Respiratory Disease following Viral Lung Infection Alters the Murine Gut Microbiota

Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying, characterizing, and understanding factors that initiate these changes. Despite their high prevalence, studies have only recently begun to investigate how...

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Published inFrontiers in immunology Vol. 9; p. 182
Main Authors Groves, Helen T, Cuthbertson, Leah, James, Phillip, Moffatt, Miriam F, Cox, Michael J, Tregoning, John S
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 12.02.2018
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Abstract Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying, characterizing, and understanding factors that initiate these changes. Despite their high prevalence, studies have only recently begun to investigate how viral lung infections have an impact on the gut microbiota. There is also considerable interest in whether the gut microbiota could be manipulated during vaccination to improve efficacy. In this highly controlled study, we aimed to establish the effect of viral lung infection on gut microbiota composition and the gut environment using mouse models of common respiratory pathogens respiratory syncytial virus (RSV) and influenza virus. This was then compared to the effect of live attenuated influenza virus (LAIV) vaccination. Both RSV and influenza virus infection resulted in significantly altered gut microbiota diversity, with an increase in and a concomitant decrease in phyla abundance. Although the increase in the phylum was consistent across several experiments, differences were observed at the family and operational taxonomic unit level. This suggests a change in gut conditions after viral lung infection that favors outgrowth but not individual families. No change in gut microbiota composition was observed after LAIV vaccination, suggesting that the driver of gut microbiota change is specific to live viral infection. Viral lung infections also resulted in an increase in fecal lipocalin-2, suggesting low-grade gut inflammation, and colonic Muc5ac levels. Owing to the important role that mucus plays in the gut environment, this may explain the changes in microbiota composition observed. This study demonstrates that the gut microbiota and the gut environment are altered following viral lung infections and that these changes are not observed during vaccination. Whether increased mucin levels and gut inflammation drive, or are a result of, these changes is still to be determined.
AbstractList Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying, characterizing, and understanding factors that initiate these changes. Despite their high prevalence, studies have only recently begun to investigate how viral lung infections have an impact on the gut microbiota. There is also considerable interest in whether the gut microbiota could be manipulated during vaccination to improve efficacy. In this highly controlled study, we aimed to establish the effect of viral lung infection on gut microbiota composition and the gut environment using mouse models of common respiratory pathogens respiratory syncytial virus (RSV) and influenza virus. This was then compared to the effect of live attenuated influenza virus (LAIV) vaccination. Both RSV and influenza virus infection resulted in significantly altered gut microbiota diversity, with an increase in Bacteroidetes and a concomitant decrease in Firmicutes phyla abundance. Although the increase in the Bacteroidetes phylum was consistent across several experiments, differences were observed at the family and operational taxonomic unit level. This suggests a change in gut conditions after viral lung infection that favors Bacteroidetes outgrowth but not individual families. No change in gut microbiota composition was observed after LAIV vaccination, suggesting that the driver of gut microbiota change is specific to live viral infection. Viral lung infections also resulted in an increase in fecal lipocalin-2, suggesting low-grade gut inflammation, and colonic Muc5ac levels. Owing to the important role that mucus plays in the gut environment, this may explain the changes in microbiota composition observed. This study demonstrates that the gut microbiota and the gut environment are altered following viral lung infections and that these changes are not observed during vaccination. Whether increased mucin levels and gut inflammation drive, or are a result of, these changes is still to be determined.
Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying, characterizing, and understanding factors that initiate these changes. Despite their high prevalence, studies have only recently begun to investigate how viral lung infections have an impact on the gut microbiota. There is also considerable interest in whether the gut microbiota could be manipulated during vaccination to improve efficacy. In this highly controlled study, we aimed to establish the effect of viral lung infection on gut microbiota composition and the gut environment using mouse models of common respiratory pathogens respiratory syncytial virus (RSV) and influenza virus. This was then compared to the effect of live attenuated influenza virus (LAIV) vaccination. Both RSV and influenza virus infection resulted in significantly altered gut microbiota diversity, with an increase in Bacteroidetes and a concomitant decrease in Firmicutes phyla abundance. Although the increase in the Bacteroidetes phylum was consistent across several experiments, differences were observed at the family and operational taxonomic unit level. This suggests a change in gut conditions after viral lung infection that favors Bacteroidetes outgrowth but not individual families. No change in gut microbiota composition was observed after LAIV vaccination, suggesting that the driver of gut microbiota change is specific to live viral infection. Viral lung infections also resulted in an increase in fecal lipocalin-2, suggesting low-grade gut inflammation, and colonic Muc5ac levels. Owing to the important role that mucus plays in the gut environment, this may explain the changes in microbiota composition observed. This study demonstrates that the gut microbiota and the gut environment are altered following viral lung infections and that these changes are not observed during vaccination. Whether increased mucin levels and gut inflammation drive, or are a result of, these changes is still to be determined.
Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying, characterizing, and understanding factors that initiate these changes. Despite their high prevalence, studies have only recently begun to investigate how viral lung infections have an impact on the gut microbiota. There is also considerable interest in whether the gut microbiota could be manipulated during vaccination to improve efficacy. In this highly controlled study, we aimed to establish the effect of viral lung infection on gut microbiota composition and the gut environment using mouse models of common respiratory pathogens respiratory syncytial virus (RSV) and influenza virus. This was then compared to the effect of live attenuated influenza virus (LAIV) vaccination. Both RSV and influenza virus infection resulted in significantly altered gut microbiota diversity, with an increase in and a concomitant decrease in phyla abundance. Although the increase in the phylum was consistent across several experiments, differences were observed at the family and operational taxonomic unit level. This suggests a change in gut conditions after viral lung infection that favors outgrowth but not individual families. No change in gut microbiota composition was observed after LAIV vaccination, suggesting that the driver of gut microbiota change is specific to live viral infection. Viral lung infections also resulted in an increase in fecal lipocalin-2, suggesting low-grade gut inflammation, and colonic Muc5ac levels. Owing to the important role that mucus plays in the gut environment, this may explain the changes in microbiota composition observed. This study demonstrates that the gut microbiota and the gut environment are altered following viral lung infections and that these changes are not observed during vaccination. Whether increased mucin levels and gut inflammation drive, or are a result of, these changes is still to be determined.
Author Moffatt, Miriam F
Tregoning, John S
James, Phillip
Groves, Helen T
Cuthbertson, Leah
Cox, Michael J
AuthorAffiliation 3 Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Trust, Imperial College London , London , United Kingdom
2 National Heart & Lung Institute, Imperial College London , London , United Kingdom
1 Mucosal Infection and Immunity Group, Department of Medicine, Section of Virology, St. Mary’s Campus, Imperial College London , London , United Kingdom
AuthorAffiliation_xml – name: 1 Mucosal Infection and Immunity Group, Department of Medicine, Section of Virology, St. Mary’s Campus, Imperial College London , London , United Kingdom
– name: 2 National Heart & Lung Institute, Imperial College London , London , United Kingdom
– name: 3 Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Trust, Imperial College London , London , United Kingdom
Author_xml – sequence: 1
  givenname: Helen T
  surname: Groves
  fullname: Groves, Helen T
  organization: Mucosal Infection and Immunity Group, Department of Medicine, Section of Virology, St. Mary's Campus, Imperial College London, London, United Kingdom
– sequence: 2
  givenname: Leah
  surname: Cuthbertson
  fullname: Cuthbertson, Leah
  organization: Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Trust, Imperial College London, London, United Kingdom
– sequence: 3
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  surname: James
  fullname: James, Phillip
  organization: Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Trust, Imperial College London, London, United Kingdom
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  givenname: Miriam F
  surname: Moffatt
  fullname: Moffatt, Miriam F
  organization: Respiratory Biomedical Research Unit, Royal Brompton & Harefield NHS Trust, Imperial College London, London, United Kingdom
– sequence: 5
  givenname: Michael J
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  fullname: Cox, Michael J
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  givenname: John S
  surname: Tregoning
  fullname: Tregoning, John S
  organization: Mucosal Infection and Immunity Group, Department of Medicine, Section of Virology, St. Mary's Campus, Imperial College London, London, United Kingdom
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Cites_doi 10.1371/journal.pone.0009836
10.1371/journal.pone.0044328
10.1186/s13059-014-0550-8
10.1093/nar/gks1219
10.1371/journal.pone.0048224
10.3389/fimmu.2017.01164
10.1136/gutjnl-2015-309728
10.1128/JVI.00102-07
10.1038/srep43859
10.1371/journal.pone.0061217
10.1101/pdb.prot4986
10.1128/AEM.71.11.7483-7492.2005
10.1016/S0140-6736(10)60206-1
10.1126/science.aad3503
10.1371/journal.pone.0009490
10.1186/gb-2013-14-1-r4
10.1093/bioinformatics/btq461
10.1016/j.cell.2014.09.008
10.1128/AEM.01043-13
10.1016/B978-0-12-800100-4.00003-9
10.1371/journal.pone.0074957
10.1242/dmm.017400
10.1152/physrev.00045.2009
10.1542/peds.2016-0218
10.1073/pnas.1310750111
10.1093/bioinformatics/btp324
10.1186/1471-2334-10-3
10.1016/j.vascn.2005.03.001
10.1038/nrmicro2859
10.1128/CMR.00032-09
10.1084/jem.20140625
10.1038/mi.2015.86
10.1186/s40168-016-0181-2
10.1016/j.immuni.2014.08.009
10.1126/science.1208344
10.1371/journal.pone.0110396
10.3389/fmicb.2016.00459
10.1128/JVI.01693-10
10.1038/4441022a
10.3389/fgene.2015.00081
10.4161/gmic.1.4.12778
10.1023/A:1025815113599
10.1126/science.1223490
10.1099/0022-1317-82-11-2664
10.4049/jimmunol.122.5.1892
10.1371/journal.ppat.1005572
10.1038/nmeth.f.303
10.1073/pnas.96.6.3081
10.1186/s40168-017-0264-8
10.1073/pnas.1019378108
10.1016/j.phrs.2012.10.020
10.1101/gr.112730.110
10.1093/nar/gkt1244
10.1111/1462-2920.13713
10.1038/mi.2012.114
10.1038/nmicrobiol.2016.131
10.1093/nar/gks808
10.1007/s00109-016-1492-2
10.3748/wjg.v21.i29.8787
10.1038/mi.2013.116
10.1093/bioinformatics/btp636
10.1038/nature05414
10.3389/fimmu.2016.00633
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Copyright Copyright © 2018 Groves, Cuthbertson, James, Moffatt, Cox and Tregoning. 2018 Groves, Cuthbertson, James, Moffatt, Cox and Tregoning
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Keywords influenza
Bacteroidetes
Mucin 5ac
respiratory syncytial virus infections
gut microbiota
Firmicutes
Language English
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Specialty section: This article was submitted to Vaccines and Molecular Therapeutics, a section of the journal Frontiers in Immunology
Edited by: Rino Rappuoli, GlaxoSmithKline, Italy
These authors have contributed equally to this work.
Reviewed by: Randy A. Albrecht, Icahn School of Medicine at Mount Sinai, United States; Raffael Nachbagauer, Icahn School of Medicine at Mount Sinai, United States
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5816042/
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PublicationCentury 2000
PublicationDate 2018-02-12
PublicationDateYYYYMMDD 2018-02-12
PublicationDate_xml – month: 02
  year: 2018
  text: 2018-02-12
  day: 12
PublicationDecade 2010
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in immunology
PublicationTitleAlternate Front Immunol
PublicationYear 2018
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References Oh (B6) 2014; 41
Jakobsson (B9) 2010; 5
Tan (B2) 2014; 121
Haas (B26) 2011; 21
Byrd (B56) 2004; 23
B29
Marin (B50) 2017; 7
Caporaso (B21) 2010; 7
Hooper (B5) 2012; 336
Stokes (B42) 2011; 85
Harris (B67) 2014; 9
Kozich (B20) 2013; 79
Caporaso (B25) 2010; 26
B32
Takeyama (B38) 1999; 96
Carabotti (B3) 2015; 28
Deriu (B53) 2016; 12
Zelaya (B18) 2016; 7
Gu (B43) 2013; 8
Johnson (B62) 2017; 95
Nguyen (B47) 2015; 8
Hildebrand (B44) 2013; 14
Borgdorff (B58) 2016; 9
Chassaing (B39) 2012; 7
Falony (B8) 2016; 352
Wu (B7) 2011; 334
Dillon (B11) 2014; 7
Quast (B24) 2013; 41
Derrien (B57) 2010; 1
Klindworth (B19) 2013; 41
Ichinohe (B16) 2011; 108
Edgar (B23) 2010; 26
Bartley (B52) 2017; 8
Scott (B59) 2013; 69
(B30) 2016
Ruiz (B61) 2017; 19
Boukhvalova (B41) 2007; 81
Koeppen (B55) 2013; 6
Nelson (B10) 2012; 7
Cole (B27) 2014; 42
Love (B34) 2014; 15
Seedorf (B65) 2014; 159
Borton (B40) 2017; 5
Ormerod (B66) 2016; 4
Hasegawa (B54) 2016; 138
Sekirov (B4) 2010; 90
Price (B28) 2010; 5
Turnbaugh (B49) 2006; 444
Macfarlane (B46) 2005; 71
Tailford (B63) 2015; 6
Jandhyala (B1) 2015; 21
Tregoning (B14) 2010; 23
B15
Wang (B51) 2014; 211
Nair (B13) 2010; 375
Fischer (B35) 2008; 2008
Jeffery (B48) 2012; 10
Ponnuraj (B36) 2001; 82
Phillips (B37) 2005; 53
Fujimura (B69) 2014; 111
Lagkouvardos (B64) 2016; 1
Jovel (B33) 2016; 7
(B12) 2016
McMurdie (B31) 2013; 8
Ley (B60) 2006; 444
McDermott (B45) 1979; 122
Schuijt (B17) 2015; 65
Li (B22) 2009; 25
Dilantika (B68) 2010; 10
References_xml – volume: 5
  start-page: e9836
  year: 2010
  ident: B9
  article-title: Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0009836
  contributor:
    fullname: Jakobsson
– volume: 7
  start-page: e44328
  year: 2012
  ident: B39
  article-title: Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0044328
  contributor:
    fullname: Chassaing
– volume: 15
  start-page: 550
  year: 2014
  ident: B34
  article-title: Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
  publication-title: Genome Biol
  doi: 10.1186/s13059-014-0550-8
  contributor:
    fullname: Love
– volume: 41
  start-page: D590
  year: 2013
  ident: B24
  article-title: The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gks1219
  contributor:
    fullname: Quast
– volume: 7
  start-page: e48224
  year: 2012
  ident: B10
  article-title: Disruption of the human gut microbiota following norovirus infection
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0048224
  contributor:
    fullname: Nelson
– volume: 8
  start-page: 1164
  year: 2017
  ident: B52
  article-title: Impact of age, caloric restriction, and influenza infection on mouse gut microbiome: an exploratory study of the role of age-related microbiome changes on influenza responses
  publication-title: Front Immunol
  doi: 10.3389/fimmu.2017.01164
  contributor:
    fullname: Bartley
– volume: 65
  start-page: 575
  year: 2015
  ident: B17
  article-title: The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia
  publication-title: Gut
  doi: 10.1136/gutjnl-2015-309728
  contributor:
    fullname: Schuijt
– volume-title: RStudio: Integrated Development for R
  year: 2016
  ident: B30
– volume: 81
  start-page: 9443
  year: 2007
  ident: B41
  article-title: Respiratory syncytial virus infects and abortively replicates in the lungs in spite of preexisting immunity
  publication-title: J Virol
  doi: 10.1128/JVI.00102-07
  contributor:
    fullname: Boukhvalova
– volume: 7
  start-page: 43859
  year: 2017
  ident: B50
  article-title: Microbiota alteration is associated with the development of stress-induced despair behavior
  publication-title: Sci Rep
  doi: 10.1038/srep43859
  contributor:
    fullname: Marin
– ident: B29
– volume: 8
  start-page: e61217
  year: 2013
  ident: B31
  article-title: Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0061217
  contributor:
    fullname: McMurdie
– volume: 2008
  start-page: db.rot4986
  year: 2008
  ident: B35
  article-title: Hematoxylin and eosin staining of tissue and cell sections
  publication-title: CSH Protoc
  doi: 10.1101/pdb.prot4986
  contributor:
    fullname: Fischer
– volume: 71
  start-page: 7483
  year: 2005
  ident: B46
  article-title: Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.71.11.7483-7492.2005
  contributor:
    fullname: Macfarlane
– volume: 375
  start-page: 1545
  year: 2010
  ident: B13
  article-title: Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis
  publication-title: Lancet
  doi: 10.1016/S0140-6736(10)60206-1
  contributor:
    fullname: Nair
– volume: 352
  start-page: 560
  year: 2016
  ident: B8
  article-title: Population-level analysis of gut microbiome variation
  publication-title: Science
  doi: 10.1126/science.aad3503
  contributor:
    fullname: Falony
– volume: 5
  start-page: e9490
  year: 2010
  ident: B28
  article-title: FastTree 2—approximately maximum-likelihood trees for large alignments
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0009490
  contributor:
    fullname: Price
– volume: 14
  start-page: R4
  year: 2013
  ident: B44
  article-title: Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice
  publication-title: Genome Biol
  doi: 10.1186/gb-2013-14-1-r4
  contributor:
    fullname: Hildebrand
– volume: 26
  start-page: 2460
  year: 2010
  ident: B23
  article-title: Search and clustering orders of magnitude faster than BLAST
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btq461
  contributor:
    fullname: Edgar
– volume-title: The Top 10 Causes of Death
  year: 2016
  ident: B12
– volume: 159
  start-page: 253
  year: 2014
  ident: B65
  article-title: Bacteria from diverse habitats colonize and compete in the mouse gut
  publication-title: Cell
  doi: 10.1016/j.cell.2014.09.008
  contributor:
    fullname: Seedorf
– volume: 79
  start-page: 5112
  year: 2013
  ident: B20
  article-title: Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.01043-13
  contributor:
    fullname: Kozich
– volume: 121
  start-page: 91
  year: 2014
  ident: B2
  article-title: The role of short-chain fatty acids in health and disease
  publication-title: Adv Immunol
  doi: 10.1016/B978-0-12-800100-4.00003-9
  contributor:
    fullname: Tan
– volume: 8
  start-page: e74957
  year: 2013
  ident: B43
  article-title: Bacterial community mapping of the mouse gastrointestinal tract
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0074957
  contributor:
    fullname: Gu
– volume: 8
  start-page: 1
  year: 2015
  ident: B47
  article-title: How informative is the mouse for human gut microbiota research?
  publication-title: Dis Model Mech
  doi: 10.1242/dmm.017400
  contributor:
    fullname: Nguyen
– volume: 28
  start-page: 203
  year: 2015
  ident: B3
  article-title: The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems
  publication-title: Ann Gastroenterol Q Publ Hell Soc Gastroenterol
  contributor:
    fullname: Carabotti
– volume: 90
  start-page: 859
  year: 2010
  ident: B4
  article-title: Gut microbiota in health and disease
  publication-title: Physiol Rev
  doi: 10.1152/physrev.00045.2009
  contributor:
    fullname: Sekirov
– volume: 138
  start-page: e20160218
  year: 2016
  ident: B54
  article-title: The fecal microbiota profile and bronchiolitis in infants
  publication-title: Pediatrics
  doi: 10.1542/peds.2016-0218
  contributor:
    fullname: Hasegawa
– volume: 111
  start-page: 805
  year: 2014
  ident: B69
  article-title: House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1310750111
  contributor:
    fullname: Fujimura
– volume: 25
  start-page: 1754
  year: 2009
  ident: B22
  article-title: Fast and accurate short read alignment with Burrows–Wheeler transform
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp324
  contributor:
    fullname: Li
– volume: 10
  start-page: 3
  year: 2010
  ident: B68
  article-title: Influenza virus infection among pediatric patients reporting diarrhea and influenza-like illness
  publication-title: BMC Infect Dis
  doi: 10.1186/1471-2334-10-3
  contributor:
    fullname: Dilantika
– volume: 53
  start-page: 160
  year: 2005
  ident: B37
  article-title: An enzyme-linked immunosorbent assay (ELISA) for the determination of mucin levels in bronchoalveolar lavage fluid
  publication-title: J Pharmacol Toxicol Methods
  doi: 10.1016/j.vascn.2005.03.001
  contributor:
    fullname: Phillips
– volume: 10
  start-page: 591
  year: 2012
  ident: B48
  article-title: Categorization of the gut microbiota: enterotypes or gradients?
  publication-title: Nat Rev Microbiol
  doi: 10.1038/nrmicro2859
  contributor:
    fullname: Jeffery
– volume: 23
  start-page: 74
  year: 2010
  ident: B14
  article-title: Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology
  publication-title: Clin Microbiol Rev
  doi: 10.1128/CMR.00032-09
  contributor:
    fullname: Tregoning
– volume: 211
  start-page: 2397
  year: 2014
  ident: B51
  article-title: Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation
  publication-title: J Exp Med
  doi: 10.1084/jem.20140625
  contributor:
    fullname: Wang
– volume: 9
  start-page: 621
  year: 2016
  ident: B58
  article-title: Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier
  publication-title: Mucosal Immunol
  doi: 10.1038/mi.2015.86
  contributor:
    fullname: Borgdorff
– volume: 4
  start-page: 36
  year: 2016
  ident: B66
  article-title: Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals
  publication-title: Microbiome
  doi: 10.1186/s40168-016-0181-2
  contributor:
    fullname: Ormerod
– volume: 41
  start-page: 478
  year: 2014
  ident: B6
  article-title: TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination
  publication-title: Immunity
  doi: 10.1016/j.immuni.2014.08.009
  contributor:
    fullname: Oh
– volume: 334
  start-page: 105
  year: 2011
  ident: B7
  article-title: Linking long-term dietary patterns with gut microbial enterotypes
  publication-title: Science
  doi: 10.1126/science.1208344
  contributor:
    fullname: Wu
– volume: 9
  start-page: e110396
  year: 2014
  ident: B67
  article-title: Specific microbiome changes in a mouse model of parenteral nutrition associated liver injury and intestinal inflammation
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0110396
  contributor:
    fullname: Harris
– volume: 7
  start-page: 459
  year: 2016
  ident: B33
  article-title: Characterization of the gut microbiome using 16S or shotgun metagenomics
  publication-title: Front Microbiol
  doi: 10.3389/fmicb.2016.00459
  contributor:
    fullname: Jovel
– volume: 85
  start-page: 5782
  year: 2011
  ident: B42
  article-title: Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice
  publication-title: J Virol
  doi: 10.1128/JVI.01693-10
  contributor:
    fullname: Stokes
– volume: 444
  start-page: 1022
  year: 2006
  ident: B60
  article-title: Microbial ecology: human gut microbes associated with obesity
  publication-title: Nature
  doi: 10.1038/4441022a
  contributor:
    fullname: Ley
– volume: 6
  start-page: 81
  year: 2015
  ident: B63
  article-title: Mucin glycan foraging in the human gut microbiome
  publication-title: Front Genet
  doi: 10.3389/fgene.2015.00081
  contributor:
    fullname: Tailford
– volume: 1
  start-page: 254
  year: 2010
  ident: B57
  article-title: Mucin-bacterial interactions in the human oral cavity and digestive tract
  publication-title: Gut Microbes
  doi: 10.4161/gmic.1.4.12778
  contributor:
    fullname: Derrien
– volume: 23
  start-page: 77
  year: 2004
  ident: B56
  article-title: Mucins and mucin binding proteins in colorectal cancer
  publication-title: Cancer Metastasis Rev
  doi: 10.1023/A:1025815113599
  contributor:
    fullname: Byrd
– volume: 336
  start-page: 1268
  year: 2012
  ident: B5
  article-title: Interactions between the microbiota and the immune system
  publication-title: Science
  doi: 10.1126/science.1223490
  contributor:
    fullname: Hooper
– volume: 82
  start-page: 2663
  year: 2001
  ident: B36
  article-title: Increased replication of respiratory syncytial virus (RSV) in pulmonary infiltrates is associated with enhanced histopathological disease in bonnet monkeys (Macaca radiata) pre-immunized with a formalin-inactivated RSV vaccine
  publication-title: J Gen Virol
  doi: 10.1099/0022-1317-82-11-2664
  contributor:
    fullname: Ponnuraj
– volume: 122
  start-page: 1892
  year: 1979
  ident: B45
  article-title: Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues
  publication-title: J Immunol
  doi: 10.4049/jimmunol.122.5.1892
  contributor:
    fullname: McDermott
– volume: 12
  start-page: e1005572
  year: 2016
  ident: B53
  article-title: Influenza virus affects intestinal microbiota and secondary salmonella infection in the gut through type I interferons
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1005572
  contributor:
    fullname: Deriu
– volume: 7
  start-page: 335
  year: 2010
  ident: B21
  article-title: QIIME allows analysis of high-throughput community sequencing data
  publication-title: Nat Methods
  doi: 10.1038/nmeth.f.303
  contributor:
    fullname: Caporaso
– volume: 96
  start-page: 3081
  year: 1999
  ident: B38
  article-title: Epidermal growth factor system regulates mucin production in airways
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.96.6.3081
  contributor:
    fullname: Takeyama
– volume: 5
  start-page: 47
  year: 2017
  ident: B40
  article-title: Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome
  publication-title: Microbiome
  doi: 10.1186/s40168-017-0264-8
  contributor:
    fullname: Borton
– volume: 108
  start-page: 5354
  year: 2011
  ident: B16
  article-title: Microbiota regulates immune defense against respiratory tract influenza A virus infection
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1019378108
  contributor:
    fullname: Ichinohe
– volume: 69
  start-page: 52
  year: 2013
  ident: B59
  article-title: The influence of diet on the gut microbiota
  publication-title: Pharmacol Res
  doi: 10.1016/j.phrs.2012.10.020
  contributor:
    fullname: Scott
– volume: 21
  start-page: 494
  year: 2011
  ident: B26
  article-title: Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons
  publication-title: Genome Res
  doi: 10.1101/gr.112730.110
  contributor:
    fullname: Haas
– volume: 42
  start-page: D633
  year: 2014
  ident: B27
  article-title: Ribosomal Database Project: data and tools for high throughput rRNA analysis
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkt1244
  contributor:
    fullname: Cole
– volume: 19
  start-page: 1536
  year: 2017
  ident: B61
  article-title: One-year calorie restriction impacts gut microbial composition but not its metabolic performance in obese adolescents
  publication-title: Environ Microbiol
  doi: 10.1111/1462-2920.13713
  contributor:
    fullname: Ruiz
– volume: 6
  start-page: 762
  year: 2013
  ident: B55
  article-title: Detrimental role of the airway mucin Muc5ac during ventilator-induced lung injury
  publication-title: Mucosal Immunol
  doi: 10.1038/mi.2012.114
  contributor:
    fullname: Koeppen
– volume: 1
  start-page: 16131
  year: 2016
  ident: B64
  article-title: The mouse intestinal bacterial collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota
  publication-title: Nat Microbiol
  doi: 10.1038/nmicrobiol.2016.131
  contributor:
    fullname: Lagkouvardos
– volume: 41
  start-page: e1
  year: 2013
  ident: B19
  article-title: Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gks808
  contributor:
    fullname: Klindworth
– volume: 95
  start-page: 1
  year: 2017
  ident: B62
  article-title: Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes
  publication-title: J Mol Med (Berl)
  doi: 10.1007/s00109-016-1492-2
  contributor:
    fullname: Johnson
– volume: 21
  start-page: 8787
  year: 2015
  ident: B1
  article-title: Role of the normal gut microbiota
  publication-title: World J Gastroenterol
  doi: 10.3748/wjg.v21.i29.8787
  contributor:
    fullname: Jandhyala
– volume: 7
  start-page: 983
  year: 2014
  ident: B11
  article-title: An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia
  publication-title: Mucosal Immunol
  doi: 10.1038/mi.2013.116
  contributor:
    fullname: Dillon
– volume: 26
  start-page: 266
  year: 2010
  ident: B25
  article-title: PyNAST: a flexible tool for aligning sequences to a template alignment
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp636
  contributor:
    fullname: Caporaso
– volume: 444
  start-page: 1027
  year: 2006
  ident: B49
  article-title: An obesity-associated gut microbiome with increased capacity for energy harvest
  publication-title: Nature
  doi: 10.1038/nature05414
  contributor:
    fullname: Turnbaugh
– volume: 7
  start-page: 633
  year: 2016
  ident: B18
  article-title: Respiratory antiviral immunity and immunobiotics: beneficial effects on inflammation-coagulation interaction during influenza virus infection
  publication-title: Front Immunol
  doi: 10.3389/fimmu.2016.00633
  contributor:
    fullname: Zelaya
– ident: B32
– ident: B15
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Snippet Alterations in the composition of the gut microbiota have profound effects on human health. Consequently, there is great interest in identifying,...
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Aggregation Database
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StartPage 182
SubjectTerms Animals
Bacteria - classification
Bacteria - isolation & purification
Bacteroidetes
Bacteroidetes - isolation & purification
Female
Firmicutes
Firmicutes - isolation & purification
Gastrointestinal Microbiome
gut microbiota
Immunology
influenza
Influenza Vaccines - administration & dosage
Lipocalin-2 - analysis
Lung - virology
Mice
Mice, Inbred BALB C
Mucin 5ac
Mucin 5AC - analysis
Orthomyxoviridae
Orthomyxoviridae Infections - complications
respiratory syncytial virus infections
Respiratory Syncytial Virus Infections - complications
Respiratory Syncytial Viruses
Respiratory Tract Infections - complications
Respiratory Tract Infections - virology
RNA, Ribosomal, 16S
Vaccines, Attenuated - administration & dosage
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Title Respiratory Disease following Viral Lung Infection Alters the Murine Gut Microbiota
URI https://www.ncbi.nlm.nih.gov/pubmed/29483910
https://search.proquest.com/docview/2008885094
https://pubmed.ncbi.nlm.nih.gov/PMC5816042
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Volume 9
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