Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family

ABSTRACT We have recently reported the isolation of a novel virus, provisionally designated C/swine/Oklahoma/1334/2011 (C/OK), with 50% overall homology to human influenza C viruses (ICV), from a pig in Oklahoma. Deep RNA sequencing of C/OK virus found a matrix 1 (M1) protein expression strategy tha...

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Autores principales:	Ben M. Hause, Emily A. Collin, Runxia Liu, Bing Huang, Zizhang Sheng, Wuxun Lu, Dan Wang, Eric A. Nelson, Feng Li
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8ea680540c014f2994dc97f75e31dfa8
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spelling	oai:doaj.org-article:8ea680540c014f2994dc97f75e31dfa82021-11-15T15:45:13ZCharacterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family10.1128/mBio.00031-142150-7511https://doaj.org/article/8ea680540c014f2994dc97f75e31dfa82014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00031-14https://doaj.org/toc/2150-7511ABSTRACT We have recently reported the isolation of a novel virus, provisionally designated C/swine/Oklahoma/1334/2011 (C/OK), with 50% overall homology to human influenza C viruses (ICV), from a pig in Oklahoma. Deep RNA sequencing of C/OK virus found a matrix 1 (M1) protein expression strategy that differed from that of ICV. The novelty of C/OK virus prompted us to investigate whether C/OK virus could exist in a nonswine species. Significantly, we found that C/OK virus was widespread in U.S. bovine herds, as demonstrated by reverse transcription (RT)-PCR and serological assays. Genome sequencing of three bovine viruses isolated from two herds in different states further confirmed these findings. To determine whether swine/bovine C/OK viruses can undergo reassortment with human ICV, and to clarify the taxonomic status of C/OK, in vitro reassortment and serological typing by agar gel immunodiffusion (AGID) were conducted. In vitro reassortment using two human ICV and two swine and bovine C/OK viruses demonstrated that human ICV and C/OK viruses were unable to reassort and produce viable progeny. Antigenically, no cross-recognition of detergent split virions was observed in AGID between human and nonhuman viruses by using polyclonal antibodies that were reactive to cognate antigens. Taken together, these results demonstrate that C/OK virus is genetically and antigenically distinct from ICV. The classification of the new virus in a separate genus of the Orthomyxoviridae family is proposed. The finding of C/OK virus in swine and bovine indicates that this new virus may spread and establish infection in other mammals, including humans. IMPORTANCE Influenza C viruses (ICV) are common human pathogens, infecting most people during childhood and adolescence, and typically cause mild respiratory symptoms. While ICV have been isolated from both pigs and dogs, humans are thought to be the natural viral reservoir. Previously, we characterized an ICV-like virus isolated from pigs exhibiting symptoms of influenza virus-like illness. Here, we show molecular and serological data demonstrating widespread circulation of similar viruses in bovines. Deep RNA sequencing, phylogenetic analysis, and in vitro reassortment experiments demonstrate that animal ICV-like viruses are genetically distinct from human ICV. Antigenically, we show that ICV-like viruses are not recognized by ICV antibodies. En masse, these results suggest that bovine influenza virus warrants classification as a new genus of influenza virus. The finding of this novel virus that can infect multiple mammalian species warrants further research into its role in human health.Ben M. HauseEmily A. CollinRunxia LiuBing HuangZizhang ShengWuxun LuDan WangEric A. NelsonFeng LiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ben M. Hause Emily A. Collin Runxia Liu Bing Huang Zizhang Sheng Wuxun Lu Dan Wang Eric A. Nelson Feng Li Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
description	ABSTRACT We have recently reported the isolation of a novel virus, provisionally designated C/swine/Oklahoma/1334/2011 (C/OK), with 50% overall homology to human influenza C viruses (ICV), from a pig in Oklahoma. Deep RNA sequencing of C/OK virus found a matrix 1 (M1) protein expression strategy that differed from that of ICV. The novelty of C/OK virus prompted us to investigate whether C/OK virus could exist in a nonswine species. Significantly, we found that C/OK virus was widespread in U.S. bovine herds, as demonstrated by reverse transcription (RT)-PCR and serological assays. Genome sequencing of three bovine viruses isolated from two herds in different states further confirmed these findings. To determine whether swine/bovine C/OK viruses can undergo reassortment with human ICV, and to clarify the taxonomic status of C/OK, in vitro reassortment and serological typing by agar gel immunodiffusion (AGID) were conducted. In vitro reassortment using two human ICV and two swine and bovine C/OK viruses demonstrated that human ICV and C/OK viruses were unable to reassort and produce viable progeny. Antigenically, no cross-recognition of detergent split virions was observed in AGID between human and nonhuman viruses by using polyclonal antibodies that were reactive to cognate antigens. Taken together, these results demonstrate that C/OK virus is genetically and antigenically distinct from ICV. The classification of the new virus in a separate genus of the Orthomyxoviridae family is proposed. The finding of C/OK virus in swine and bovine indicates that this new virus may spread and establish infection in other mammals, including humans. IMPORTANCE Influenza C viruses (ICV) are common human pathogens, infecting most people during childhood and adolescence, and typically cause mild respiratory symptoms. While ICV have been isolated from both pigs and dogs, humans are thought to be the natural viral reservoir. Previously, we characterized an ICV-like virus isolated from pigs exhibiting symptoms of influenza virus-like illness. Here, we show molecular and serological data demonstrating widespread circulation of similar viruses in bovines. Deep RNA sequencing, phylogenetic analysis, and in vitro reassortment experiments demonstrate that animal ICV-like viruses are genetically distinct from human ICV. Antigenically, we show that ICV-like viruses are not recognized by ICV antibodies. En masse, these results suggest that bovine influenza virus warrants classification as a new genus of influenza virus. The finding of this novel virus that can infect multiple mammalian species warrants further research into its role in human health.
format	article
author	Ben M. Hause Emily A. Collin Runxia Liu Bing Huang Zizhang Sheng Wuxun Lu Dan Wang Eric A. Nelson Feng Li
author_facet	Ben M. Hause Emily A. Collin Runxia Liu Bing Huang Zizhang Sheng Wuxun Lu Dan Wang Eric A. Nelson Feng Li
author_sort	Ben M. Hause
title	Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
title_short	Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
title_full	Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
title_fullStr	Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
title_full_unstemmed	Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family
title_sort	characterization of a novel influenza virus in cattle and swine: proposal for a new genus in the <italic toggle="yes">orthomyxoviridae</italic> family
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/8ea680540c014f2994dc97f75e31dfa8
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Characterization of a Novel Influenza Virus in Cattle and Swine: Proposal for a New Genus in the <italic toggle="yes">Orthomyxoviridae</italic> Family

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