β-Glucans in food modify colonic microflora by inducing antimicrobial protein, calprotectin, in a Dectin-1-induced-IL-17F-dependent manner

Mucosal Immunology

Volumn 11, Issue 3, 2018, Pages 763-773

  Kamiya, T ^a,b   Tang, C ^a,b,c   Kadoki, M ^a,b   Oshima, K ^a   Hattori, M ^a   Saijo, S ^a,d   Adachi, Y ^e   Ohno, N ^e   Iwakura, Y ^a,b,c,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d CHIBA UNIVERSITY   (Japan)

^e TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; CALGRANULIN A; CALGRANULIN B; CD11B ANTIGEN; DECTIN 1; DEXTRAN SULFATE; GLYCOPROTEIN P 15095; HETERODIMER; INTERLEUKIN 17F; ANTIINFECTIVE AGENT; CALGRANULIN; INTERLEUKIN 17; LECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BONE MARROW CELL; CLEC7A GENE; COLITIS; COLON FLORA; COLONIC LAMINA PROPRIA; CONTROLLED STUDY; FEMALE; FOOD; HOMEOSTASIS; IL17F GENE; IMMUNOCOMPETENT CELL; INNATE IMMUNE CELL; INTESTINAL HOMEOSTASIS; LACTOBACILLUS; LACTOBACILLUS MURINUS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLON; GENETICS; IMMUNOLOGY; INTESTINE FLORA; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTI-INFECTIVE AGENTS; BETA-GLUCANS; CALGRANULIN A; COLITIS; COLON; FOOD; GASTROINTESTINAL MICROBIOME; HOST MICROBIAL INTERACTIONS; INTERLEUKIN-17; INTESTINAL MUCOSA; LACTOBACILLUS; LECTINS, C-TYPE; LEUKOCYTE L1 ANTIGEN COMPLEX; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS;

EID: 85048013797     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2017.86     Document Type: Article

References (46)

1. Round, J. L. &Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-23 (2009).
2. Iliev, I. D. et al. Interactions between commensal fungi and the c-type lectin receptor Dectin-1 influence colitis. Science 336, 1314-1317 (2012).
3. O'Hara, A. M. &Shanahan, F. The gut flora as a forgotten organ. EMBO Rep. 7, 688-93 (2006).
4. Cash, H. L., Whitham, C. V, Behrendt, C. L. &Hooper, L. V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-30 (2006).
5. Hooper, L. V., Stappenbeck, T. S., Hong, C. V &Gordon, J. I.Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol. 4, 269-73 (2003).
6. Ivanov, I. I. &Honda, K. Intestinal commensal microbes as immune modulators. Cell Host Microbe 12, 496-508 (2012).
7. Kosiewicz, M. M., Zirnheld, A. L. &Alard, P. Gut microbiota, immunity, and disease: a complex relationship. Front. Microbiol. 2, 180 (2011).
8. Guarner, F. Enteric flora in health and disease. Digestion 73, 5-12 (2006).
9. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. &Medzhitov, R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229-41 (2004).
10. Maloy, K. J. &Powrie, F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298-306 (2011).
11. Figuredor, C. G., Kooyk, Y., Van, &Adema, G. J. C-type lectin receptors on decdritic cells and langerhans cells. Nat. Rev. Immunol. 2, 77-84 (2002).
12. Marakalala, M. J., Graham, L. M. &Brown, G. D. The role of Syk/CARD9-coupled C-type lectin receptors in immunity to Mycobacterium tuberculosis infections. Clin. Dev. Immunol. 2010, 567571 (2010).
13. Saijo, S. &Iwakura, Y. Dectin-1 and Dectin-2 in innate immunity against fungi. Int. Immunol. 23, 467-72 (2011).
14. Saijo, S. et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32, 681-691 (2010).
15. Yonekawa, A. et al. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 41, 402-413 (2014).
16. Brown, G. D. et al. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196, 407-412 (2002).
17. Taylor, P. R. et al. Dectin-1 is required for b-Glucan recognition and control of fungal infection. Nat. Immunol. 8, 31-8 (2007).
18. Saijo, S. et al. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat. Immunol. 8, 39-46 (2007).
19. Hiemstra, P. S. Epithelial antimicrobial peptides and proteins: their role in host defence and inflammation. Paediatr. Respir. Rev. 2, 306-310 (2001).
20. Kolls, J. K., McCray, P. B. &Chan, Y. R. Cytokine-mediated regulation of antimicrobial proteins. Nat. Rev. Immunol. 8, 829-835 (2008).
21. Ganz, T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-20 (2003).
22. Lai, Y. &Gallo, R. L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 30, 131-141 (2009).
23. Cua, D. J. &Tato, C. M. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10, 479-489 (2010).
24. Ishigame, H. et al. Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30, 108-119 (2008).
25. Tang, C. et al. Inhibition ofDectin-1 signaling ameliorates colitis by inducing lactobacillus-mediated regulatory T cell expansion in the intestine. Cell Host Microbe 18, 183-197 (2015).
26. Viemann, D. et al. Myeloid-related proteins 8 and 14 induce a specific inflammatory response in human microvascular endothelial cells. Blood 105, 2955-2962 (2005).
27. Pilling, D., Fan, T., Huang, D., Kaul, B. &Gomer, R. H. Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS ONE 4, e7475 (2009).
28. Zindl, C. L. et al. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc. Natl. Acad. Sci. USA 110, 12768-73 (2013).
29. Corbin, B. D. et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965 (2008).
30. Vogl, T. et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13, 1042-1049 (2007).
31. Xu, K., Geczy, C. L. &Sa, C. S. P. IFN-g and TNF regulate macrophage expression of the chemotactic S100 protein S100A8. J. Immunol. 164, 4916-4923 (2000).
32. Song, X. et al. IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat. Immunol. 12, 1151-8 (2011).
33. Reid, D.M., Gow, N.A. &Brown, G. D. Pattern recognition: recent insights from Dectin-1. Curr. Opin. Immunol. 21, 30-7 (2009).
34. Kanagawa, M., Satoh, T., Ikeda, A., Adachi, Y., Ohno, N. &Yamaguchi, Y. Structural insights into recognition of triple-helical beta-glucans by an insect fungal receptor. J. Biol. Chem. 286, 29158-65 (2011).
35. Saito , H., Ohki, T. &Sasaki, T. A 13C nuclear magnetic resonance study of gel-forming (1 goes to 3)-beta-d-glucans. Evidence of the presence of single-helical conformation in a resilient gel of a curdlan-type polysaccharide 13140 from Alcaligenes faecalis var. myxogenes IFO 13140. Biochemistry 16, 908-14 (1977).
36. Phillips, K. R. et al. Production of curdlan-type polysaccharide by Alcaligenes faecalis in batch and continuous culture. Can. J. Microbiol. 29, 1331-8 (1983).
37. Ehrchen, J. M., Sunderkö tter, C., Foell, D., Vogl, T. &Roth, J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J. Leukoc. Biol. 86, 557-66 (2009).
38. Wu, H.-J. et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32, 815-27 (2010).
39. Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11, 76-83 (2010).
40. Petnicki-ocwieja, T., Hrncir, T., Liu, Y., Biswas, A. &Hudcovic, T. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc. Natl. Acad. Sci. USA 106, 15813-15818 (2009).
41. Gessner,M.A et al. Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect. Immun. 80, 410-417 (2012).
42. Cayatte, C. et al. Biomarkers of therapeutic response in the IL-23 pathway in inflammatory bowel disease. Clin. Transl. Gastroenterol. 3, e10 (2012).
43. Hessian, P.A., Edgeworth, J &Hogg,NMRP-8 and MRP-14, two abundant Ca(2)-binding proteins of neutrophils and monocytes. J. Leukoc. Biol. 53, 197-204 (1993).
44. Nakae, S. et al. Antigen-specific T cell sensitization is impaired in Il-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17, 375-387 (2002).
45. Gordon, D. et al. Automated finishing with Autofinish. Genome Res. 11, 614-625 (2001).
46. Obermeier, F. et al. CpG motifs of bacterial DNA exacerbate colitis of dextran sulfate sodium-treated mice. Eur. J. Immunol. 32, 2084-2092 (2002).