Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles

Cell Host and Microbe

Volumn 17, Issue 5, 2015, Pages 672-680

  Hickey, Christina A ^a   Kuhn, Kristine A ^a,d   Donermeyer, David L ^a   Porter, Nathan T ^b   Jin, Chunsheng ^c   Cameron, Elizabeth A ^b   Jung, Haerin ^a   Kaiko, Gerard E ^a   Wegorzewska, Marta ^a   Malvin, Nicole P ^a   Glowacki, Robert W P ^b   Hansson, Gunnar C ^c   Allen, Paul M ^a   Martens, Eric C ^b   Stappenbeck, Thaddeus S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTEROIDES THETAIOTAOMICRON ANTIGEN; SULFATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM MUTANT; COLITIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HOST CELL; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IMMUNOSTIMULATION; MEMBRANE VESICLE; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BACTERIAL GENE; BACTEROIDES; CHEMICALLY INDUCED; DISEASE MODEL; ENZYMOLOGY; GENE DELETION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOLOGY; SECRETORY VESICLE;

BACTERIA (MICROORGANISMS); BACTEROIDES THETAIOTAOMICRON; MUS;

ANIMALS; ANTIGENS, BACTERIAL; BACTEROIDES; COLITIS; DISEASE MODELS, ANIMAL; GENE DELETION; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MICE; SECRETORY VESICLES; SULFATASES;

EID: 84929298167     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.04.002     Document Type: Article

References (43)

1. D. Ambort, M.E. Johansson, J.K. Gustafsson, H.E. Nilsson, A. Ermund, B.R. Johansson, P.J. Koeck, H. Hebert, and G.C. Hansson Calcium and pH-dependent packing and release of the gel-forming MUC2 mucin Proc. Natl. Acad. Sci. USA 109 2012 5645 5650
2. C.C. Bain, C.L. Scott, H. Uronen-Hansson, S. Gudjonsson, O. Jansson, O. Grip, M. Guilliams, B. Malissen, W.W. Agace, and A.M. Mowat Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors Mucosal Immunol. 6 2013 498 510
3. S.J. Bauman, and M.J. Kuehn Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response Microbes Infect. 8 2006 2400 2408
4. A. Benjdia, E.C. Martens, J.I. Gordon, and O. Berteau Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron J. Biol. Chem. 286 2011 25973 25982
5. O. Berteau, A. Guillot, A. Benjdia, and S. Rabot A new type of bacterial sulfatase reveals a novel maturation pathway in prokaryotes J. Biol. Chem. 281 2006 22464 22470
6. S.M. Bloom, 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 Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease Cell Host Microbe 9 2011 390 403
7. E.A. Cameron, K.J. Kwiatkowski, B.H. Lee, B.R. Hamaker, N.M. Koropatkin, and E.C. Martens Multifunctional nutrient-binding proteins adapt human symbiotic bacteria for glycan competition in the gut by separately promoting enhanced sensing and catalysis mBio 5 2014 e01441-01414
8. H. Chutkan, I. Macdonald, A. Manning, and M.J. Kuehn Quantitative and qualitative preparations of bacterial outer membrane vesicles Methods Mol. Biol. 966 2013 259 272
9. A.P. Corfield, S.A. Wagner, J.R. Clamp, M.S. Kriaris, and L.C. Hoskins Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria Infect. Immun. 60 1992 3971 3978
10. A.P. Corfield, N. Myerscough, N. Bradfield, Cdo A. Corfield, M. Gough, J.R. Clamp, P. Durdey, B.F. Warren, D.C. Bartolo, K.R. King, and J.M. Williams Colonic mucins in ulcerative colitis: evidence for loss of sulfation Glycoconj. J. 13 1996 809 822
11. W. Elhenawy, M.O. Debelyy, and M.F. Feldman Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles mBio 5 2014 e00909 00914
12. T.N. Ellis, and M.J. Kuehn Virulence and immunomodulatory roles of bacterial outer membrane vesicles Microbiol. Mol. Biol. Rev. 74 2010 81 94
13. H. Gankema, J. Wensink, P.A. Guinée, W.H. Jansen, and B. Witholt Some characteristics of the outer membrane material released by growing enterotoxigenic Escherichia coli Infect. Immun. 29 1980 704 713
14. J.M. Holmén Larsson, K.A. Thomsson, A.M. Rodríguez-Piñeiro, H. Karlsson, and G.C. Hansson Studies of mucus in mouse stomach, small intestine, and colon. III. Gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution Am. J. Physiol. Gastrointest. Liver Physiol. 305 2013 G357 G363
15. F. Housseau, and C.L. Sears Enterotoxigenic Bacteroides fragilis (ETBF)-mediated colitis in Min (Apc+/-) mice: a human commensal-based murine model of colon carcinogenesis Cell Cycle 9 2010 3 5
16. Human Microbiome Project Consortium A framework for human microbiome research Nature 486 2012 215 221
17. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
18. D.A. Hume, V.H. Perry, and S. Gordon The mononuclear phagocyte system of the mouse defined by immunohistochemical localisation of antigen F4/80: macrophages associated with epithelia Anat. Rec. 210 1984 503 512
19. D.A. Hume, W. Allan, J. Golder, R.W. Stephens, W.F. Doe, and H.S. Warren Preparation and characterization of human bone marrow-derived macrophages J. Leukoc. Biol. 38 1985 541 552
20. A.T. Irving, H. Mimuro, T.A. Kufer, C. Lo, R. Wheeler, L.J. Turner, B.J. Thomas, C. Malosse, M.P. Gantier, and L.N. Casillas The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling Cell Host Microbe 15 2014 623 635
21. M.E. Johansson, M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G.C. Hansson The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria Proc. Natl. Acad. Sci. USA 105 2008 15064 15069
22. M.E. Johansson, H. Sjovall, and G.C. Hansson The gastrointestinal mucus system in health and disease Nat. Rev. Gastroenterol. Hepatol. 10 2013 352 361
23. G.E. Kaiko, and T.S. Stappenbeck Host-microbe interactions shaping the gastrointestinal environment Trends Immunol. 35 2014 538 548
24. S.S. Kang, S.M. Bloom, L.A. Norian, M.J. Geske, R.A. Flavell, T.S. Stappenbeck, and P.M. Allen An antibiotic-responsive mouse model of fulminant ulcerative colitis PLoS Med. 5 2008 e41
25. J.F. Kearney, A. Radbruch, B. Liesegang, and K. Rajewsky A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines J. Immunol. 123 1979 1548 1550
26. F. Kuhnert, C.R. Davis, H.T. Wang, P. Chu, M. Lee, J. Yuan, R. Nusse, and C.J. Kuo Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1 Proc. Natl. Acad. Sci. USA 101 2004 266 271
27. A. Kulp, and M.J. Kuehn Biological functions and biogenesis of secreted bacterial outer membrane vesicles Annu. Rev. Microbiol. 64 2010 163 184
28. S.H. Lee, P.M. Starkey, and S. Gordon Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80 J. Exp. Med. 161 1985 475 489
29. G. Lee, L.S. White, K.E. Hurov, T.S. Stappenbeck, and H. Piwnica-Worms Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion Proc. Natl. Acad. Sci. USA 106 2009 4701 4706
30. R. Lev, and S.S. Spicer Specific staining of sulphate groups with alcian blue at low pH J. Histochem. Cytochem. 12 1964 309
31. E.C. Martens, H.C. Chiang, and J.I. Gordon Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont Cell Host Microbe 4 2008 447 457
32. E.C. Martens, R. Roth, J.E. Heuser, and J.I. Gordon Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont J. Biol. Chem. 284 2009 18445 18457
33. N. Mian, C.E. Anderson, and P.W. Kent Effect of O-sulphate groups in lactose and N-acetylneuraminyl-lactose on their enzymic hydrolysis Biochem. J. 181 1979 387 399
34. J.H. Niess, S. Brand, X. Gu, L. Landsman, S. Jung, B.A. McCormick, J.M. Vyas, M. Boes, H.L. Ploegh, and J.G. Fox CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance Science 307 2005 254 258
35. D.K. Podolsky, and K.J. Isselbacher Composition of human colonic mucin. Selective alteration in inflammatory bowel disease J. Clin. Invest. 72 1983 142 153
36. J.L. Round, S.M. Lee, J. Li, G. Tran, B. Jabri, T.A. Chatila, and S.K. Mazmanian The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota Science 332 2011 974 977
37. Y. Shen, M.L. Giardino Torchia, G.W. Lawson, C.L. Karp, J.D. Ashwell, and S.K. Mazmanian Outer membrane vesicles of a human commensal mediate immune regulation and disease protection Cell Host Microbe 12 2012 509 520
38. D.S. Shouval, A. Biswas, J.A. Goettel, K. McCann, E. Conaway, N.S. Redhu, I.D. Mascanfroni, Z. Al Adham, S. Lavoie, and M. Ibourk Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function Immunity 40 2014 706 719
39. L.E. Smythies, M. Sellers, R.H. Clements, M. Mosteller-Barnum, G. Meng, W.H. Benjamin, J.M. Orenstein, and P.D. Smith Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity J. Clin. Invest. 115 2005 66 75
40. J.L. Sonnenburg, J. Xu, D.D. Leip, C.H. Chen, B.P. Westover, J. Weatherford, J.D. Buhler, and J.I. Gordon Glycan foraging in vivo by an intestine-adapted bacterial symbiont Science 307 2005 1955 1959
41. A. Swidsinski, V. Loening-Baucke, H. Lochs, and L.P. Hale Spatial organization of bacterial flora in normal and inflamed intestine: a fluorescence in situ hybridization study in mice World J. Gastroenterol. 11 2005 1131 1140
42. G.M. Tannahill, A.M. Curtis, J. Adamik, E.M. Palsson-McDermott, A.F. McGettrick, G. Goel, C. Frezza, N.J. Bernard, B. Kelly, and N.H. Foley Succinate is an inflammatory signal that induces IL-1β through HIF-1α Nature 496 2013 238 242
43. H.H. Tsai, D. Sunderland, G.R. Gibson, C.A. Hart, and J.M. Rhodes A novel mucin sulphatase from human faeces: its identification, purification and characterization Clin. Sci. 82 1992 447 454