IgA regulates the composition and metabolic function of gut microbiota by promoting symbiosis between bacteria

Journal of Experimental Medicine

Volumn 215, Issue 8, 2018, Pages 2019-2034

  Nakajima, Akira ^a   Vogelzang, Alexis ^b   Maruya, Mikako ^b   Miyajima, Michio ^b   Murata, Megumi ^a   Son, Aoi ^a   Kuwahara, Tomomi ^c   Tsuruyama, Tatsuaki ^a   Yamada, Satoshi ^a   Matsuura, Minoru ^a   Nakase, Hiroshi ^a,d   Peterson, Daniel A ^e   Fagarasan, Sidonia ^b   Suzuki, Keiichiro ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b Institute of Physical and Chemical Research   (Japan)

^c KAGAWA UNIVERSITY   (Japan)

^d SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; LIPOPOLYSACCHARIDE; MAFF PROTEIN, MOUSE; MONOCLONAL ANTIBODY; NUCLEAR PROTEIN; OVALBUMIN; TRANSCRIPTION FACTOR MAFF;

ADULT; AGED; ANIMAL; BACTERIUM; BACTEROIDES; BIOLOGICAL MODEL; C57BL MOUSE; COLON; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; HOMEOSTASIS; HUMAN; INTESTINE FLORA; MALE; METABOLISM; MIDDLE AGED; MUCUS; PHENOTYPE; PHYSIOLOGY; SYMBIOSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODIES, MONOCLONAL; BACTERIA; BACTEROIDES; COLON; FEMALE; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOSYLATION; HOMEOSTASIS; HUMANS; IMMUNOGLOBULIN A; LIPOPOLYSACCHARIDES; MAFF TRANSCRIPTION FACTOR; MALE; MICE, INBRED C57BL; MIDDLE AGED; MODELS, BIOLOGICAL; MUCUS; NUCLEAR PROTEINS; OVALBUMIN; PHENOTYPE; SYMBIOSIS;

EID: 85053769565     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20180427     Document Type: Article

References (56)

1. Anders, S., P.T. Pyl, and W. Huber. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics. 31:166–169. https://doi.org/10.1093/bioinformatics/btu638
2. Artis, D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8:411–420. https://doi.org/10.1038/nri2316
3. Bäckhed, F., R.E. Ley, J.L. Sonnenburg, D.A. Peterson, and J.I. Gordon. 2005. Host-bacterial mutualism in the human intestine. Science. 307:1915–1920. https://doi.org/10.1126/science.1104816
4. Belkaid, Y., and T.W. Hand. 2014. Role of the microbiota in immunity and inflammation. Cell. 157:121–141. https://doi.org/10.1016/j.cell.2014.03.011
5. Bloom, S.M., V.N. Bijanki, G.M. Nava, L. Sun, N.P. Malvin, D.L. Donermeyer, W.M. Dunne Jr., P.M. Allen, and T.S. Stappenbeck. 2011. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. CellHostMicrobe. 9:390–403. https://doi.org/10.1016/j.chom.2011.04.009
6. Bunker, J.J., T.M. Flynn, J.C. Koval, D.G. Shaw, M. Meisel, B.D. McDonald, I.E. Ishizuka, A.L. Dent, P.C. Wilson, B. Jabri, et al. 2015. Innate and Adaptive Humoral Responses Coat Distinct Commensal Bacteria with Immunoglobulin A. Immunity. 43:541–553. https://doi.org/10.1016/j.immuni.2015.08.007
7. Bunker, J.J., S.A. Erickson, T.M. Flynn, C. Henry, J.C. Koval, M. Meisel, B. Jabri, D.A. Antonopoulos, P.C. Wilson, and A. Bendelac. 2017. Natural polyreactive IgA antibodies coat the intestinal microbiota. Science. 358:eaan6619. https://doi.org/10.1126/science.aan6619
8. Caporaso, J.G., J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Peña, J.K. Goodrich, J.I. Gordon, et al. 2010. QII ME allows analysis of high-throughput community sequencing data. Nat. Methods. 7:335–336. https://doi.org/10.1038/nmeth.f.303
9. De Filippo, C., D. Cavalieri, M. Di Paola, M. Ramazzotti, J.B. Poullet, S. Massart, S. Collini, G. Pieraccini, and P. Lionetti. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA. 107:14691–14696. https://doi.org/10.1073/pnas.1005963107
10. Donaldson, G.P., M.S. Ladinsky, K.B. Yu, J.G. Sanders, B.B. Yoo, W.C. Chou, M.E. Conner, A.M. Earl, R. Knight, P.J. Bjorkman, and S.K. Mazmanian. 2018. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science. 360:795–800. https://doi.org/10.1126/science.aaq0926
11. Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
12. Edgar, R.C., B.J. Haas, J.C. Clemente, C. Quince, and R. Knight. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
13. Fadlallah, J., H. El Kafsi, D. Sterlin, C. Juste, C. Parizot, K. Dorgham, G. Autaa, D. Gouas, M. Almeida, P. Lepage, et al. 2018. Microbial ecology perturbation in human IgA deficiency. Sci. Transl. Med. 10:eaan1217. https://doi.org/10 .1126/scitranslmed.aan1217
14. Fagarasan, S., M. Muramatsu, K. Suzuki, H. Nagaoka, H. Hiai, and T. Honjo. 2002. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science. 298:1424–1427. https://doi.org/10.1126/science.1077336
15. Glenwright, A.J., K.R. Pothula, S.P. Bhamidimarri, D.S. Chorev, A. Baslé, S.J. Firbank, H. Zheng, C.V. Robinson, M. Winterhalter, U. Kleinekathöfer, et al. 2017. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 541:407–411. https://doi.org/10.1038/nature20828
16. Goodrich, J.K., J.L. Waters, A.C. Poole, J.L. Sutter, O. Koren, R. Blekhman, M. Beaumont, W. Van Treuren, R. Knight, J.T. Bell, et al. 2014. Human genetics shape the gut microbiome. Cell. 159:789–799. https://doi.org/10.1016/j.cell.2014.09.053
17. Huang, J., A. Guerrero, E. Parker, J.S. Strum, J.T. Smilowitz, J.B. German, and C.B. Lebrilla. 2015. Site-specific glycosylation of secretory immunoglobulin A from human colostrum. J. Proteome Res. 14:1335–1349. https://doi.org/10.1021/pr500826q
18. Huang, W., B.T. Sherman, and R.A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44–57. https://doi.org/10.1038/nprot.2008.211
19. Inoue, K., J. Wada, J. Eguchi, A. Nakatsuka, S. Teshigawara, K. Murakami, D. Ogawa, T. Terami, A. Katayama, A. Tone, et al. 2013. Urinary fetuin-A is a novel marker for diabetic nephropathy in type 2 diabetes identified by lectin microarray. PLoSOne. 8:e77118. https://doi.org/10.1371/journal.pone.0077118
20. Johansson, M.E., M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G.C. Hansson. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA. 105:15064–15069. https://doi.org/10.1073/pnas.0803124105
21. Kawamoto, S., T.H. Tran, M. Maruya, K. Suzuki, Y. Doi, Y. Tsutsui, L.M. Kato, and S. Fagarasan. 2012. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science. 336:485–489. https://doi.org/10.1126/science.1217718
22. Kawamoto, S., M. Maruya, L.M. Kato, W. Suda, K. Atarashi, Y. Doi, Y. Tsutsui, H. Qin, K. Honda, T. Okada, et al. 2014. Foxp3(+) T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity. 41:152–165. https://doi.org/10.1016/j.immuni.2014.05.016
23. Kersey, P.J., J.E. Allen, I. Armean, S. Boddu, B.J. Bolt, D. Carvalho-Silva, M. Christensen, P. Davis, L.J. Falin, C. Grabmueller, et al. 2016. Ensembl Genomes 2016: more genomes, more complexity. Nucleic Acids Res. 44(D1):D574–D580. https://doi.org/10.1093/nar/gkv1209
24. Koropatkin, N.M., E.A. Cameron, and E.C. Martens. 2012. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10:323–335. https://doi.org/10.1038/nrmicro2746
25. Lécuyer, E., S. Rakotobe, H. Lengliné-Garnier, C. Lebreton, M. Picard, C. Juste, R. Fritzen, G. Eberl, K.D. McCoy, A.J. Macpherson, et al. 2014. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity. 40:608–620. https://doi.org/10.1016/j.immuni.2014.03.009
26. Lee, S.M., G.P. Donaldson, Z. Mikulski, S. Boyajian, K. Ley, and S.K. Mazmanian. 2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature. 501:426–429. https://doi.org/10.1038/ nature12447
27. Li, H.2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM.arXiv.https://arxiv.org/abs/1303.3997 (Preprint posted May 26, 2013)
28. Li, H., J.P. Limenitakis, T. Fuhrer, M.B. Geuking, M.A. Lawson, M. Wyss, S. Brugiroux, I. Keller, J.A. Macpherson, S. Rupp, et al. 2015. The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun. 6:8292. https://doi.org/10.1038/ncomms9292
29. Love, M.I., W. Huber, and S. Anders. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550. https://doi.org/10.1186/s13059-014-0550-8
30. Macfarlane, S., and G.T. Macfarlane. 2003. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 62:67–72. https://doi.org/10.1079/ PNS2002207
31. Manz, W., R. Amann, W. Ludwig, M. Vancanneyt, and K.H. Schleifer. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroi-des in the natural environment. Microbiology. 142:1097–1106. https://doi.org/10.1099/13500872-142-5-1097
32. Martens, E.C., H.C. Chiang, and J.I. Gordon. 2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe. 4:447–457. https://doi.org/10.1016/j.chom.2008.09.007
33. Martin, J., S. Sykes, S. Young, K. Kota, R. Sanka, N. Sheth, J. Orvis, E. Soder-gren, Z. Wang, G.M. Weinstock, and M. Mitreva. 2012. Optimizing read mapping to reference genomes to determine composition and species prevalence in microbial communities. PLoS One. 7:e36427. https://doi.org/10.1371/journal.pone.0036427
34. Maslowski, K.M., A.T. Vieira, A. Ng, J. Kranich, F. Sierro, D. Yu, H.C. Schilter, M.S. Rolph, F. Mackay, D. Artis, et al. 2009. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 461:1282–1286. https://doi.org/10.1038/nature08530
35. Mathias, A., and B. Corthésy. 2011. Recognition of gram-positive intestinal bacteria by hybridoma- and colostrum-derived secretory immunoglobulin A is mediated by carbohydrates. J. Biol. Chem. 286:17239–17247. https://doi.org/10.1074/jbc.M110.209015
36. Maurice, C.F., H.J. Haiser, and P.J. Turnbaugh. 2013. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell. 152:39–50. https://doi.org/10.1016/j.cell.2012.10.052
37. McLoughlin, K., J. Schluter, S. Rakoff-Nahoum, A.L. Smith, and K.R. Foster. 2016. Host Selection of Microbiota via Differential Adhesion. Cell Host Microbe. 19:550–559. https://doi.org/10.1016/j.chom.2016.02.021
38. Meyer, F., D. Paarmann, M. D’Souza, R. Olson, E.M. Glass, M. Kubal, T. Paczian, A. Rodriguez, R. Stevens, A. Wilke, et al. 2008. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics. 9:386. https://doi.org/10.1186/1471-2105-9-386
39. Momose, Y., S.H. Park, Y. Miyamoto, and K. Itoh. 2011. Design of species-specific oligonucleotide probes for the detection of Bacteroides and Parabacteroides by fluorescence in situ hybridization and their application to the analysis of mouse caecal Bacteroides-Parabacteroides microbiota. J. Appl. Microbiol. 111:176–184. https://doi.org/10.1111/j.1365-2672.2011.05039.x
40. Morteau, O., S.G. Morham, R. Sellon, L.A. Dieleman, R. Langenbach, O. Smithies, and R.B. Sartor. 2000. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J. Clin. Invest. 105:469–478. https://doi.org/10.1172/JCI6899
41. Nakayama-Imaohji, H., H. Hirakawa, M. Ichimura, S. Wakimoto, S. Kuhara, T. Hayashi, and T. Kuwahara. 2009. Identification of the site-specific DNA invertase responsible for the phase variation of SusC/SusD family outer membrane proteins in Bacteroides fragilis. J. Bacteriol. 191:6003–6011. https://doi.org/10.1128/JB.00687-09
42. Odamaki, T., J.Z. Xiao, M. Sakamoto, S. Kondo, T. Yaeshima, K. Iwatsuki, H. Togashi, T. Enomoto, and Y. Benno. 2008. Distribution of different species of the Bacteroides fragilis group in individuals with Japanese cedar pollinosis. Appl. Environ. Microbiol. 74:6814–6817. https://doi.org/10.1128/AEM.01106-08
43. Peterson, D.A., N.P. McNulty, J.L. Guruge, and J.I. Gordon. 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. CellHostMicrobe. 2:328–339. https://doi.org/10.1016/j.chom.2007.09.013
44. Plöger, S., F. Stumpff, G.B. Penner, J.D. Schulzke, G. Gäbel, H. Martens, Z. Shen, D. Günzel, and J.R. Aschenbach. 2012. Microbial butyrate and its role for barrier function in the gastrointestinal tract. Ann. N. Y. Acad. Sci. 1258:52–59. https://doi.org/10.1111/j.1749-6632.2012.06553.x
45. Pylro, V.S., L.F. Roesch, D.K. Morais, I.M. Clark, P.R. Hirsch, and M.R. Tótola. 2014. Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J. Microbiol. Methods. 107:30–37. https://doi.org/10.1016/j.mimet.2014.08.018
46. Rogier, E.W., A.L. Frantz, M.E. Bruno, and C.S. Kaetzel. 2014. Secretory IgA is Concentrated in the Outer Layer of Colonic Mucus along with Gut Bacteria. Pathogens. 3:390–403. https://doi.org/10.3390/pathogens3020390
47. Royle, L., A. Roos, D.J. Harvey, M.R. Wormald, D. van Gijlswijk-Janssen, R.M. Redwan, I.A. Wilson, M.R. Daha, R.A. Dwek, and P.M. Rudd. 2003. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 278:20140–20153. https://doi.org/10.1074/jbc.M301436200
48. Suzuki, K., B. Meek, Y. Doi, M. Muramatsu, T. Chiba, T. Honjo, and S. Fagarasan. 2004. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. USA. 101:1981–1986. https://doi.org/10.1073/pnas.0307317101
49. Talham, G.L., H.Q. Jiang, N.A. Bos, and J.J. Cebra. 1999. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the mu-rine gut mucosal immune system. Infect. Immun. 67:1992–2000.
50. Tong, J., C. Liu, P. Summanen, H. Xu, and S.M. Finegold. 2011. Application of quantitative real-time PCR for rapid identification of Bacteroides fragilis group and related organisms in human wound samples. Anaerobe. 17:64–68. https://doi.org/10.1016/j.anaerobe.2011.03.004
51. Tsukahara, T., N. Matsukawa, S. Tomonaga, R. Inoue, K. Ushida, and K. Ochiai. 2014. High-sensitivity detection of short-chain fatty acids in porcine ileal, cecal, portal and abdominal blood by gas chromatography-mass spectrometry. Anim. Sci. J. 85:494–498. https://doi.org/10.1111/asj.12188
52. Turner, S., K.M. Pryer, V.P. Miao, and J.D. Palmer. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46:327–338. https://doi.org/10.1111/j.1550-7408.1999.tb04612.x
53. Umesaki, Y., Y. Okada, S. Matsumoto, A. Imaoka, and H. Setoyama. 1995. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol. Immunol. 39:555–562. https://doi.org/10.1111/j.1348-0421.1995.tb02242.x
54. van der Waaij, L.A., P.C. Limburg, G. Mesander, and D. van der Waaij. 1996. In vivo IgA coating of anaerobic bacteria in human faeces. Gut. 38:348–354. https://doi.org/10.1136/gut.38.3.348
55. Weller, R., F.O. Glöckner, and R. Amann. 2000. 16S rRNA-targeted oligonucleotide probes for the in situ detection of members of the phylum Cy-tophaga-Flavobacterium-Bacteroides. Syst. Appl. Microbiol. 23:107–114. https://doi.org/10.1016/S0723-2020(00)80051-X
56. Wilke, A., J. Bischof, T. Harrison, T. Brettin, M. D’Souza, W. Gerlach, H. Matthews, T. Paczian, J. Wilkening, E.M. Glass, et al. 2015. A RESTful API for accessing microbial community data for MG-RAST. PLOS Comput. Biol. 11:e1004008. https://doi.org/10.1371/journal.pcbi.1004008