Networks of genomic co-occurrence capture characteristics of human influenza A (H3N2) evolution.

The recent availability of full genomic sequence data for a large number of human influenza A (H3N2) virus isolates over many years provides us an opportunity to analyze human influenza virus evolution by considering all gene segments simultaneously. However, such analysis requires development of new computational models that can capture the complex evolutionary features over the entire genome. By analyzing nucleotide co-occurrence over the entire genome of human H3N2 viruses, we have developed a network model to describe H3N2 virus evolutionary patterns and dynamics. The network model effectively captures the evolutionary antigenic features of H3N2 virus at the whole-genome level and accurately describes the complex evolutionary patterns between individual gene segments. Our analyses show that the co-occurring nucleotide modules apparently underpin the dynamics of human H3N2 evolution and that amino acid substitutions corresponding to nucleotide co-changes cluster preferentially in known antigenic regions of the viral HA. Therefore, our study demonstrates that nucleotide co-occurrence networks represent a powerful method for tracking influenza A virus evolution and that cooperative genomic interaction is a major force underlying influenza virus evolution.

[1]  N. Slonim,et al.  Ab initio genotype–phenotype association reveals intrinsic modularity in genetic networks , 2006, Molecular systems biology.

[2]  W. Fitch,et al.  Positive Darwinian evolution in human influenza A viruses. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Hong Jin,et al.  Two residues in the hemagglutinin of A/Fujian/411/02-like influenza viruses are responsible for antigenic drift from A/Panama/2007/99. , 2005, Virology.

[4]  A. Lapedes,et al.  Mapping the Antigenic and Genetic Evolution of Influenza Virus , 2004, Science.

[5]  Andrew Rambaut,et al.  A phylogenetic method for detecting positive epistasis in gene sequences and its application to RNA virus evolution. , 2006, Molecular biology and evolution.

[6]  Christopher J. Lee,et al.  Distinguishing HIV-1 drug resistance, accessory, and viral fitness mutations using conditional selection pressure analysis of treated versus untreated patient samples , 2006, Biology Direct.

[7]  O. Pybus,et al.  Unifying the Epidemiological and Evolutionary Dynamics of Pathogens , 2004, Science.

[8]  Derek J Smith,et al.  Predictability and Preparedness in Influenza Control , 2006, Science.

[9]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[10]  E. Fodor,et al.  Influenza virus replication , 2002 .

[11]  Cecile Viboud,et al.  Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus , 2006, Biology Direct.

[12]  S. Wuchty,et al.  Evolutionary cores of domain co-occurrence networks , 2005, BMC Evolutionary Biology.

[13]  Yoshihiro Kawaoka,et al.  The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. , 2005, Annual review of microbiology.

[14]  J. Skehel,et al.  Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. , 2000, Annual review of biochemistry.

[15]  E. Nobusawa,et al.  Accumulation of Amino Acid Substitutions Promotes Irreversible Structural Changes in the Hemagglutinin of Human Influenza AH3 Virus during Evolution , 2005, Journal of Virology.

[16]  Jonathan Dushoff,et al.  Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Bruce T Lahn,et al.  Robust signals of coevolution of interacting residues in mammalian proteomes identified by phylogeny-aided structural analysis , 2005, Nature Genetics.

[18]  W. Fitch,et al.  Predicting the evolution of human influenza A. , 1999, Science.

[19]  N. Ferguson,et al.  Ecological and immunological determinants of influenza evolution , 2003, Nature.

[20]  Arthur Chun-Chieh Shih,et al.  Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution , 2007, Proceedings of the National Academy of Sciences.

[21]  Ron Shamir,et al.  EXPANDER – an integrative program suite for microarray data analysis , 2005, BMC Bioinformatics.

[22]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[23]  C. Naeve,et al.  Large-Scale Sequence Analysis of Avian Influenza Isolates , 2006, Science.

[24]  Bryan T Grenfell,et al.  Whole-Genome Analysis of Human Influenza A Virus Reveals Multiple Persistent Lineages and Reassortment among Recent H3N2 Viruses , 2005, PLoS biology.

[25]  Remis Balaniuk,et al.  Structural identification , 1997, Proceedings of the 1997 IEEE/RSJ International Conference on Intelligent Robot and Systems. Innovative Robotics for Real-World Applications. IROS '97.

[26]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[27]  M. Pereira,et al.  Influenza in the United Kingdom 1982–85 , 1986, Journal of Hygiene.

[28]  D. Pollock,et al.  Genomic biodiversity, phylogenetics and coevolution in proteins. , 2002, Applied bioinformatics.

[29]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[30]  C. Sander,et al.  Correlated mutations and residue contacts in proteins , 1994, Proteins.

[31]  I. Wilson,et al.  Structural basis of immune recognition of influenza virus hemagglutinin. , 1990, Annual review of immunology.

[32]  Y. Guan,et al.  Avian flu: H5N1 virus outbreak in migratory waterfowl , 2005, Nature.

[33]  Keiji Fukuda,et al.  Influenza-associated deaths among children in the United States, 2003-2004. , 2005, The New England journal of medicine.

[34]  Elizabeth C. Theil,et al.  Epochal Evolution Shapes the Phylodynamics of Interpandemic Influenza A (H3N2) in Humans , 2006, Science.

[35]  J. Skehel,et al.  Structural evidence for recognition of a single epitope by two distinct antibodies , 2000, Proteins.

[36]  M. Gerstein,et al.  Genomic analysis of regulatory network dynamics reveals large topological changes , 2004, Nature.

[37]  I. Wilson,et al.  Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation , 1981, Nature.

[38]  Anthony S. Fauci,et al.  Race against time , 2005, Nature.

[39]  S. Salzberg,et al.  Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution , 2005, Nature.

[40]  A. Osterhaus,et al.  Full restoration of viral fitness by multiple compensatory co-mutations in the nucleoprotein of influenza A virus cytotoxic T-lymphocyte escape mutants. , 2005, The Journal of general virology.

[41]  H. Klenk,et al.  Functional balance between haemagglutinin and neuraminidase in influenza virus infections , 2002, Reviews in medical virology.