Dynamic PB2-E627K substitution of influenza H7N9 virus indicates the in vivo genetic tuning and rapid host adaptation.

Adaptation, Biological / genetics Amino Acid Substitution / genetics High-Throughput Nucleotide Sequencing Host-Pathogen Interactions Humans Influenza A Virus, H7N9 Subtype / genetics Influenza, Human / virology RNA, Viral / genetics RNA-Dependent RNA Polymerase / genetics Sequence Analysis, RNA Viral Proteins / genetics Virus Replication / genetics
H7N9 virus PB2-627 dynamic substitution host adaptation next-generation sequencing

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
22 09 2020
Historique:
pubmed: 3 9 2020
medline: 18 11 2020
entrez: 3 9 2020
Statut: ppublish

Résumé

Avian-origin influenza viruses overcome the bottleneck of the interspecies barrier and infect humans through the evolution of variants toward more efficient replication in mammals. The dynamic adaptation of the genetic substitutions and the correlation with the virulence of avian-origin influenza virus in patients remain largely elusive. Here, based on the one-health approach, we retrieved the original virus-positive samples from patients with H7N9 and their surrounding poultry/environment. The specimens were directly deep sequenced, and the subsequent big data were integrated with the clinical manifestations. Unlike poultry/environment-derived samples with the consistent dominance of avian signature 627E of H7N9 polymerase basic protein 2 (PB2), patient specimens had diverse ratios of mammalian signature 627K, indicating the rapid dynamics of H7N9 adaptation in patients during the infection process. In contrast, both human- and poultry/environment-related viruses had constant dominance of avian signature PB2-701D. The intrahost dynamic adaptation was confirmed by the gradual replacement of 627E by 627K in H7N9 in the longitudinally collected specimens from one patient. These results suggest that host adaptation for better virus replication to new hosts, termed "genetic tuning," actually occurred in H7N9-infected patients in vivo. Notably, our findings also demonstrate the correlation between rapid host adaptation of H7N9 PB2-E627K and the fatal outcome and disease severity in humans. The feature of H7N9 genetic tuning in vivo and its correlation with the disease severity emphasize the importance of testing for the evolution of this avian-origin virus during the course of infection.

Identifiants

DOI: 10.1073/pnas.2013267117 PMID: 32873642 PMC: PMC7519270
pubmed: 32873642
pii: 2013267117
doi: 10.1073/pnas.2013267117
pmc: PMC7519270
doi:

Substances chimiques

PB2 protein, Influenzavirus A 0
RNA, Viral 0
Viral Proteins 0
RNA-Dependent RNA Polymerase EC 2.7.7.48

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

23807-23814

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

Competing interest statement: T.J., L. Li., G.L., and H.J. were employees of BGI-Shenzhen during the project.

Références

Cell Host Microbe. 2015 Mar 11;17(3):309-319
pubmed: 25704008
Lancet. 2013 Jun 1;381(9881):1916-25
pubmed: 23623390
PLoS Pathog. 2010 Aug 05;6(8):e1001034
pubmed: 20700447
Lancet Infect Dis. 2017 Aug;17(8):822-832
pubmed: 28583578
J Virol. 2015 Dec 09;90(5):2240-53
pubmed: 26656717
Infect Genet Evol. 2017 Nov;55:269-276
pubmed: 28943407
Front Med. 2013 Sep;7(3):275-6
pubmed: 23888377
Lancet. 2013 Jun 1;381(9881):1926-32
pubmed: 23643111
J Virol. 2009 May;83(10):5278-81
pubmed: 19264775
Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21312-6
pubmed: 19995968
J Virol. 2014 Jun;88(11):5977-86
pubmed: 24623411
Emerg Infect Dis. 2019 Dec;25(12):2215-2225
pubmed: 31742536
Sci Rep. 2016 Feb 05;6:19933
pubmed: 26847414
N Engl J Med. 2013 May 16;368(20):1888-97
pubmed: 23577628
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Trends Microbiol. 2017 Sep;25(9):713-728
pubmed: 28734617
J Virol. 2009 Nov;83(21):11102-15
pubmed: 19692471
PLoS Pathog. 2009 Jan;5(1):e1000252
pubmed: 19119420
J Infect Dis. 2014 Feb 15;209(4):551-6
pubmed: 23990570
Sci Rep. 2015 Jan 27;5:8039
pubmed: 25623817
Sci China Life Sci. 2013 Jun;56(6):485-92
pubmed: 23657795
Science. 2014 Apr 18;344(6181):235
pubmed: 24744345
Emerg Microbes Infect. 2019;8(1):1157-1167
pubmed: 31373538
J Virol. 2014 Mar;88(6):3568-76
pubmed: 24403592
Sci China Life Sci. 2018 Sep;61(9):1123-1126
pubmed: 29995198
Protein Cell. 2010 May;1(5):459-67
pubmed: 21203961
J Virol. 2013 Oct;87(19):10884-8
pubmed: 23864613
J Virol. 2015 Jan;89(1):2-13
pubmed: 25320305
Nature. 2016 Jan 7;529(7584):101-4
pubmed: 26738596
Emerg Infect Dis. 2016 Apr;22(4):598-607
pubmed: 26982379
Nat Commun. 2015 Jun 17;6:7491
pubmed: 26082035
Genome Res. 2010 Feb;20(2):265-72
pubmed: 20019144
J Biol Chem. 2011 Mar 25;286(12):10439-48
pubmed: 21216958
Nat Commun. 2014 Nov 20;5:5509
pubmed: 25409547
J Virol. 2014 Feb;88(3):1694-702
pubmed: 24257603
Curr Opin Virol. 2014 Apr;5:91-7
pubmed: 24705093
J Virol. 1993 Apr;67(4):1761-4
pubmed: 8445709
PLoS Pathog. 2019 Jul 2;15(7):e1007919
pubmed: 31265471
Cell Host Microbe. 2016 Dec 14;20(6):810-821
pubmed: 27916476
J Virol. 2014 Jul;88(14):8153-65
pubmed: 24807722
N Engl J Med. 2013 Jun 13;368(24):2337-9
pubmed: 23697471
Arch Virol. 2001 Dec;146(12):2275-89
pubmed: 11811679
mBio. 2011 Aug 16;2(4):
pubmed: 21846828
Nat Struct Mol Biol. 2007 Mar;14(3):229-33
pubmed: 17310249
J Virol. 2001 Jun;75(11):5398-404
pubmed: 11333924
J Virol. 2015 Oct;89(19):9939-51
pubmed: 26202239
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
J Am Chem Soc. 2015 Dec 9;137(48):15122-34
pubmed: 26424125
Sci Rep. 2015 Sep 22;5:14170
pubmed: 26391278
Clin Infect Dis. 2019 Mar 19;68(7):1100-1109
pubmed: 30124826
Cell. 2018 Mar 8;172(6):1157-1159
pubmed: 29522735
J Biol Chem. 2011 Oct 7;286(40):34504-13
pubmed: 21816827
Science. 2001 Sep 7;293(5536):1840-2
pubmed: 11546875
Virol J. 2019 Jan 8;16(1):3
pubmed: 30621708
J Gen Virol. 2000 May;81(Pt 5):1283-91
pubmed: 10769071
Biosaf Health. 2019 Sep;1(2):56-58
pubmed: 32501443
Infect Genet Evol. 2016 Jan;37:8-13
pubmed: 26477933

Auteurs

William J Liu (WJ)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China.
NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 102206 Beijing, China.

Jun Li (J)

Hangzhou Center for Disease Control and Prevention, 310021 Hangzhou, China.

Rongrong Zou (R)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China.

Jingcao Pan (J)

Hangzhou Center for Disease Control and Prevention, 310021 Hangzhou, China.

Tao Jin (T)

BGI-Shenzhen, 518083 Shenzhen, China.
China National GeneBank, BGI-Shenzhen, 518083 Shenzhen, China.

Liqiang Li (L)

BGI-Shenzhen, 518083 Shenzhen, China.
ORCID: 0000-0003-0180-7052

Peipei Liu (P)

NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 102206 Beijing, China.

Yingze Zhao (Y)

NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 102206 Beijing, China.

Xinfen Yu (X)

Hangzhou Center for Disease Control and Prevention, 310021 Hangzhou, China.

Haoqiu Wang (H)

Hangzhou Center for Disease Control and Prevention, 310021 Hangzhou, China.

Guang Liu (G)

BGI-Shenzhen, 518083 Shenzhen, China.
China National GeneBank, BGI-Shenzhen, 518083 Shenzhen, China.

Hui Jiang (H)

BGI-Shenzhen, 518083 Shenzhen, China.
China National GeneBank, BGI-Shenzhen, 518083 Shenzhen, China.

Yuhai Bi (Y)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China.
CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, 100101 Beijing, China.
Center for Influenza Research and Early-Warning, Chinese Academy of Sciences, 100101 Beijing, China.

Lei Liu (L)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China.

Kwok-Yung Yuen (KY)

State Key Laboratory of Emerging Infectious Diseases and the HKU-Shenzhen Hospital, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China.

Yingxia Liu (Y)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China; yingxialiu@hotmail.com gaofu@chinacdc.cn.

George F Gao (GF)

Shenzhen Key Laboratory of Pathogen and Immunity, State Key Discipline of Infectious Diseases, Shenzhen Third People's Hospital, Second Hospital Affiliated to Southern University of Science and Technology, 518112 Shenzhen, China; yingxialiu@hotmail.com gaofu@chinacdc.cn.
NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 102206 Beijing, China.
CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, 100101 Beijing, China.
Center for Influenza Research and Early-Warning, Chinese Academy of Sciences, 100101 Beijing, China.
ORCID: 0000-0002-3869-615X

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Classifications MeSH

Recherchemedicale.com › Phénomènes biologiques › Adaptation biologique › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Phénomènes génétiques › Mutagenèse › Substitution d'acide aminé › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Séquençage nucléotidique à haut débit › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Phénomènes biologiques › Interactions hôte-microbes › Interactions hôte-pathogène › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Virus › Virus à ARN › Virus à ARN de polarité négative › Orthomyxoviridae › Influenzavirus A › Virus de la grippe A › Sous-type H7N9 du virus de la grippe A › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Maladies de l'appareil respiratoire › Infections de l'appareil respiratoire › Grippe humaine › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN viral › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › RNA nucleotidyltransferases › RNA replicase › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Analyse de séquence d'ARN › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines virales › Dynamic PB2-E627K substitution of influenza...
Recherchemedicale.com › Phénomènes microbiologiques › Phénomènes physiologiques viraux › Réplication virale › Dynamic PB2-E627K substitution of influenza...