1,635
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

GlcNac produced by the gut microbiome enhances host influenza resistance by modulating NK cells

, , , , , & show all
Article: 2271620 | Received 23 Feb 2023, Accepted 12 Oct 2023, Published online: 12 Nov 2023

References

  • Brown EM, Sadarangani M, Finlay BB. The role of the immune system in governing host-microbe interactions in the intestine. Nat Immunol. 2013;14(7):660–26. doi:10.1038/ni.2611.
  • Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. doi:10.1152/physrev.00045.2009.
  • Zhang D, Gao X, Li H, Borger DK, Wei Q, Yang E, Xu C, Pinho S, Frenette PS. The microbiota regulates hematopoietic stem cell fate decisions by controlling iron availability in bone marrow. Cell Stem Cell. 2022;29(2):232–247.e7. doi:10.1016/j.stem.2021.12.009.
  • Zheng Y, Hunt RL, Villaruz AE, Fisher EL, Liu R, Liu Q, Cheung GYC, Li M, Otto M. Commensal Staphylococcus epidermidis contributes to skin barrier homeostasis by generating protective ceramides. Cell Host & Microbe. 2022;30(3):301–313.e9. doi:10.1016/j.chom.2022.01.004.
  • Yang Y, Torchinsky MB, Gobert M, Xiong H, Xu M, Linehan JL, Alonzo F, Ng C, Chen A, Lin X, et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature. 2014;510(7503):152–156. doi:10.1038/nature13279.
  • Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–455. doi:10.1038/nature12726.
  • Kim M, Qie Y, Park J, Kim CH. Gut microbial metabolites fuel host antibody responses. Cell Host & Microbe. 2016;20(2):202–214. doi:10.1016/j.chom.2016.07.001.
  • Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014;111(6):2247–2252. doi:10.1073/pnas.1322269111.
  • Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients. Sci. 2018;359(6371):97–103. doi:10.1126/science.aan4236.
  • Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Sci. 2013;342(6161):967–970. doi:10.1126/science.1240527.
  • Matson V, Fessler J, Bao R, Chongsuwat, T. The commensal microbiome is associated with anti–PD-1 efficacy in metastatic melanoma patients. Sci. 2018;359(6371):104–108. doi:10.1126/science.aao3290.
  • Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–249. doi:10.1038/nature11552.
  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023. doi:10.1038/4441022a.
  • Woo V, Eshleman EM, Hashimoto-Hill S, Whitt J, Wu S-E, Engleman L, Rice T, Karns R, Qualls JE, Haslam DB, et al. Commensal segmented filamentous bacteria-derived retinoic acid primes host defense to intestinal infection. Cell Host & Microbe. 2021;29(12):1744–1756.e5. doi:10.1016/j.chom.2021.09.010.
  • Brown RL, Sequeira RP, Clarke TB. The microbiota protects against respiratory infection via GM-CSF signaling. Nat Commun. 2017;8(1):1512. doi:10.1038/s41467-017-01803-x.
  • Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, Hickman HD, McCulloch JA, Badger JH, Ajami NJ, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171(5):1015–1028.e13. doi:10.1016/j.cell.2017.09.016.
  • Marsland BJ, Gollwitzer ES. Host–microorganism interactions in lung diseases. Nat Rev Immunol. 2014;14(12):827–835. doi:10.1038/nri3769.
  • Steinhauer DA, Skehel JJ. Genetics of influenza viruses. Annu Rev Genet. 2002;36(1):305–332. doi:10.1146/annurev.genet.36.052402.152757.
  • Guan Y, Vijaykrishna D, Bahl J, Zhu H, Wang J, Smith GJD. The emergence of pandemic influenza viruses. Protein Cell. 2010;1(1):9–13. doi:10.1007/s13238-010-0008-z.
  • Centers for Disease Control and Prevention (CDC). Swine influenza a (H1N1) infection in two children--Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep. 2009;58(15):400–402.
  • Saunders-Hastings PR, Krewski D. Reviewing the history of pandemic influenza: understanding patterns of emergence and transmission. Pathogens (Basel, Switzerland). 2016;5(4):66. doi:10.3390/pathogens5040066.
  • Krammer F, Smith GJD, Fouchier RAM, Peiris M, Kedzierska K, Doherty PC, Palese P, Shaw ML, Treanor J, Webster RG, et al. Influenza. Nat Rev Dis Primers. 2018;4(1). doi:10.1038/s41572-018-0002-y.
  • Palese P. Influenza: old and new threats. Nat Med. 2004;10(S12):S82–87. doi:10.1038/nm1141.
  • Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A. Microbiota regulates immune defense against respiratory tract influenza a virus infection. Proc Natl Acad Sci U S A. 2011;108(13):5354–5359. doi:10.1073/pnas.1019378108.
  • Abt MC, Osborne L, Monticelli L, Doering T, Alenghat T, Sonnenberg G, Paley M, Antenus M, Williams K, Erikson J, et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity. 2012;37(1):158–170. doi:10.1016/j.immuni.2012.04.011.
  • Bradley KC, Finsterbusch K, Schnepf D, Crotta S, Llorian M, Davidson S, Fuchs SY, Staeheli P, Wack A. Microbiota-driven tonic interferon signals in lung stromal cells protect from influenza virus infection. Cell Rep. 2019;28(1):245–256.e4. doi:10.1016/j.celrep.2019.05.105.
  • Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Sci. 2013;341(6145):569–573. doi:10.1126/science.1241165.
  • Kaiko GE, Ryu SH, Koues OI, Collins PL, Solnica-Krezel L, Pearce EJ, Pearce EL, Oltz EM, Stappenbeck TS. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell. 2016;165(7):1708–1720. doi:10.1016/j.cell.2016.05.018.
  • Mossad O, Batut B, Yilmaz B, Dokalis N, Mezö C, Nent E, Nabavi LS, Mayer M, Maron FJM, Buescher JM, et al. Gut microbiota drives age-related oxidative stress and mitochondrial damage in microglia via the metabolite N(6)-carboxymethyllysine. Nat Neurosci. 2022;25(3):295–305. doi:10.1038/s41593-022-01027-3.
  • He Y, Fu L, Li Y, Wang W, Gong M, Zhang J, Dong X, Huang J, Wang Q, Mackay CR, et al. Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8+ T cell immunity. Cell Metab. 2021;33(5):988–1000.e7. doi:10.1016/j.cmet.2021.03.002.
  • Han J, Lin K, Sequeira C, Borchers CH. An isotope-labeled chemical derivatization method for the quantitation of short-chain fatty acids in human feces by liquid chromatography-tandem mass spectrometry. Anal Chim Acta. 2015;854:86–94. doi:10.1016/j.aca.2014.11.015.
  • Schultz-Cherry S. Role of NK cells in influenza infection. Curr Top Microbiol Immunol. 2015;386:109–120.
  • Dons’koi BV, Chernyshov VP, Osypchuk DV. Measurement of NK activity in whole blood by the CD69 up-regulation after co-incubation with K562, comparison with NK cytotoxicity assays and CD107a degranulation assay. J Immunol Methods. 2011;372(1–2):187–195. doi:10.1016/j.jim.2011.07.016.
  • El Bakkouri K, Descamps F, De Filette M, Smet A, Festjens E, Birkett A, Van Rooijen N, Verbeek S, Fiers W, Saelens X, et al. Universal vaccine based on ectodomain of matrix protein 2 of influenza A: fc receptors and alveolar macrophages mediate protection. J Immunol. 2011;186(2):1022–1031. doi:10.4049/jimmunol.0902147.
  • Azam MS, Kim EJ, Yang HS, Kim JK. High antioxidant and DNA protection activities of N-acetylglucosamine (GlcNac) and chitobiose produced by exolytic chitinase from Bacillus cereus EW5. SpringerPlus. 2014;3(1):354. doi:10.1186/2193-1801-3-354.
  • Derrien M, Belzer C, de Vos WM. Akkermansia muciniphila and its role in regulating host functions. Microb Pathog. 2017;106:171–181. doi:10.1016/j.micpath.2016.02.005.
  • Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet. 2015;6:81. doi:10.3389/fgene.2015.00081.
  • Fujita M, Tsuchida A, Hirata A, Kobayashi N, Goto K, Osumi K, Hirose Y, Nakayama J, Yamanoi T, Ashida H, et al. Glycoside hydrolase family 89 α-N-acetylglucosaminidase from Clostridium perfringens specifically acts on GlcNAcα1,4Galβ1R at the non-reducing terminus of O-Glycans in gastric mucin. J Biol Chem. 2011;286(8):6479–6489. doi:10.1074/jbc.M110.206722.
  • Zhang Q, Hu J, Feng J-W, Hu X-T, Wang T, Gong W-X, Huang K, Guo Y-X, Zou Z, Lin X, et al. Influenza infection elicits an expansion of gut population of endogenous Bifidobacterium animalis which protects mice against infection. Genome Biol. 2020;21(1):99. doi:10.1186/s13059-020-02007-1.
  • Steed AL, Christophi GP, Kaiko GE, Sun L, Goodwin VM, Jain U, Esaulova E, Artyomov MN, Morales DJ, Holtzman MJ, et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Sci. 2017;357(6350):498–502. doi:10.1126/science.aam5336.
  • Sencio V, Gallerand A, Gomes Machado M, Deruyter L, Heumel S, Soulard D, Barthelemy J, Cuinat C, Vieira AT, Barthelemy A, et al. Influenza virus infection impairs the gut’s barrier properties and favors secondary enteric bacterial infection through reduced production of short-chain fatty acids. Infect Immun. 2021;89(9):e0073420. doi:10.1128/IAI.00734-20.
  • Iwasaki A, Pillai PS. Innate immunity to influenza virus infection. Nat Rev Immunol. 2014;14(5):315–328. doi:10.1038/nri3665.
  • Masetti G, Moshkelgosha S, Köhling H-L, Covelli D, Banga JP, Berchner-Pfannschmidt U, Horstmann M, Diaz-Cano S, Goertz G-E, Plummer S, et al. Gut microbiota in experimental murine model of graves’ orbitopathy established in different environments may modulate clinical presentation of disease. Microbiome. 2018;6(1):97. doi:10.1186/s40168-018-0478-4.
  • Brown RL, Clarke TB. The regulation of host defences to infection by the microbiota. Immunology. 2017;150(1):1–6. doi:10.1111/imm.12634.
  • Bills B, Barshop WD, Sharma S, Canterbury J, Robitaille AM, Goodwin M, Senko MW, Zabrouskov V. Novel real-time library search driven data acquisition strategy for identification and characterization of metabolites. Anal Chem. 2022;94(9):3749–3755. doi:10.1021/acs.analchem.1c04336.
  • Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, et al. Evolution of mammals and their gut microbes. Sci. 2008;320(5883):1647–1651. doi:10.1126/science.1155725.
  • Hammer Q, Rückert T, Romagnani C. Natural killer cell specificity for viral infections. Nat Immunol. 2018;19(8):800–808. doi:10.1038/s41590-018-0163-6.
  • Masuda S, Azuma K, Kurozumi S, Kiyose M, Osaki T, Tsuka T, Itoh N, Imagawa T, Minami S, Sato K, et al. Anti-tumor properties of orally administered glucosamine and N-acetyl-D-glucosamine oligomers in a mouse model. Carbohydr Polym. 2014;111:783–787. doi:10.1016/j.carbpol.2014.04.102.
  • Xu W, Jiang C, Kong X, Liang YE, ROng MI, LIu W. Chitooligosaccharides and N-acetyl-D-glucosamine stimulate peripheral blood mononuclear cell-mediated antitumor immune responses. Mol Med Rep. 2012;6(2):385–390. doi:10.3892/mmr.2012.918.
  • Zhou G, Juang SW, Kane KP. NK cells exacerbate the pathology of influenza virus infection in mice. Eur J Immunol. 2013;43(4):929–938. doi:10.1002/eji.201242620.
  • Chen C, Sun W, Chen J, Huang JA. Dynamic variations of the peripheral blood immune cell subpopulation in patients with critical H7N9 swine-origin influenza a virus infection: a retrospective small-scale study. Exp Ther Med. 2017;13(4):1490–1494. doi:10.3892/etm.2017.4144.
  • Nishikado H, Mukai K, Kawano Y, Minegishi Y, Karasuyama H. NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo. J Immunol. 2011;186(10):5766–5771. doi:10.4049/jimmunol.1100370.
  • Gaulden EC, Keating WC. The effect of intravenous N-acetyl-D-GLUCOSAMINE on the blood and urine sugar concentrations of normal subjects. Metabolism. 1964;13(5):466–472. doi:10.1016/0026-0495(64)90120-9.
  • Talent JM, Gracy RW. Pilot study of oral polymeric N-acetyl-D-glucosamine as a potential treatment for patients with osteoarthritis. Clin Ther. 1996;18(6):1184–1190. doi:10.1016/S0149-2918(96)80073-7.
  • Chen JK, Shen CR, Liu CL. N-acetylglucosamine: production and applications. Mar Drugs. 2010;8(9):2493–2516. doi:10.3390/md8092493.
  • Salvatore S, Heuschkel R, Tomlin S, Davies SE, Edwards S, Walker-Smith JA, French I, Murch SH. A pilot study of N-acetyl glucosamine, a nutritional substrate for glycosaminoglycan synthesis, in paediatric chronic inflammatory bowel disease. Aliment Pharmacol Ther. 2000;14(12):1567–1579. doi:10.1046/j.1365-2036.2000.00883.x.
  • Anderson JW, Nicolosi RJ, Borzelleca JF. Glucosamine effects in humans: a review of effects on glucose metabolism, side effects, safety considerations and efficacy. Food Chem Toxicol. 2005;43(2):187–201. doi:10.1016/j.fct.2004.11.006.
  • Zhu Y, Liu Y, Li J, Shin H-D, Du G, Liu L, Chen J. An optimal glucose feeding strategy integrated with step-wise regulation of the dissolved oxygen level improves N-acetylglucosamine production in recombinant Bacillus subtilis. Bioresour Technol. 2015;177:387–392. doi:10.1016/j.biortech.2014.11.055.
  • Da Silva AS, Baldissera MD, Souza CF. Role of adenosine in the treatment of cardiovascular diseases: focus on hyperemia. Int J Cardiol. 2019;291:140–141. doi:10.1016/j.ijcard.2019.05.004.
  • Man S, Lu Y, Yin L, Cheng X, Ma L. Potential and promising anticancer drugs from adenosine and its analogs. Drug Discov Today. 2021;26(6):1490–1500. doi:10.1016/j.drudis.2021.02.020.
  • Eyer L, Zouharová D, Širmarová J, Fojtíková M, Štefánik M, Haviernik J, Nencka R, de Clercq E, Růžek D. Antiviral activity of the adenosine analogue BCX4430 against West Nile Virus and tick-borne flaviviruses. Antiviral Res. 2017;142:63–67. doi:10.1016/j.antiviral.2017.03.012.
  • Shang L, Wang Y, Qing J, Shu B, Cao L, Lou Z, Gong P, Sun Y, Yin Z. An adenosine nucleoside analogue NITD008 inhibits EV71 proliferation. Antiviral Res. 2014;112:47–58. doi:10.1016/j.antiviral.2014.10.009.
  • Suzuki T, Sometani A, Yamazaki Y, Horiike G, Mizutani Y, Masuda H, Yamada M, Tahara H, Xu G, Miyamoto D, et al. Sulphatide binds to human and animal influenza a viruses, and inhibits the viral infection. Biochem J. 1996;318(2):389–393. doi:10.1042/bj3180389.
  • Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al. Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors. Sci. 2018;359(6371):91–97. doi:10.1126/science.aan3706.
  • Yildiz S, Mazel-Sanchez B, Kandasamy M, Manicassamy B, Schmolke M. Influenza a virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome. 2018;6(9):1–7. doi:10.1186/s40168-017-0386-z.
  • Imai M, Iwatsuki-Horimoto K, Hatta M, Loeber S, Halfmann PJ, Nakajima N, Watanabe T, Ujie M, Takahashi K, Ito M, et al. Syrian hamsters as a small animal model for SARS-CoV-2 infection and countermeasure development. Proc Natl Acad Sci U S A. 2020;117(28):16587–16595. doi:10.1073/pnas.2009799117.
  • Sencio V, Benech N, Robil C, Deruyter L, Heumel S, Machelart A, Sulpice T, Lamazière A, Grangette C, Briand F, et al. Alteration of the gut microbiota’s composition and metabolic output correlates with COVID-19-like severity in obese NASH hamsters. Gut Microbes. 2022;14(1):2100200. doi:10.1080/19490976.2022.2100200.
  • Zhang X, Lin X, Qin C, Huang K, Sun X, Zhao L, Jin M. Avian chaperonin containing TCP1 subunit 5 supports influenza a virus replication by interacting with viral nucleoprotein, PB1, and PB2 proteins. Front Microbiol. 2020;11:538355. doi:10.3389/fmicb.2020.538355.
  • Cook JC, Wu H, Aleo MD, Adkins K. Principles of precision medicine and its application in toxicology. J Toxicol Sci. 2018;43(10):565–577. doi:10.2131/jts.43.565.
  • Zhou K, Wang J, Li A, Zhao W, Wang D, Zhang W, Yan J, Gao GF, Liu W, Fang M, et al. Swift and strong NK cell responses protect 129 mice against high-dose influenza virus infection. J Immunol. 2016;196(4):1842–1854. doi:10.4049/jimmunol.1501486.
  • Fang M, Lanier LL, Sigal LJ, Buller ML. A role for NKG2D in NK cell–mediated resistance to poxvirus disease. PLoS Pathog. 2008;4(2):e30. doi:10.1371/journal.ppat.0040030.
  • Fang M, Roscoe F, Sigal LJ. Age-dependent susceptibility to a viral disease due to decreased natural killer cell numbers and trafficking. J Exp Med. 2010;207(11):2369–2381. doi:10.1084/jem.20100282.
  • Fiore MF, Moon DH, Tsai SM, Lee H, Trevors JT. Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J Microbiol Methods. 2000;39(2):159–169. doi:10.1016/S0167-7012(99)00110-4.
  • Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B, Nielsen J, Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498(7452):99–103. doi:10.1038/nature12198.
  • Karlsson FH, Fåk F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, Bäckhed F, Nielsen J. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3(1):1245. doi:10.1038/ncomms2266.
  • Peng Y, Leung HC, Yiu SM, Chin FY. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinform (Oxford, England). 2012;28(11):1420–1428. doi:10.1093/bioinformatics/bts174.
  • IDBA-UD package. http://i.cs.hku.hk/~alse/hkubrg/projects/idba_ud/
  • Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinform (Oxford, England). 2006;22(13):1658–1659. doi:10.1093/bioinformatics/btl158.
  • Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinform (Oxford, England). 2012;28(23):3150–3152. doi:10.1093/bioinformatics/bts565.
  • Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–841. doi:10.1038/nbt.2942.
  • Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi:10.1038/nature08821.
  • Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N, Pan Y, Li J, Zhu L, Wang X, et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat Commun. 2013;4(1):2151. doi:10.1038/ncomms3151.
  • Villar E, Farrant GK, Follows M, Garczarek L, Speich S, Audic S, Bittner L, Blanke B, Brum JR, Brunet C, et al. Ocean plankton. Environmental characteristics of agulhas rings affect interocean plankton transport. Sci. 2015;348(6237):1261447. doi:10.1126/science.1261447.
  • Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60. doi:10.1038/nmeth.3176.
  • White JR, Nagarajan N, Pop M, Ouzounis CA. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol. 2009;5(4):e1000352. doi:10.1371/journal.pcbi.1000352.