دورية أكاديمية
Shotgun metagenomics and systemic targeted metabolomics highlight indole-3-propionic acid as a protective gut microbial metabolite against influenza infection.
العنوان: | Shotgun metagenomics and systemic targeted metabolomics highlight indole-3-propionic acid as a protective gut microbial metabolite against influenza infection. |
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المؤلفون: | Heumel S; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., de Rezende Rodovalho V; Laboratory of Immunoinflammation, Institute of Biology, University of Campinas (UNICAMP), Campinas, Brazil., Urien C; Genoscreen, Lille, France., Specque F; Biomathematica, Rue des Aloes, Quartier Balestrino, Ajaccio, France., Brito Rodrigues P; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France.; Laboratory of Immunoinflammation, Institute of Biology, University of Campinas (UNICAMP), Campinas, Brazil., Robil C; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Delval L; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Sencio V; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Descat A; Univ. Lille, CHU Lille, EA 7365 - GRITA - Groupe de Recherche sur les formes Injectables et les Technologies Associées, Lille, France., Deruyter L; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Ferreira S; Genoscreen, Lille, France., Gomes Machado M; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Barthelemy A; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Angulo FS; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Haas JT; Univ. Lille, INSERM, CHU Lille, Institut Pasteur de Lille, Lille, France., Goosens JF; Univ. Lille, CHU Lille, EA 7365 - GRITA - Groupe de Recherche sur les formes Injectables et les Technologies Associées, Lille, France., Wolowczuk I; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Grangette C; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Rouillé Y; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France., Grimaud G; Biomathematica, Rue des Aloes, Quartier Balestrino, Ajaccio, France., Lenski M; Univ. Lrille, CHU Lille, Service de toxicologie et Génopathies, ULR 4483 - IMPECS - IMPact de l'Environnement Chimique sur la Santé humaine, Lille, France., Hennart B; Univ. Lrille, CHU Lille, Service de toxicologie et Génopathies, ULR 4483 - IMPECS - IMPact de l'Environnement Chimique sur la Santé humaine, Lille, France., Ramirez Vinolo MA; Laboratory of Immunoinflammation, Institute of Biology, University of Campinas (UNICAMP), Campinas, Brazil., Trottein F; Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Center for Infection and Immunity of Lille, Lille, France. |
المصدر: | Gut microbes [Gut Microbes] 2024 Jan-Dec; Vol. 16 (1), pp. 2325067. Date of Electronic Publication: 2024 Mar 06. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Taylor & Francis Country of Publication: United States NLM ID: 101495343 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1949-0984 (Electronic) Linking ISSN: 19490976 NLM ISO Abbreviation: Gut Microbes Subsets: MEDLINE |
أسماء مطبوعة: | Publication: 2015- : Philadelphia, PA : Taylor & Francis Original Publication: Austin, Tex. : Landes Bioscience |
مواضيع طبية MeSH: | Influenza, Human* , Gastrointestinal Microbiome* , Actinobacteria*, Humans ; Animals ; Mice ; Propionates ; Tryptophan ; Inflammation ; Polyamines |
مستخلص: | The gut-to-lung axis is critical during respiratory infections, including influenza A virus (IAV) infection. In the present study, we used high-resolution shotgun metagenomics and targeted metabolomic analysis to characterize influenza-associated changes in the composition and metabolism of the mouse gut microbiota. We observed several taxonomic-level changes on day (D)7 post-infection, including a marked reduction in the abundance of members of the Lactobacillaceae and Bifidobacteriaceae families, and an increase in the abundance of Akkermansia muciniphila . On D14, perturbation persisted in some species. Functional scale analysis of metagenomic data revealed transient changes in several metabolic pathways, particularly those leading to the production of short-chain fatty acids (SCFAs), polyamines, and tryptophan metabolites. Quantitative targeted metabolomics analysis of the serum revealed changes in specific classes of gut microbiota metabolites, including SCFAs, trimethylamine, polyamines, and indole-containing tryptophan metabolites. A marked decrease in indole-3-propionic acid (IPA) blood level was observed on D7. Changes in microbiota-associated metabolites correlated with changes in taxon abundance and disease marker levels. In particular, IPA was positively correlated with some Lactobacillaceae and Bifidobacteriaceae species ( Limosilactobacillus reuteri, Lactobacillus animalis ) and negatively correlated with Bacteroidales bacterium M7, viral load, and inflammation markers. IPA supplementation in diseased animals reduced viral load and lowered local (lung) and systemic inflammation. Treatment of mice with antibiotics targeting IPA-producing bacteria before infection enhanced viral load and lung inflammation, an effect inhibited by IPA supplementation. The results of this integrated metagenomic-metabolomic analysis highlighted IPA as an important contributor to influenza outcomes and a potential biomarker of disease severity. |
References: | Pharmacol Res Perspect. 2021 Aug;9(4):e00837. (PMID: 34289267) Annu Rev Nutr. 2017 Aug 21;37:157-181. (PMID: 28715991) Mucosal Immunol. 2021 Mar;14(2):296-304. (PMID: 33500564) Nutrients. 2020 Mar 25;12(4):. (PMID: 32218248) Microbiol Spectr. 2021 Oct 31;9(2):e0018221. (PMID: 34612695) Pathogens. 2021 Jun 17;10(6):. (PMID: 34204203) Blood. 2018 Jun 28;131(26):2978-2986. (PMID: 29674425) Infect Immun. 2021 Aug 16;89(9):e0073420. (PMID: 33820816) Nat Commun. 2018 Aug 17;9(1):3294. (PMID: 30120222) Front Microbiol. 2017 Sep 22;8:1765. (PMID: 29018410) Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):3118-3125. (PMID: 30718396) Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3698-703. (PMID: 19234110) Cell Rep. 2019 Jul 2;28(1):245-256.e4. (PMID: 31269444) Sci Transl Med. 2022 Nov 16;14(671):eabo3445. (PMID: 36383683) Front Microbiol. 2015 Oct 07;6:1085. (PMID: 26500629) Front Nutr. 2021 Dec 14;8:790561. (PMID: 34970580) Nat Commun. 2019 Mar 4;10(1):1014. (PMID: 30833550) Nat Commun. 2019 Jun 20;10(1):2719. (PMID: 31222023) Cell Rep. 2017 Apr 25;19(4):733-745. (PMID: 28445725) EBioMedicine. 2022 Mar;77:103891. (PMID: 35220042) Front Endocrinol (Lausanne). 2022 Mar 18;13:841703. (PMID: 35370963) Cell Rep. 2020 Jul 21;32(3):107915. (PMID: 32649864) Nat Rev Gastroenterol Hepatol. 2022 Oct;19(10):625-637. (PMID: 35641786) Metabolites. 2022 Jul 14;12(7):. (PMID: 35888769) J Exp Med. 2014 Nov 17;211(12):2397-410. (PMID: 25366965) Mol Med. 2023 May 19;29(1):65. (PMID: 37208586) Front Immunol. 2018 Mar 05;9:320. (PMID: 29556226) Cell. 2016 Aug 25;166(5):1103-1116. (PMID: 27565341) Proc Natl Acad Sci U S A. 2011 Mar 29;108(13):5354-9. (PMID: 21402903) Cell Rep. 2020 Mar 3;30(9):2909-2922.e6. (PMID: 32130896) Allergy. 2018 Oct;73(10):2033-2045. (PMID: 29729200) PLoS One. 2020 Feb 13;15(2):e0228899. (PMID: 32053657) Mol Nutr Food Res. 2020 Sep;64(18):e2000426. (PMID: 32761878) Nat Med. 2016 Jun;22(6):598-605. (PMID: 27158904) Genome Biol. 2020 Apr 28;21(1):99. (PMID: 32345342) BMC Genomics. 2018 Apr 20;19(1):274. (PMID: 29678163) Circ Res. 2022 Aug 19;131(5):404-420. (PMID: 35893593) Immunity. 2018 May 15;48(5):992-1005.e8. (PMID: 29768180) Ann Surg. 2023 Dec 1;278(6):e1164-e1174. (PMID: 37185230) Mucosal Immunol. 2017 Mar;10(2):460-469. (PMID: 27220813) Science. 2017 Aug 25;357(6353):806-810. (PMID: 28775213) Immunity. 2012 Jul 27;37(1):158-70. (PMID: 22705104) BMC Microbiol. 2021 Feb 27;21(1):68. (PMID: 33639835) Nutrients. 2022 Dec 28;15(1):. (PMID: 36615808) Nat Methods. 2012 Mar 04;9(4):357-9. (PMID: 22388286) mBio. 2020 Feb 18;11(1):. (PMID: 32071269) Bioinformatics. 2022 Jun 24;38(Suppl 1):i378-i385. (PMID: 35758795) Microorganisms. 2020 Jun 18;8(6):. (PMID: 32570850) Int J Mol Sci. 2021 Nov 18;22(22):. (PMID: 34830317) Commun Biol. 2020 May 14;3(1):237. (PMID: 32409640) Anal Bioanal Chem. 2022 Sep;414(22):6419-6430. (PMID: 35841415) Gut Microbes. 2022 Jan-Dec;14(1):2105609. (PMID: 35915556) Microbiol Spectr. 2022 Jun 29;10(3):e0012522. (PMID: 35658593) Sci Rep. 2015 Oct 22;5:14771. (PMID: 26490635) Science. 2017 Aug 4;357(6350):498-502. (PMID: 28774928) Cell Rep. 2020 Mar 3;30(9):2934-2947.e6. (PMID: 32130898) Genome Biol. 2011 Jun 24;12(6):R60. (PMID: 21702898) J Pediatr. 2013 Feb;162(2):257-62. (PMID: 22981952) Front Microbiol. 2018 Apr 19;9:757. (PMID: 29725324) Clin Infect Dis. 2020 Dec 17;71(10):2669-2678. (PMID: 32497191) Nat Med. 2016 Jun;22(6):586-97. (PMID: 27158906) Microbiome. 2018 Jan 10;6(1):9. (PMID: 29321057) Mol Aspects Med. 2017 Aug;56:54-65. (PMID: 28602676) Nat Commun. 2019 Jul 22;10(1):3273. (PMID: 31332169) Lancet Healthy Longev. 2021 Jan;2(1):e13-e23. (PMID: 36098111) Nature. 2022 Jul;607(7919):585-592. (PMID: 35732737) Transl Res. 2021 Feb;228:109-125. (PMID: 32841736) Front Microbiol. 2021 Feb 02;11:586476. (PMID: 33603716) Front Microbiol. 2020 May 27;11:973. (PMID: 32547507) Int J Syst Evol Microbiol. 2004 Sep;54(Pt 5):1469-1476. (PMID: 15388697) Front Immunol. 2018 Feb 12;9:182. (PMID: 29483910) Open Forum Infect Dis. 2021 Jun 02;8(7):ofab288. (PMID: 34258318) Cell. 2020 Nov 25;183(5):1312-1324.e10. (PMID: 33212011) Proc Natl Acad Sci U S A. 2013 May 28;110(22):9066-71. (PMID: 23671105) Infect Immun. 2018 Jun 21;86(7):. (PMID: 29661933) J Lipid Res. 2019 Nov;60(11):1892-1904. (PMID: 31484693) Sci Rep. 2017 Jul 31;7(1):6589. (PMID: 28761145) Mucosal Immunol. 2019 Jul;12(4):843-850. (PMID: 30976087) J Intensive Care. 2021 Oct 21;9(1):65. (PMID: 34674768) Bioinformatics. 2020 Apr 1;36(7):2251-2252. (PMID: 31742321) PLoS Pathog. 2016 May 05;12(5):e1005572. (PMID: 27149619) |
فهرسة مساهمة: | Keywords: Influenza; disease severity; gut microbiota; indole-3-propionic acid; metabolomics; shotgun metagenomics |
المشرفين على المادة: | JHU490RVYR (propionic acid) 0 (Propionates) 8DUH1N11BX (Tryptophan) 0 (Polyamines) |
تواريخ الأحداث: | Date Created: 20240306 Date Completed: 20240307 Latest Revision: 20240809 |
رمز التحديث: | 20240809 |
مُعرف محوري في PubMed: | PMC10936607 |
DOI: | 10.1080/19490976.2024.2325067 |
PMID: | 38445660 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1949-0984 |
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DOI: | 10.1080/19490976.2024.2325067 |