A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses
Abstract
The H1 subtype of influenza A viruses (IAVs) has been circulating in swine since the 1918 human influenza pandemic. Over time, and aided by further introductions from nonswine hosts, swine H1 viruses have diversified into three genetic lineages. Due to limited global data, these H1 lineages were named based on colloquial context, leading to a proliferation of inconsistent regional naming conventions. In this study, we propose rigorous phylogenetic criteria to establish a globally consistent nomenclature of swine H1 virus hemagglutinin (HA) evolution. These criteria applied to a data set of 7,070 H1 HA sequences led to 28 distinct clades as the basis for the nomenclature. We developed and implemented a web-accessible annotation tool that can assign these biologically informative categories to new sequence data. The annotation tool assigned the combined data set of 7,070 H1 sequences to the correct clade more than 99% of the time. Our analyses indicated that 87% of the swine H1 viruses from 2010 to the present had HAs that belonged to 7 contemporary cocirculating clades. Our nomenclature and web-accessible classification tool provide an accurate method for researchers, diagnosticians, and health officials to assign clade designations to HA sequences. The tool can be updated readily tomore »
- Authors:
-
- Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
- Bioinformatics Institute, University of Auckland, Auckland, New Zealand
- Department of Zoology, University of Cambridge, Cambridge, United Kingdom
- J. Craig Venter Institute, La Jolla, California, USA, Department of Pathology, University of California, San Diego, California, USA
- Laboratory of Virology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
- Animal and Plant Health Agency, Weybridge, United Kingdom
- National Veterinary Services Laboratories, USDA-APHIS, Ames, Iowa, USA
- ANSES, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France
- Division of Transboundary Animal Disease, National Institute of Animal Health, National Agriculture and Food Research Organization, Ibaraki, Japan
- Canadian Food Inspection Agency, National Centre for Foreign Animal Disease, Winnipeg, Manitoba, Canada
- Embrapa Swine and Poultry, Animal Health and Genetic Laboratory, Concórdia, SC, Brazil
- Instituto de Patobiología, CICVyA INTA, Hurlingham, Buenos Aires, Argentina
- Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
- Department of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, Tennessee, USA
- Publication Date:
- Research Org.:
- Oak Ridge Associated Univ., Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1618366
- Alternate Identifier(s):
- OSTI ID: 1626157
- Grant/Contract Number:
- AC05-06OR23100
- Resource Type:
- Published Article
- Journal Name:
- mSphere
- Additional Journal Information:
- Journal Name: mSphere Journal Volume: 1 Journal Issue: 6; Journal ID: ISSN 2379-5042
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Microbiology; H1N1; H1N2; influenza A virus; molecular epidemiology; nomenclature; swine; virus evolution
Citation Formats
Anderson, Tavis K., Macken, Catherine A., Lewis, Nicola S., Scheuermann, Richard H., Van Reeth, Kristien, Brown, Ian H., Swenson, Sabrina L., Simon, Gaëlle, Saito, Takehiko, Berhane, Yohannes, Ciacci-Zanella, Janice, Pereda, Ariel, Davis, C. Todd, Donis, Ruben O., Webby, Richard J., Vincent, Amy L., and Lowen, ed., Anice C. A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses. United States: N. p., 2016.
Web. doi:10.1128/mSphere.00275-16.
Anderson, Tavis K., Macken, Catherine A., Lewis, Nicola S., Scheuermann, Richard H., Van Reeth, Kristien, Brown, Ian H., Swenson, Sabrina L., Simon, Gaëlle, Saito, Takehiko, Berhane, Yohannes, Ciacci-Zanella, Janice, Pereda, Ariel, Davis, C. Todd, Donis, Ruben O., Webby, Richard J., Vincent, Amy L., & Lowen, ed., Anice C. A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses. United States. https://doi.org/10.1128/mSphere.00275-16
Anderson, Tavis K., Macken, Catherine A., Lewis, Nicola S., Scheuermann, Richard H., Van Reeth, Kristien, Brown, Ian H., Swenson, Sabrina L., Simon, Gaëlle, Saito, Takehiko, Berhane, Yohannes, Ciacci-Zanella, Janice, Pereda, Ariel, Davis, C. Todd, Donis, Ruben O., Webby, Richard J., Vincent, Amy L., and Lowen, ed., Anice C. Wed .
"A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses". United States. https://doi.org/10.1128/mSphere.00275-16.
@article{osti_1618366,
title = {A Phylogeny-Based Global Nomenclature System and Automated Annotation Tool for H1 Hemagglutinin Genes from Swine Influenza A Viruses},
author = {Anderson, Tavis K. and Macken, Catherine A. and Lewis, Nicola S. and Scheuermann, Richard H. and Van Reeth, Kristien and Brown, Ian H. and Swenson, Sabrina L. and Simon, Gaëlle and Saito, Takehiko and Berhane, Yohannes and Ciacci-Zanella, Janice and Pereda, Ariel and Davis, C. Todd and Donis, Ruben O. and Webby, Richard J. and Vincent, Amy L. and Lowen, ed., Anice C.},
abstractNote = {The H1 subtype of influenza A viruses (IAVs) has been circulating in swine since the 1918 human influenza pandemic. Over time, and aided by further introductions from nonswine hosts, swine H1 viruses have diversified into three genetic lineages. Due to limited global data, these H1 lineages were named based on colloquial context, leading to a proliferation of inconsistent regional naming conventions. In this study, we propose rigorous phylogenetic criteria to establish a globally consistent nomenclature of swine H1 virus hemagglutinin (HA) evolution. These criteria applied to a data set of 7,070 H1 HA sequences led to 28 distinct clades as the basis for the nomenclature. We developed and implemented a web-accessible annotation tool that can assign these biologically informative categories to new sequence data. The annotation tool assigned the combined data set of 7,070 H1 sequences to the correct clade more than 99% of the time. Our analyses indicated that 87% of the swine H1 viruses from 2010 to the present had HAs that belonged to 7 contemporary cocirculating clades. Our nomenclature and web-accessible classification tool provide an accurate method for researchers, diagnosticians, and health officials to assign clade designations to HA sequences. The tool can be updated readily to track evolving nomenclature as new clades emerge, ensuring continued relevance. A common global nomenclature facilitates comparisons of IAVs infecting humans and pigs, within and between regions, and can provide insight into the diversity of swine H1 influenza virus and its impact on vaccine strain selection, diagnostic reagents, and test performance, thereby simplifying communication of such data.},
doi = {10.1128/mSphere.00275-16},
journal = {mSphere},
number = 6,
volume = 1,
place = {United States},
year = {Wed Dec 28 00:00:00 EST 2016},
month = {Wed Dec 28 00:00:00 EST 2016}
}
https://doi.org/10.1128/mSphere.00275-16
Web of Science
Works referenced in this record:
Review of Influenza A Virus in Swine Worldwide: A Call for Increased Surveillance and Research
journal, April 2013
- Vincent, A.; Awada, L.; Brown, I.
- Zoonoses and Public Health, Vol. 61, Issue 1
Inference from Iterative Simulation Using Multiple Sequences
journal, November 1992
- Gelman, Andrew; Rubin, Donald B.
- Statistical Science, Vol. 7, Issue 4
Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States
journal, August 2015
- Rajão, Daniela S.; Gauger, Phillip C.; Anderson, Tavis K.
- Journal of Virology, Vol. 89, Issue 22
Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic
journal, June 2009
- Smith, Gavin J. D.; Vijaykrishna, Dhanasekaran; Bahl, Justin
- Nature, Vol. 459, Issue 7250
MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis
journal, August 2012
- Kumar, S.; Stecher, G.; Peterson, D.
- Bioinformatics, Vol. 28, Issue 20
Antigenic and Genetic Characteristics of Swine-Origin 2009 A(H1N1) Influenza Viruses Circulating in Humans
journal, May 2009
- Garten, R. J.; Davis, C. T.; Russell, C. A.
- Science, Vol. 325, Issue 5937
Enhanced pneumonia and disease in pigs vaccinated with an inactivated human-like (δ-cluster) H1N2 vaccine and challenged with pandemic 2009 H1N1 influenza virus
journal, March 2011
- Gauger, Phillip C.; Vincent, Amy L.; Loving, Crystal L.
- Vaccine, Vol. 29, Issue 15
The global antigenic diversity of swine influenza A viruses
journal, April 2016
- Lewis, Nicola S.; Russell, Colin A.; Langat, Pinky
- eLife, Vol. 5
Genetic Reassortment of Avian, Swine, and Human Influenza A Viruses in American Pigs
journal, October 1999
- Zhou, Nan Nan; Senne, Dennis A.; Landgraf, John S.
- Journal of Virology, Vol. 73, Issue 10
Genetic Reassortment between Avian and Human Influenza A Viruses in Italian Pigs
journal, March 1993
- Castrucci, Maria R.; Donatelli, Isabella; Sidoli, Luigi
- Virology, Vol. 193, Issue 1
European Surveillance Network for Influenza in Pigs: Surveillance Programs, Diagnostic Tools and Swine Influenza Virus Subtypes Identified in 14 European Countries from 2010 to 2013
journal, December 2014
- Simon, Gaëlle; Larsen, Lars E.; Dürrwald, Ralf
- PLoS ONE, Vol. 9, Issue 12
Antigenic and genetic diversity among swine influenza A H1N1 and H1N2 viruses in Europe
journal, April 2002
- Marozin, S.; Gregory, V.; Cameron, K.
- Journal of General Virology, Vol. 83, Issue 4
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Continual Reintroduction of Human Pandemic H1N1 Influenza A Viruses into Swine in the United States, 2009 to 2014
journal, April 2015
- Nelson, Martha I.; Stratton, Jered; Killian, Mary Lea
- Journal of Virology, Vol. 89, Issue 12
Pathogenesis and Vaccination of Influenza A Virus in Swine
book, January 2014
- Rajao, Daniela S.; Anderson, Tavis K.; Gauger, Phillip C.
- Influenza Pathogenesis and Control - Volume I
Detection of Influenza a Virus in Porcine Oral Fluid Samples
journal, March 2011
- Detmer, Susan E.; Patnayak, Devi P.; Jiang, Yin
- Journal of Veterinary Diagnostic Investigation, Vol. 23, Issue 2
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002
- Katoh, K.
- Nucleic Acids Research, Vol. 30, Issue 14
Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States
journal, July 2009
- Vincent, Amy L.; Ma, Wenjun; Lager, Kelly M.
- Virus Genes, Vol. 39, Issue 2
How Many Bootstrap Replicates Are Necessary?
journal, March 2010
- Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P.
- Journal of Computational Biology, Vol. 17, Issue 3
Swine Influenza
journal, September 1931
- Shope, Richard E.
- The Journal of Experimental Medicine, Vol. 54, Issue 3
Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012
journal, November 2013
- Anderson, Tavis K.; Nelson, Martha I.; Kitikoon, Pravina
- Influenza and Other Respiratory Viruses, Vol. 7
Influenza Research Database: An integrated bioinformatics resource for influenza virus research
journal, September 2016
- Zhang, Yun; Aevermann, Brian D.; Anderson, Tavis K.
- Nucleic Acids Research, Vol. 45, Issue D1
Novel Human-like Influenza A Viruses Circulate in Swine in Mexico and Chile
journal, January 2015
- Nelson, Martha; Culhane, Marie R.; Rovira, Albert
- PLoS Currents
Persistence of Hong Kong influenza virus variants in pigs
journal, June 1977
- Shortridge, K.; Webster, R.; Butterfield, W.
- Science, Vol. 196, Issue 4297
Molecular Epidemiology and Evolution of Influenza Viruses Circulating within European Swine between 2009 and 2013
journal, July 2015
- Watson, Simon J.; Langat, Pinky; Reid, Scott M.
- Journal of Virology, Vol. 89, Issue 19
Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010
- Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
- 2010 Gateway Computing Environments Workshop (GCE)
Toward a Unified Nomenclature System for Highly Pathogenic Avian Influenza Virus (H5N1)
journal, July 2008
- ,
- Emerging Infectious Diseases, Vol. 14, Issue 7, p. e1-e1
Reassortment of Pandemic H1N1/2009 Influenza A Virus in Swine
journal, June 2010
- Vijaykrishna, D.; Poon, L. L. M.; Zhu, H. C.
- Science, Vol. 328, Issue 5985
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009
- Schloss, P. D.; Westcott, S. L.; Ryabin, T.
- Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
Global migration of influenza A viruses in swine
journal, March 2015
- Nelson, Martha I.; Viboud, Cécile; Vincent, Amy L.
- Nature Communications, Vol. 6, Issue 1
Efficacy in Pigs of Inactivated and Live Attenuated Influenza Virus Vaccines against Infection and Transmission of an Emerging H3N2 Similar to the 2011-2012 H3N2v
journal, July 2013
- Loving, C. L.; Lager, K. M.; Vincent, A. L.
- Journal of Virology, Vol. 87, Issue 17
Influenza Research Database: an integrated bioinformatics resource for influenza research and surveillance: Influenza Research Database
journal, January 2012
- Squires, R. Burke; Noronha, Jyothi; Hunt, Victoria
- Influenza and Other Respiratory Viruses, Vol. 6, Issue 6
Antigenic drift in swine influenza H3 haemagglutinins with implications for vaccination policy
journal, March 1999
- Dejong, J.
- Vaccine, Vol. 17, Issue 11-12
Influenza A Viruses of Human Origin in Swine, Brazil
journal, August 2015
- Nelson, Martha I.; Schaefer, Rejane; Gava, Danielle
- Emerging Infectious Diseases, Vol. 21, Issue 8
Genetics, Evolution, and the Zoonotic Capacity of European Swine Influenza Viruses
book, January 2012
- Zell, Roland; Scholtissek, Christoph; Ludwig, Stephan
- Swine Influenza
Reverse zoonosis of influenza to swine: new perspectives on the human–animal interface
journal, March 2015
- Nelson, Martha I.; Vincent, Amy L.
- Trends in Microbiology, Vol. 23, Issue 3
Swine Influenza Virus Vaccines: To Change or Not to Change—That’s the Question
book, January 2012
- Van Reeth, Kristien; Ma, Wenjun
- Swine Influenza
Long-term evolution and transmission dynamics of swine influenza A virus
journal, May 2011
- Vijaykrishna, Dhanasekaran; Smith, Gavin J. D.; Pybus, Oliver G.
- Nature, Vol. 473, Issue 7348
Genetic Characterization of H1N1 and H1N2 Influenza A Viruses Circulating in Ontario Pigs in 2012
journal, June 2015
- Grgić, Helena; Costa, Marcio; Friendship, Robert M.
- PLOS ONE, Vol. 10, Issue 6
Hemagglutinin mutations related to antigenic variation in H1 swine influenza viruses.
journal, January 1992
- Luoh, S. M.; McGregor, M. W.; Hinshaw, V. S.
- Journal of Virology, Vol. 66, Issue 2
The impact of maternally derived immunity on influenza A virus transmission in neonatal pig populations
journal, January 2013
- Allerson, Matt; Deen, John; Detmer, Susan E.
- Vaccine, Vol. 31, Issue 3
Disease outbreaks in pigs in Great Britain due to an influenza A virus of H1N2 subtype
journal, April 1995
- Brown, I.; Chakraverty, P.; Harris, P.
- Veterinary Record, Vol. 136, Issue 13
pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree
journal, October 2010
- Matsen, Frederick A.; Kodner, Robin B.; Armbrust, E. Virginia
- BMC Bioinformatics, Vol. 11, Issue 1
Hemagglutinin of swine influenza virus: a single amino acid change pleiotropically affects viral antigenicity and replication.
journal, November 1983
- Both, G. W.; Shi, C. H.; Kilbourne, E. D.
- Proceedings of the National Academy of Sciences, Vol. 80, Issue 22
MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003
- Ronquist, Fredrik; Huelsenbeck, John P.
- Bioinformatics, Vol. 19, Issue 12, p. 1572-1574
Efficacy of commercial swine influenza vaccines against challenge with a recent European H1N1 field isolate
journal, July 2010
- Kyriakis, C. S.; Gramer, M. R.; Barbé, F.
- Veterinary Microbiology, Vol. 144, Issue 1-2
Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008
journal, December 2010
- Lorusso, A.; Vincent, A. L.; Harland, M. L.
- Journal of General Virology, Vol. 92, Issue 4
Co-circulation of avian H9N2 and human H3N2 viruses in pigs in southern China
journal, October 2001
- Peiris, J. S. M.; Guan, Y.; Ghose, P.
- International Congress Series, Vol. 1219
Characterization of co-circulating swine influenza A viruses in North America and the identification of a novel H1 genetic clade with antigenic significance
journal, April 2015
- Anderson, Tavis K.; Campbell, Brian A.; Nelson, Martha I.
- Virus Research, Vol. 201
Ranking viruses: measures of positional importance within networks define core viruses for rational polyvalent vaccine development
journal, April 2012
- Anderson, Tavis K.; Laegreid, William W.; Cerutti, Francesco
- Bioinformatics, Vol. 28, Issue 12