Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses
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,...
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| Published in | PLoS pathogens Vol. 9; no. 2; p. e1003176 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | 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. |
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| AbstractList | 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.
Influenza C viruses infect most humans during childhood. Unlike influenza A viruses, influenza C viruses exhibit little genetic variability and evolve at a comparably slower rate. Influenza A viruses exist as multiple subtypes and cause disease in numerous mammals. In contrast, influenza C viruses are comprised of a single subtype in its primary human host. Here we characterize a novel swine influenza virus, C/swine/Oklahoma/1334/2011 (C/OK), having only modest genetic similarity to human influenza C viruses. No cross-reaction was observed between C/OK and human influenza C viruses. Antibodies that cross react with C/OK were identified in a significant number of swine but not human sera samples, suggesting that C/OK circulates in pigs. Additionally, we show that C/OK is capable of infecting and transmitting by direct contact in both pigs and ferrets. These results suggest that C/OK represents a new subtype of influenza C viruses. This is significant, as co-circulation of multiple subtypes of influenza allows for rapid viral evolution through antigenic shift, a property previously only shown for influenza A viruses. The ability of C/OK to infect ferrets along with the absence of antibodies to C/OK in humans, suggests that such viruses may become a potential threat to human health. 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. Of the Orthomyxoviridae family of viruses, only influenza A viruses are thought to exist as multiple subtypes and has nonhuman 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. 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.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. 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. |
| Audience | Academic |
| Author | Collin, Emily A. Webby, Richard J. Li, Feng Liu, Runxia Hause, Ben M. Chakravarty, Suvobrata Kaplan, Bryan Hoppe, Adam D. Sheng, Zizhang Ducatez, Mariette Simonson, Randy R. Armien, Anibal Ran, Zhiguang |
| AuthorAffiliation | 3 Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, United States of America 5 Department of Chemistry and Biochemistry, South Dakota State University, Brookings, South Dakota, United States of America Erasmus Medical Center, Netherlands 4 Department of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, United States of America 1 Newport Laboratories, Worthington, Minnesota, United States of America 2 Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, United States of America 6 Veterinary Diagnostic Laboratory, University of Minnesota, St. Paul, Minnesota, United States of America |
| AuthorAffiliation_xml | – name: 2 Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, South Dakota, United States of America – name: 4 Department of Biology and Microbiology, South Dakota State University, Brookings, South Dakota, United States of America – name: 6 Veterinary Diagnostic Laboratory, University of Minnesota, St. Paul, Minnesota, United States of America – name: 1 Newport Laboratories, Worthington, Minnesota, United States of America – name: 3 Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, United States of America – name: Erasmus Medical Center, Netherlands – name: 5 Department of Chemistry and Biochemistry, South Dakota State University, Brookings, South Dakota, United States of America |
| Author_xml | – sequence: 1 givenname: Ben M. surname: Hause fullname: Hause, Ben M. – sequence: 2 givenname: Mariette surname: Ducatez fullname: Ducatez, Mariette – sequence: 3 givenname: Emily A. surname: Collin fullname: Collin, Emily A. – sequence: 4 givenname: Zhiguang surname: Ran fullname: Ran, Zhiguang – sequence: 5 givenname: Runxia surname: Liu fullname: Liu, Runxia – sequence: 6 givenname: Zizhang surname: Sheng fullname: Sheng, Zizhang – sequence: 7 givenname: Anibal surname: Armien fullname: Armien, Anibal – sequence: 8 givenname: Bryan surname: Kaplan fullname: Kaplan, Bryan – sequence: 9 givenname: Suvobrata surname: Chakravarty fullname: Chakravarty, Suvobrata – sequence: 10 givenname: Adam D. surname: Hoppe fullname: Hoppe, Adam D. – sequence: 11 givenname: Richard J. surname: Webby fullname: Webby, Richard J. – sequence: 12 givenname: Randy R. surname: Simonson fullname: Simonson, Randy R. – sequence: 13 givenname: Feng surname: Li fullname: Li, Feng |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23408893$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-02651233$$DView record in HAL |
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| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Hause et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hause BM, Ducatez M, Collin EA, Ran Z, Liu R, et al. (2013) Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses. PLoS Pathog 9(2): e1003176. doi:10.1371/journal.ppat.1003176 Distributed under a Creative Commons Attribution 4.0 International License 2013 Hause et al 2013 Hause et al |
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| Keywords | Genome, Viral Humans Oklahoma Models, Molecular Molecular Sequence Data Host Specificity Male Swine Diseases Phylogeny Antibodies, Viral Ferrets Sequence Analysis, DNA Hemagglutination Inhibition Tests Influenzavirus C Animals Antigens, Viral Swine Base Sequence Hemagglutinins, Viral Orthomyxoviridae Infections Cell Culture Techniques Viral Fusion Proteins |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The authors have read the journal's policy and have the following conflicts: BMH, EAC and RRS are employed by Newport Laboratories, a company that produces swine influenza virus vaccines. This does not alter the authors' adherence to all the PLoS Journal policies on sharing data and materials. Conceived and designed the experiments: BMH RJW RRS FL. Performed the experiments: BMH MD EAC ZR RL ZS AA BK . Analyzed the data: BMH MD EAC ZR RL ZS AA BK SC ADH RJW FL. Contributed reagents/materials/analysis tools: AA SC ADH. Wrote the paper: BMH RJW ZS ADH FL. |
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| Snippet | 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... Of the Orthomyxoviridae family of viruses, only influenza A viruses are thought to exist as multiple subtypes and has nonhuman maintenance hosts. In April... 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... 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... |
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| SubjectTerms | Amino acids Animal biology Animals Antibodies, Viral - blood Antigens, Viral - immunology Base Sequence Binding sites Biology Cell culture Cell Culture Techniques Comparative analysis Evolution Experiments Ferrets Gammainfluenzavirus - genetics Gammainfluenzavirus - immunology Gammainfluenzavirus - isolation & purification Gammainfluenzavirus - ultrastructure Genome, Viral - genetics Health aspects Hemagglutination Inhibition Tests Hemagglutinins, Viral - genetics Hemagglutinins, Viral - metabolism Hogs Host Specificity Host-parasite relationships Human health and pathology Humans Influenza Life Sciences Male Microbiology and Parasitology Models, Molecular Molecular Sequence Data Oklahoma Orthomyxoviridae Infections - immunology Orthomyxoviridae Infections - transmission Orthomyxoviridae Infections - virology Pandemics Phylogeny Physiological aspects Proteins Santé publique et épidémiologie Sequence Analysis, DNA Structural analysis Swine Swine Diseases - immunology Swine Diseases - transmission Swine Diseases - virology Viral Fusion Proteins - genetics Viral Fusion Proteins - metabolism Viruses |
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| Title | Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses |
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