DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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 » 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.« less

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11];  [12];  [13];  [13];  [14];  [1];
  1. Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
  2. Bioinformatics Institute, University of Auckland, Auckland, New Zealand
  3. Department of Zoology, University of Cambridge, Cambridge, United Kingdom
  4. J. Craig Venter Institute, La Jolla, California, USA, Department of Pathology, University of California, San Diego, California, USA
  5. Laboratory of Virology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
  6. Animal and Plant Health Agency, Weybridge, United Kingdom
  7. National Veterinary Services Laboratories, USDA-APHIS, Ames, Iowa, USA
  8. ANSES, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France
  9. Division of Transboundary Animal Disease, National Institute of Animal Health, National Agriculture and Food Research Organization, Ibaraki, Japan
  10. Canadian Food Inspection Agency, National Centre for Foreign Animal Disease, Winnipeg, Manitoba, Canada
  11. Embrapa Swine and Poultry, Animal Health and Genetic Laboratory, Concórdia, SC, Brazil
  12. Instituto de Patobiología, CICVyA INTA, Hurlingham, Buenos Aires, Argentina
  13. Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
  14. 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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mSphere.00275-16

Citation Metrics:
Cited by: 120 works
Citation information provided by
Web of Science

Save / Share:

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
  • DOI: 10.1111/zph.12049

Inference from Iterative Simulation Using Multiple Sequences
journal, November 1992


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
  • DOI: 10.1128/JVI.01675-15

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
  • DOI: 10.1038/nature08182

MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis
journal, August 2012


Antigenic and Genetic Characteristics of Swine-Origin 2009 A(H1N1) Influenza Viruses Circulating in Humans
journal, May 2009


The global antigenic diversity of swine influenza A viruses
journal, April 2016


Genetic Reassortment of Avian, Swine, and Human Influenza A Viruses in American Pigs
journal, October 1999


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
  • DOI: 10.1006/viro.1993.1155

Antigenic and genetic diversity among swine influenza A H1N1 and H1N2 viruses in Europe
journal, April 2002


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
  • DOI: 10.1093/molbev/mst010

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
  • DOI: 10.1128/JVI.00459-15

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
  • DOI: 10.1007/82_2014_391

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
  • DOI: 10.1177/104063871102300207

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002


Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States
journal, July 2009


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
  • DOI: 10.1089/cmb.2009.0179

Swine Influenza
journal, September 1931

  • Shope, Richard E.
  • The Journal of Experimental Medicine, Vol. 54, Issue 3
  • DOI: 10.1084/jem.54.3.373

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
  • DOI: 10.1111/irv.12193

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
  • DOI: 10.1093/nar/gkw857

Novel Human-like Influenza A Viruses Circulate in Swine in Mexico and Chile
journal, January 2015


Persistence of Hong Kong influenza virus variants in pigs
journal, June 1977


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
  • DOI: 10.1128/JVI.00840-15

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)
  • DOI: 10.1109/GCE.2010.5676129

Toward a Unified Nomenclature System for Highly Pathogenic Avian Influenza Virus (H5N1)
journal, July 2008


Reassortment of Pandemic H1N1/2009 Influenza A Virus in Swine
journal, June 2010


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
  • DOI: 10.1128/AEM.01541-09

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
  • DOI: 10.1038/ncomms7696

Influenza Research Database: an integrated bioinformatics resource for influenza research and surveillance: Influenza Research Database
journal, January 2012


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
  • DOI: 10.3201/eid2108.141891

Genetics, Evolution, and the Zoonotic Capacity of European Swine Influenza Viruses
book, January 2012

  • Zell, Roland; Scholtissek, Christoph; Ludwig, Stephan
  • Swine Influenza
  • DOI: 10.1007/82_2012_267

Reverse zoonosis of influenza to swine: new perspectives on the human–animal interface
journal, March 2015


Swine Influenza Virus Vaccines: To Change or Not to Change—That’s the Question
book, January 2012


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
  • DOI: 10.1038/nature10004

Genetic Characterization of H1N1 and H1N2 Influenza A Viruses Circulating in Ontario Pigs in 2012
journal, June 2015


Hemagglutinin mutations related to antigenic variation in H1 swine influenza viruses.
journal, January 1992


The impact of maternally derived immunity on influenza A virus transmission in neonatal pig populations
journal, January 2013


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
  • DOI: 10.1136/vr.136.13.328

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
  • DOI: 10.1186/1471-2105-11-538

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
  • DOI: 10.1073/pnas.80.22.6996

MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003


Efficacy of commercial swine influenza vaccines against challenge with a recent European H1N1 field isolate
journal, July 2010


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
  • DOI: 10.1099/vir.0.027557-0

Co-circulation of avian H9N2 and human H3N2 viruses in pigs in southern China
journal, October 2001


Ranking viruses: measures of positional importance within networks define core viruses for rational polyvalent vaccine development
journal, April 2012