Summary
Avian-to-human transmission of highly pathogenic avian influenza viruses (HPAIV) and
their subsequent adaptation to humans are of great concern to public health. Surveillance
and early warning of AIVs with the potential to infect humans and pandemic potential
is crucial. In this study, we determined whether adaptive evolution occurred in human-isolated
H5 viruses. We evaluated all available genomes of H5N1 and H5N6 avian influenza A
virus. Firstly, we systematically identified several new mutations in H5 AIV that
might be associated with human adaptation using a combination of novel comparative
phylogenetic methods and structural analysis. Some changes are the result of parallel
evolution, further demonstrating their importance. In total, we identified 102 adaptive
evolution sites in eight genes. Some residues had been previously identified, such
as 227 in HA and 627 in PB2, while others have not been reported so far. Ten sites
from four genes evolved in parallel but no obvious positive selection was detected.
Our study suggests that during infection of humans, H5 viruses evolved to adapt to
their new host environment and that the sites of adaptive/parallel evolution might
play a role in crossing the species barrier and are the response to new selection
pressure. The results provide insight to implement early detection systems for transitional
stages in H5 AIV evolution before its potential adaptation for humans.
Author summary line
The prerequisite of surveillance and early warning of avian influenza viruses with
the potential to infect humans depends on the identification of human-adaptation related
mutations. In this study, we used a novel approach combining both phylogenetic and
structural analysis to identify possible human-adaptation related mutations in H5
AIVs. Previous studies reported human-adaptation related mutations and some novel
mutations exhibiting parallel evolution. Our result provides new insights into how
AIVs adapt to humans by point mutations.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic and PersonalCorporate R&D ProfessionalsOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Journal of InfectionAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- A pandemic warning?.Nature. 1997; 389: 554
- Epidemiology, evolution, and recent outbreaks of avian influenza virus in china.J Virol. 2015; 89: 8671-8676
- Silent spread of H5N1 in vaccinated poultry.Nature. 2006; 442: 757
- Experimental challenge of chicken vaccinated with commercially available H5 vaccines reveals loss of protection to some highly pathogenic avian influenza H5N1 strains circulating in hong kong/china.Vaccine. 2013; 31: 3536-3542
- Vaccination of domestic ducks against H5N1 HPAI: a review.Virus Res. 2013; 178: 21-34
- The development and genetic diversity of H5N1 influenza virus in china, 1996-2006.Virology. 2008; 380: 243-254
- Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses.PLoS Pathog. 2008; 4e1000161
- The evolution of H5N1 influenza viruses in ducks in southern china.Proc Natl Acad Sci USA. 2004; 101: 10452-10457
- H5N1 influenza viruses isolated from geese in southeastern china: evidence for genetic reassortment and interspecies transmission to ducks.Virology. 2002; 292: 16-23
- Genesis, evolution and prevalence of H5N6 avian influenza viruses in China.Cell Host Microbe. 2016; 20: 810-821
- Experimental adaptation of an influenza H5 ha confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets.Nature. 2012; 486: 420-428
- Airborne transmission of influenza A/H5N1 virus between ferrets.Science. 2012; 336: 1534-1541
- Transmission of influenza a viruses.Virology. 2015; 479–480: 234-246
- Receptor binding and pH stability – how influenza a virus hemagglutinin affects host-specific virus infection.Biochim Biophys Acta. 2014; 1838: 1153-1168
- Enabling the 'host jump': structural determinants of receptor-binding specificity in influenza a viruses.Nat Rev Microbiol. 2014; 12: 822-831
- The genetic causes of convergent evolution.Nat Rev Genet. 2013; 14: 751-764
- Probable limited person-to-person transmission of highly pathogenic avian influenza a (H5N1) virus in china.Lancet. 2008; 371: 1427-1434
- Probable person-to-person transmission of avian influenza a (H5N1).N Engl J Med. 2005; 352: 333-340
- Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.Bioinformatics. 2006; 22: 1658-1659
- CD-HIT: accelerated for clustering the next-generation sequencing data.Bioinformatics. 2012; 28: 3150-3152
- MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Nucleic Acids Res. 2002; 30: 3059-3066
- RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Bioinformatics. 2014; 30: 1312-1313
- How many bootstrap replicates are necessary?.J Comput Biol. 2010; 17: 337-354
- Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees.Nucleic Acids Res. 2016; 44: W242-W245
- BEAST: bayesian evolutionary analysis by sampling trees.BMC Evol Biol. 2007; 7: 214
- IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Mol Biol Evol. 2015; 32: 268-274
- PAML 4: phylogenetic analysis by maximum likelihood.Mol Biol Evol. 2007; 24: 1586-1591
- An airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level.Science. 2013; 340: 1463-1467
- Structures of influenza a virus RNA polymerase offer insight into viral genome replication.Nature. 2019; https://doi.org/10.1038/s41586-019-1530-7
- Structural insights into RNA synthesis by the influenza virus transcription-replication machine.Virus Res. 2017; : 103-117
- Evolution of the receptor binding phenotype of influenza a (H5) viruses.Virology. 2006; 344: 432-438
- Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses.Science. 2001; 293: 1840-1842
- The T160A hemagglutinin substitution affects not only receptor binding property but also transmissibility of H5N1 clade 2.3.4 avian influenza virus in guinea pigs.Vet Res. 2017; 48: 7
- An avian influenza H5N1 virus that binds to a human-type receptor.J Virol. 2007; 81: 9950
- Adaptive mutations in the H5N1 polymerase complex.Virus Res. 2013; 178: 53-62
- Parallel evolution of influenza across multiple spatiotemporal scales.Elife. 2017; 6: 16
- Novel polymerase gene mutations for human adaptation in clinical isolates of avian H5N1 influenza viruses.PLoS Pathog. 2016; 12e1005583
- Genetic characterization of seasonal influenza a (H3N2) viruses in ontario during 2010-2011 influenza season: high prevalence of mutations at antigenic sites.Influenza Other Respir Viruses. 2014; 8: 250-257
- Enhanced human receptor binding by H5 haemagglutinins.Virology. 2014; 456-457: 179-187
- A single amino acid in the PB2 gene of influenza a virus is a determinant of host range.J Virol. 1993; 67: 1761-1764
- Avian influenza a (H5N1) infection in humans.N Engl J Med. 2005; 353: 1374-1385
- Convergent evolution of human-isolated H7N9 avian influenza a viruses.J Infect Dis. 2018; 217: 1699-1707
- Large-scale sequence analysis reveals novel human-adaptive markers in PB2 segment of seasonal influenza a viruses.Emerg Microbes Infect. 2018; 7: 47
- Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model.J Virol. 2005; 79: 12058-12064
- Detection of convergent and parallel evolution at the amino acid sequence level.Mol Biol Evol. 1997; 14: 527-536
- Enhanced human-type receptor binding by ferret-transmissible H5N1 with a K193T mutation.J Virol. 2018; 92: 10
- Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus.Science. 2006; 312: 404-410
- Diversity of influenza A(H5N1) viruses in infected humans, northern vietnam, 2004-2010.Emerg Infect Dis. 2018; 24: 1128-1238
- Influenza virus RNA polymerase: insights into the mechanisms of viral RNA synthesis.Nat Rev Microbiol. 2016; 14: 479-493
- Species difference in anp32a underlies influenza a virus polymerase host restriction.Nature. 2016; 529: 101-104
- Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza virus in humans in the United Kingdom.J Virol. 2014; 88: 13269-13283
- Evolution and virulence of influenza a virus protein PB1-F2.Int J Mol Sci. 2017; 19: 15
- Biological fitness and natural selection of amantadine resistant variants of avian influenza H5N1 viruses.Virus Res. 2017; 228: 109-113
Article Info
Publication History
Published online: January 30, 2020
Accepted:
January 18,
2020
Identification
Copyright
© 2020 The British Infection Association. Published by Elsevier Ltd. All rights reserved.
