. Interaction network linking the human H3N2 influenza A virus genomic RNA segments. Vaccine 2012, 30, 7359-7367
16. Fournier, E.; Moules, V.; Essere, B.; Paillart, J.C.; Sirbat, J.D.; Isel, C.; Cavalier, A.; Rolland, J.P.; Thomas, D.; Lina, B.; et al. A supramolecular assembly formed by influenza A virus genomic RNA segments. Nucleic Acids Res. 2012, 40, 2197-2209
17. Gavazzi, C.; Isel, C.; Fournier, E.; Moules, V.; Cavalier, A.; Thomas, D.; Lina, B.; Marquet, R. An in vitro network of intermolecular interactions between viral RNA segments of an avian H5N2 influenza A virus: Comparison with a human H3N2 virus. Nucleic Acids Res. 2013, 41, 1241-1254
18. Gavazzi, C.; Yver, M.; Isel, C.; Smyth, R.P.; Rosa-Calatrava, M.; Lina, B.; Moules, V.; Marquet, R. A functional sequence-specific interaction between influenza A virus genomic RNA segments. Proc. Natl. Acad. Sci. USA 2013, 110, 16604-16609
19. Cauldwell, A.V.; Long, J.S.; Moncorge, O.; Barclay,W.S. Viral determinants of influenza A virus host range. J. Gen. Virol. 2014, 95, 1193-1210
20. Jeong, O.M.; Kim, M.C.; Kim, M.J.; Kang, H.M.; Kim, H.R.; Kim, Y.J.; Joh, S.J.; Kwon, J.H.; Lee, Y.J. Experimental infection of chickens, ducks and quails with the highly pathogenic H5N1 avian influenza virus. J. Vet. Sci. 2009, 10, 53-60
21. Nelli, R.K.; Dunham, S.P.; Kuchipudi, S.V.; White, G.A.; Baquero-Perez, B.; Chang, P.; Ghaemmaghami, A.; Brookes, S.M.; Brown, I.H.; Chang, K.C. Mammalian innate resistance to highly pathogenic avian influenza H5N1 virus infection is mediated through reduced proinflammation and infectious virus release. J. Virol. 2012, 86, 9201-9210
22. Parrish, C.R.; Murcia, P.R.; Holmes, E.C. Influenza virus reservoirs and intermediate hosts: Dogs, horses, and new possibilities for influenza virus exposure of humans. J. Virol. 2015, 89, 2990-2994
23. Fiorentini, L.; Taddei, R.; Moreno, A.; Gelmetti, D.; Barbieri, I.; De Marco, M.A.; Tosi, G.; Cordioli, P.; Massi, P. Influenza A pandemic (H1N1) 2009 virus outbreak in a cat colony in Italy. Zoonoses Public Health 2011, 58, 573-581
24. Hatta,M.; Zhong, G.; Gao, Y.; Nakajima, N.; Fan, S.; Chiba, S.; Deering, K.M.; Ito,M.; Imai,M.; Kiso,M.; et al. Characterization of a Feline Influenza A(H7N2) Virus. Emerg. Infect. Dis. 2018, 24, 75-86
25. Song, D.; Kim, H.; Na,W.; Hong, M.; Park, S.J.; Moon, H.; Kang, B.; Lyoo, K.S.; Yeom, M.; Jeong, D.G.; et al. Canine susceptibility to human influenza viruses (A/pdm 09H1N1, A/H3N2 and B). J. Gen. Virol. 2015, 96, 254-258
26. Kuchipudi, S.V.; Tellabati, M.; Sebastian, S.; Londt, B.Z.; Jansen, C.; Vervelde, L.; Brookes, S.M.; Brown, I.H.; Dunham, S.P.; Chang, K.C. Highly pathogenic avian influenza virus infection in chickens but not ducks is associated with elevated host immune and pro-inflammatory responses. Vet. Res. 2014, 45, 118
27. Puryear, W.B.; Keogh, M.; Hill, N.; Moxley, J.; Josephson, E.; Davis, K.R.; Bandoro, C.; Lidgard, D.; Bogomolni, A.; Levin, M.; et al. Prevalence of influenza A virus in live-captured North Atlantic gray seals: A possible wild reservoir. Emerg. Microbes Infect. 2016, 5, e81
28. Tong, S.; Li, Y.; Rivailler, P.; Conrardy, C.; Castillo, D.A.; Chen, L.M.; Recuenco, S.; Ellison, J.A.; Davis, C.T.; York, I.A.; et al. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 2012, 109, 4269-4274
29. Tong, S.; Zhu, X.; Li, Y.; Shi, M.; Zhang, J.; Bourgeois, M.; Yang, H.; Chen, X.; Recuenco, S.; Gomez, J.; et al. New world bats harbor diverse influenza A viruses. PLoS Pathog. 2013, 9, e1003657
30. Smith, I.;Wang, L.F. Bats and their virome: An important source of emerging viruses capable of infecting humans. Curr. Opin. Virol. 2013, 3, 84-91
31. Memish, Z.A.; Mishra, N.; Olival, K.J.; Fagbo, S.F.; Kapoor, V.; Epstein, J.H.; Alhakeem, R.; Durosinloun, A.; Al Asmari, M.; Islam, A.; et al. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg. Infect. Dis. 2013, 19, 1819-1823
32. Brook, C.E.; Dobson, A.P. Bats as 'special' reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015, 23, 172-180
33. Quan, P.L.; Firth, C.; Conte, J.M.; Williams, S.H.; Zambrana-Torrelio, C.M.; Anthony, S.J.; Ellison, J.A.; Gilbert, A.T.; Kuzmin, I.V.; Niezgoda, M.; et al. Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc. Natl. Acad. Sci. USA 2013, 110, 8194-8199
34. Moreira, E.A.; Locher, S.; Kolesnikova, L.; Bolte, H.; Aydillo, T.; Garcia-Sastre, A.; Schwemmle, M.; Zimmer, G. Synthetically derived bat influenza A-like viruses reveal a cell type-but not species-specific tropism. Proc. Natl. Acad. Sci. USA 2016
35. Juozapaitis, M.; Aguiar Moreira, E.; Mena, I.; Giese, S.; Riegger, D.; Pohlmann, A.; Hoper, D.; Zimmer, G.; Beer, M.; Garcia-Sastre, A.; et al. An infectious bat-derived chimeric influenza virus harbouring the entry machinery of an influenza A virus. Nat. Commun. 2014, 5, 4448
36. Zhou, B.; Ma, J.; Liu, Q.; Bawa, B.; Wang, W.; Shabman, R.S.; Duff, M.; Lee, J.; Lang, Y.; Cao, N.; et al. Characterization of uncultivable bat influenza virus using a replicative synthetic virus. PLoS Pathog. 2014, 10, e1004420
37. Yang, J.; Lee, J.; Ma, J.; Lang, Y.; Nietfeld, J.; Li, Y.; Duff, M.; Li, Y.; Yang, Y.; Liu, H.; et al. Pathogenicity of modified bat influenza virus with different M genes and its reassortment potential with swine influenza A virus. J. Gen. Virol. 2017, 98, 577-584
38. Noronha, J.M.; Liu, M.; Squires, R.B.; Pickett, B.E.; Hale, B.G.; Air, G.M.; Galloway, S.E.; Takimoto, T.; Schmolke, M.; Hunt, V.; et al. Influenza virus sequence feature variant type analysis: Evidence of a role for NS1 in influenza virus host range restriction. J. Virol. 2012, 86, 5857-5866
39. Hale, B.G. Conformational plasticity of the influenza A virus NS1 protein. J. Gen. Virol. 2014, 95, 2099-2105
40. Turkington, H.L.; Juozapaitis, M.; Tsolakos, N.; Corrales-Aguilar, E.; Schwemmle, M.; Hale, B.G. Unexpected Functional Divergence of Bat Influenza Virus NS1 Proteins. J. Virol. 2018, 92, JVI-02097
41. Li, Q.; Sun, X.; Li, Z.; Liu, Y.; Vavricka, C.J.; Qi, J.; Gao, G.F. Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc. Natl. Acad. Sci. USA 2012, 109, 18897-18902
42. Sun, X.; Shi, Y.; Lu, X.; He, J.; Gao, F.; Yan, J.; Qi, J.; Gao, G.F. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 2013, 3, 769-778
43. Freidl, G.S.; Binger, T.; Muller, M.A.; de Bruin, E.; van Beek, J.; Corman, V.M.; Rasche, A.; Drexler, J.F.; Sylverken, A.; Oppong, S.K.; et al. Serological evidence of influenza A viruses in frugivorous bats from Africa. PLoS ONE 2015, 10, e0127035
44. Poole, D.S.; Yu, S.; Cai, Y.; Dinis, J.M.; Muller, M.A.; Jordan, I.; Friedrich, T.C.; Kuhn, J.H. Influenza A virus polymerase is a site for adaptive changes during experimental evolution in bat cells. J. Virol. 2014, 88, 12572-12585
45. Kuchipudi, S.V.; Nelli, R.; White, G.A.; Bain, M.; Chang, K.C.; Dunham, S. Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. J. Mol. Genet. Med. 2009, 3, 143-151
46. Lakadamyali, M.; Rust, M.J.; Zhuang, X. Endocytosis of influenza viruses. Microbes Infect. 2004, 6, 929-936
47. Nelli, R.K.; Kuchipudi, S.V.;White, G.A.; Perez, B.B.; Dunham, S.P.; Chang, K.-C. Comparative distribution of human and avian type sialic acid influenza receptors in the pig. BMC Vet. Res. 2010, 6, 1-9
48. Chothe, S.K.; Bhushan, G.; Nissly, R.H.; Yeh, Y.T.; Brown, J.; Turner, G.; Fisher, J.; Sewall, B.J.; Reeder, D.M.; Terrones, M.; et al. Avian and human influenza virus compatible sialic acid receptors in little brown bats. Sci. Rep. 2017, 7, 660
49. Hause, B.M.; Ducatez, M.; Collin, E.A.; Ran, Z.; Liu, R.; Sheng, Z.; Armien, A.; Kaplan, B.; Chakravarty, S.; Hoppe, A.D.; et al. Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses. PLoS Pathog. 2013, 9, e1003176
50. Hause, B.M.; Collin, E.A.; Liu, R.; Huang, B.; Sheng, Z.; Lu,W.;Wang, D.; Nelson, E.A.; Li, F. Characterization of a novel influenza virus in cattle and Swine: Proposal for a new genus in the Orthomyxoviridae family. mBio 2014, 5, e00031-14
51. Ducatez, M.F.; Pelletier, C.; Meyer, G. Influenza D virus in cattle, France, 2011-2014. Emerg. Infect. Dis. 2015, 21, 368-371
52. Chiapponi, C.; Faccini, S.; De Mattia, A.; Baioni, L.; Barbieri, I.; Rosignoli, C.; Nigrelli, A.; Foni, E. Detection of Influenza D Virus among Swine and Cattle, Italy. Emerg. Infect. Dis. 2016, 22, 352-354
53. Zhai, S.L.; Zhang, H.; Chen, S.N.; Zhou, X.; Lin, T.; Liu, R.; Lv, D.H.;Wen, X.H.;Wei,W.K.;Wang, D.; et al. Influenza D Virus in Animal Species in Guangdong Province, Southern China. Emerg. Infect. Dis. 2017, 23, 1392-1396
54. Murakami, S.; Endoh, M.; Kobayashi, T.; Takenaka-Uema, A.; Chambers, J.K.; Uchida, K.; Nishihara, M.; Hause, B.; Horimoto, T. Influenza D Virus Infection in Herd of Cattle, Japan. Emerg. Infect. Dis. 2016, 22, 1517-1519
55. Flynn, O.; Gallagher, C.; Mooney, J.; Irvine, C.; Ducatez, M.; Hause, B.; McGrath, G.; Ryan, E. Influenza D Virus in Cattle, Ireland. Emerg. Infect. Dis. 2018, 24, 389-391
56. Salem, E.; Cook, E.A.J.; Lbacha, H.A.; Oliva, J.; Awoume, F.; Aplogan, G.L.; Hymann, E.C.; Muloi, D.; Deem, S.L.; Alali, S.; et al. Serologic Evidence for Influenza C and D Virus among Ruminants and Camelids, Africa, 1991-2015. Emerg. Infect. Dis. 2017, 23, 1556-1559
57. ICTV. Virus Taxonomy: 2017 Release. Available online: https://talk.ictvonline.org/ictv-reports/ictv_9th_report/ negative-sense-rna-viruses-2011/w/negrna_viruses/209/orthomyxoviridae (accessed on 5 August 2018)
58. ICTV. Virus Taxonomy: 2009 Release. Available online: https://talk.ictvonline.org/ictv-reports/ictv_9th_report/ negative-sense-rna-viruses-2011/w/negrna_viruses/209/orthomyxoviridae (accessed on 5 August 2018)
59. Ferguson, L.; Olivier, A.K.; Genova, S.; Epperson,W.B.; Smith, D.R.; Schneider, L.; Barton, K.; McCuan, K.; Webby, R.J.;Wan, X.F. Pathogenesis of Influenza D Virus in Cattle. J. Virol. 2016, 90, 5636-5642
60. Song, H.; Qi, J.; Khedri, Z.; Diaz, S.; Yu, H.; Chen, X.; Varki, A.; Shi, Y.; Gao, G.F. An Open Receptor-Binding Cavity of Hemagglutinin-Esterase-Fusion Glycoprotein from Newly-Identified Influenza D Virus: Basis for Its Broad Cell Tropism. PLoS Pathog. 2016, 12, e1005411
61. Mitra, N.; Cernicchiaro, N.; Torres, S.; Li, F.; Hause, B.M. Metagenomic characterization of the virome associated with bovine respiratory disease in feedlot cattle identified novel viruses and suggests an etiologic role for influenza D virus. J. Gen. Virol. 2016, 97, 1771-1784
62. Ng, T.F.; Kondov, N.O.; Deng, X.; Van Eenennaam, A.; Neibergs, H.L.; Delwart, E. A metagenomics and case-control study to identify viruses associated with bovine respiratory disease. J. Virol. 2015, 89, 5340-5349. 63. Hilton, W.M. BRD in 2014: Where have we been, where are we now, and where do we want to go? Anim. Health Res. Rev. 2014, 15, 120-122
63. Hilton, W.M. BRD in 2014: Where have we been, where are we now, and where do we want to go?. Anim. Health Res. Rev. 2014;15:120-122
64. Portis, E.; Lindeman, C.; Johansen, L.; Stoltman, G. A ten-year (2000-2009) study of antimicrobial susceptibility of bacteria that cause bovine respiratory disease complex-Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni-In the United States and Canada. J. Vet. Diagn. Investig. 2012, 24, 932-944
65. Nickell, J.S.; White, B.J. Metaphylactic antimicrobial therapy for bovine respiratory disease in stocker and feedlot cattle. Vet. Clin. N. Am. Food Anim. Pract. 2010, 26, 285-301
66. Mosier, D. Review of BRD pathogenesis: The old and the new. Anim. Health Res. Rev. 2014, 15, 166-168
67. Duff, G.C.; Galyean, M.L. Board-invited review: Recent advances in management of highly stressed, newly received feedlot cattle. J. Anim. Sci. 2007, 85, 823-840
68. White, S.K.;Ma,W.;McDaniel, C.J.; Gray, G.C.; Lednicky, J.A. Serologic evidence of exposure to influenza D virus among persons with occupational contact with cattle. J. Clin. Virol. 2016, 81, 31-33
69. Longdon, B.; Brockhurst, M.A.; Russell, C.A.;Welch, J.J.; Jiggins, F.M. The evolution and genetics of virus host shifts. PLoS Pathog. 2014, 10, e1004395
70. Davies, T.J.; Pedersen, A.B. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc. Biol. Sci. 2008, 275, 1695-1701
71. Hadfield, J.D.; Krasnov, B.R.; Poulin, R.; Nakagawa, S. A tale of two phylogenies: Comparative analyses of ecological interactions. Am. Nat. 2014, 183, 174-187
72. Woolhouse, M.E.; Haydon, D.T.; Antia, R. Emerging pathogens: The epidemiology and evolution of species jumps. Trends Ecol. Evol. 2005, 20, 238-244
73. Woolhouse, M.E.; Gowtage-Sequeria, S. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 2005, 11, 1842-1847
74. Woolhouse, M.; Scott, F.; Hudson, Z.; Howey, R.; Chase-Topping, M. Human viruses: Discovery and emergence. Philos. Trans R. Soc. 2012, 367, 2864-2871
75. Imai, M.; Watanabe, T.; Hatta, M.; Das, S.C.; Ozawa, M.; Shinya, K.; Zhong, G.; Hanson, A.; Katsura, H.; Watanabe, S.; et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486, 420-428
76. Watanabe, Y.; Ibrahim, M.S.; Ellakany, H.F.; Kawashita, N.; Mizuike, R.; Hiramatsu, H.; Sriwilaijaroen, N.; Takagi, T.; Suzuki, Y.; Ikuta, K. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog. 2011, 7, e1002068