Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen

Cell Host and Microbe

Volumn 16, Issue 4, 2014, Pages 504-516

  Pham, Tu Anh N ^a   Clare, Simon ^a   Goulding, David ^a   Arasteh, Julia M ^a   Stares, Mark D ^a   Browne, Hilary P ^a   Keane, Jacqueline A ^a   Page, Andrew J ^a   Kumasaka, Natsuhiko ^a   Kane, Leanne ^a   Mottram, Lynda ^a   Harcourt, Katherine ^a   Hale, Christine ^a   Arends, Mark J ^b   Gaffney, Daniel J ^a   Dougan, Gordon ^a   Lawley, Trevor D ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84908075358     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.08.017     Document Type: Article

References (50)

1. C.A. Arias, and B.E. Murray The rise of the Enterococcus: beyond vancomycin resistance Nat. Rev. Microbiol. 10 2012 266 278
2. S.J. Aujla, Y.R. Chan, M. Zheng, M. Fei, D.J. Askew, D.A. Pociask, T.A. Reinhart, F. McAllister, J. Edeal, and K. Gaus IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia Nat. Med. 14 2008 275 281
3. D.J. Becker, and J.B. Lowe Fucose: biosynthesis and biological function in mammals Glycobiology 13 2003 41R 53R
4. J. Behnsen, S. Jellbauer, C.P. Wong, R.A. Edwards, M.D. George, W. Ouyang, and M. Raffatellu The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria Immunity 40 2014 262 273
5. J.L. Benjamin, R. Sumpter Jr., B. Levine, and L.V. Hooper Intestinal epithelial autophagy is essential for host defense against invasive bacteria Cell Host Microbe 13 2013 723 734
6. A. Bourgogne, D.A. Garsin, X. Qin, K.V. Singh, J. Sillanpaa, S. Yerrapragada, Y. Ding, S. Dugan-Rocha, C. Buhay, and H. Shen Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF Genome Biol. 9 2008 R110
7. L. Bry, P.G. Falk, T. Midtvedt, and J.I. Gordon A model of host-microbial interactions in an open mammalian ecosystem Science 273 1996 1380 1383
8. H.L. Cash, C.V. Whitham, C.L. Behrendt, and L.V. Hooper Symbiotic bacteria direct expression of an intestinal bactericidal lectin Science 313 2006 1126 1130
9. S. Clare, R. Goldin, C. Hale, R. Aspinall, C. Simmons, P. Mastroeni, and G. Dougan Intracellular adhesion molecule 1 plays a key role in acquired immunity to salmonellosis Infect. Immun. 71 2003 5881 5891
10. B.L. Deatherage Kaiser, J. Li, J.A. Sanford, Y.M. Kim, S.R. Kronewitter, M.B. Jones, C.T. Peterson, S.N. Peterson, B.C. Frank, and S.O. Purvine A Multi-Omic View of Host-Pathogen-Commensal Interplay in Salmonella-Mediated Intestinal Infection PLoS ONE 8 2013 e67155
11. S. Eyre, J. Bowes, D. Diogo, A. Lee, A. Barton, P. Martin, A. Zhernakova, E. Stahl, S. Viatte, K. McAllister Biologics in Rheumatoid Arthritis Genetics and Genomics Study Syndicate Wellcome Trust Case Control Consortium High-density genetic mapping identifies new susceptibility loci for rheumatoid arthritis Nat. Genet. 44 2012 1336 1340
12. B. Feinen, and M.W. Russell Contrasting Roles of IL-22 and IL-17 in Murine Genital Tract Infection by Neisseria gonorrhoeae Front Immunol. 3 2012 11
13. A.C. Graham, K.D. Carr, A.N. Sieve, M. Indramohan, T.J. Break, and R.E. Berg IL-22 production is regulated by IL-23 during Listeria monocytogenes infection but is not required for bacterial clearance or tissue protection PLoS ONE 6 2011 e17171
14. L.V. Hooper, and J.I. Gordon Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity Glycobiology 11 2001 1R 10R
15. M.M. Huycke, C.A. Spiegel, and M.S. Gilmore Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis Antimicrob. Agents Chemother. 35 1991 1626 1634
16. D. Ilver, A. Arnqvist, J. Ogren, I.M. Frick, D. Kersulyte, E.T. Incecik, D.E. Berg, A. Covacci, L. Engstrand, and T. Borén Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging Science 279 1998 373 377
17. B.D. Jett, M.M. Huycke, and M.S. Gilmore Virulence of enterococci Clin. Microbiol. Rev. 7 1994 462 478
18. L. Jostins, S. Ripke, R.K. Weersma, R.H. Duerr, D.P. McGovern, K.Y. Hui, J.C. Lee, L.P. Schumm, Y. Sharma, C.A. Anderson International IBD Genetics Consortium (IIBDGC) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease Nature 491 2012 119 124
19. P.C. Kashyap, A. Marcobal, L.K. Ursell, S.A. Smits, E.D. Sonnenburg, E.K. Costello, S.K. Higginbottom, S.E. Domino, S.P. Holmes, and D.A. Relman Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota Proc. Natl. Acad. Sci. USA 110 2013 17059 17064
20. R.J. Kelly, S. Rouquier, D. Giorgi, G.G. Lennon, and J.B. Lowe Sequence and expression of a candidate for the human Secretor blood group alpha(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype J. Biol. Chem. 270 1995 4640 4649
21. M.A. Kinnebrew, C. Ubeda, L.A. Zenewicz, N. Smith, R.A. Flavell, and E.G. Pamer Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection J. Infect. Dis. 201 2010 534 543
22. T.D. Lawley, S. Clare, A.W. Walker, M.D. Stares, T.R. Connor, C. Raisen, D. Goulding, R. Rad, F. Schreiber, and C. Brandt Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice PLoS Pathog. 8 2012 e1002995
23. L. Lindesmith, C. Moe, S. Marionneau, N. Ruvoen, X. Jiang, L. Lindblad, P. Stewart, J. LePendu, and R. Baric Human susceptibility and resistance to Norwalk virus infection Nat. Med. 9 2003 548 553
24. C. Lupp, M.L. Robertson, M.E. Wickham, I. Sekirov, O.L. Champion, E.C. Gaynor, and B.B. Finlay Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae Cell Host Microbe 2 2007 204
25. A. Marcobal, M. Barboza, E.D. Sonnenburg, N. Pudlo, E.C. Martens, P. Desai, C.B. Lebrilla, B.C. Weimer, D.A. Mills, J.B. German, and J.L. Sonnenburg Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways Cell Host Microbe 10 2011 507 514
26. 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
27. S.M. McBride, V.A. Fischetti, D.J. Leblanc, R.C. Moellering Jr., and M.S. Gilmore Genetic diversity among Enterococcus faecalis PLoS ONE 2 2007 e582
28. D.P. McGovern, M.R. Jones, K.D. Taylor, K. Marciante, X. Yan, M. Dubinsky, A. Ippoliti, E. Vasiliauskas, D. Berel, C. Derkowski International IBD Genetics Consortium Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease Hum. Mol. Genet. 19 2010 3468 3476
29. K.M. Ng, J.A. Ferreyra, S.K. Higginbottom, J.B. Lynch, P.C. Kashyap, S. Gopinath, N. Naidu, B. Choudhury, B.C. Weimer, D.M. Monack, and J.L. Sonnenburg Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens Nature 502 2013 96 99
30. I.T. Paulsen, L. Banerjei, G.S. Myers, K.E. Nelson, R. Seshadri, T.D. Read, D.E. Fouts, J.A. Eisen, S.R. Gill, and J.F. Heidelberg Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis Science 299 2003 2071 2074
31. M. Raffatellu, R.L. Santos, D.E. Verhoeven, M.D. George, R.P. Wilson, S.E. Winter, I. Godinez, S. Sankaran, T.A. Paixao, and M.A. Gordon Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut Nat. Med. 14 2008 421 428
32. G.M. Ruiz-Palacios, L.E. Cervantes, P. Ramos, B. Chavez-Munguia, and D.S. Newburg Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection J. Biol. Chem. 278 2003 14112 14120
33. R. Sabat, W. Ouyang, and K. Wolk Therapeutic opportunities of the IL-22-IL-22R1 system Nat. Rev. Drug Discov. 13 2014 21 38
34. T. Sato, D.E. Stange, M. Ferrante, R.G. Vries, J.H. Van Es, S. Van den Brink, W.J. Van Houdt, A. Pronk, J. Van Gorp, P.D. Siersema, and H. Clevers Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium Gastroenterology 141 2011 1762 1772
35. P.D. Schloss, S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, B.B. Oakley, D.H. Parks, and C.J. Robinson Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities Appl. Environ. Microbiol. 75 2009 7537 7541
36. N. Shankar, A.S. Baghdayan, and M.S. Gilmore Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis Nature 417 2002 746 750
37. W.C. Skarnes, B. Rosen, A.P. West, M. Koutsourakis, W. Bushell, V. Iyer, A.O. Mujica, M. Thomas, J. Harrow, and T. Cox A conditional knockout resource for the genome-wide study of mouse gene function Nature 474 2011 337 342
38. G.F. Sonnenberg, L.A. Fouser, and D. Artis Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22 Nat. Immunol. 12 2011 383 390
39. B. Stecher, and W.D. Hardt The role of microbiota in infectious disease Trends Microbiol. 16 2008 107 114
40. B. Stecher, and W.D. Hardt Mechanisms controlling pathogen colonization of the gut Curr. Opin. Microbiol. 14 2011 82 91
41. B. Stecher, R. Robbiani, A.W. Walker, A.M. Westendorf, M. Barthel, M. Kremer, S. Chaffron, A.J. Macpherson, J. Buer, and J. Parkhill Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota PLoS Biol. 5 2007 2177 2189
42. C. Ubeda, V. Bucci, S. Caballero, A. Djukovic, N.C. Toussaint, M. Equinda, L. Lipuma, L. Ling, A. Gobourne, and D. No Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization Infect. Immun. 81 2013 965 973
43. S. Vaishnava, M. Yamamoto, K.M. Severson, K.A. Ruhn, X. Yu, O. Koren, R. Ley, E.K. Wakeland, and L.V. Hooper The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine Science 334 2011 255 258
44. J.K. White, A.K. Gerdin, N.A. Karp, E. Ryder, M. Buljan, J.N. Bussell, J. Salisbury, S. Clare, N.J. Ingham, C. Podrini Sanger Institute Mouse Genetics Project Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes Cell 154 2013 452 464
45. S. Wiles, K.M. Pickard, K. Peng, T.T. MacDonald, and G. Frankel In vivo bioluminescence imaging of the murine pathogen Citrobacter rodentium Infect. Immun. 74 2006 5391 5396
46. M.S. Wilson, C.G. Feng, D.L. Barber, F. Yarovinsky, A.W. Cheever, A. Sher, M. Grigg, M. Collins, L. Fouser, and T.A. Wynn Redundant and pathogenic roles for IL-22 in mycobacterial, protozoan, and helminth infections J. Immunol. 184 2010 4378 4390
47. S.E. Winter, M.G. Winter, M.N. Xavier, P. Thiennimitr, V. Poon, A.M. Keestra, R.C. Laughlin, G. Gomez, J. Wu, and S.D. Lawhon Host-derived nitrate boosts growth of E. coli in the inflamed gut Science 339 2013 708 711
48. K. Wolk, S. Kunz, E. Witte, M. Friedrich, K. Asadullah, and R. Sabat IL-22 increases the innate immunity of tissues Immunity 21 2004 241 254
49. L.A. Zenewicz, X. Yin, G. Wang, E. Elinav, L. Hao, L. Zhao, and R.A. Flavell IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic J. Immunol. 190 2013 5306 5312
50. Y. Zheng, P.A. Valdez, D.M. Danilenko, Y. Hu, S.M. Sa, Q. Gong, A.R. Abbas, Z. Modrusan, N. Ghilardi, F.J. de Sauvage, and W. Ouyang Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens Nat. Med. 14 2008 282 289