Dectin-3 Deficiency Promotes Colitis Development due to Impaired Antifungal Innate Immune Responses in the Gut

PLoS Pathogens

Volumn 12, Issue 6, 2016, Pages

  Wang, Tingting ^a,b   Pan, Deng ^a,c   Zhou, Zhicheng ^a,c   You, Yun ^a   Jiang, Changying ^a   Zhao, Xueqiang ^d   Lin, Xin ^a,c,d  

^a UNIVERSITY OF TEXAS   (United States)

^b NANJING UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS   (United States)

^d Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DECTIN 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LECTIN RECEPTOR; UNCLASSIFIED DRUG; CLEC4D PROTEIN, MOUSE; DEXTRAN SULFATE; IMMUNOGLOBULIN RECEPTOR; LECTIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA TROPICALIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; IMMUNOREGULATION; INNATE IMMUNITY; LAMINA PROPRIA; MOUSE; MYCOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN INTERACTION; ULCERATIVE COLITIS; WEIGHT REDUCTION; WESTERN BLOTTING; WOUND HEALING; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; DEFICIENCY; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; INTESTINE FLORA; KNOCKOUT MOUSE; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BLOTTING, WESTERN; CANDIDA TROPICALIS; COLITIS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GASTROINTESTINAL MICROBIOME; IMMUNITY, INNATE; IMMUNOPRECIPITATION; LECTINS, C-TYPE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, IMMUNOLOGIC;

EID: 84978897601     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005662     Document Type: Article

References (35)

1. Kaser A, Zeissig S, Blumberg RS, (2010) Inflammatory bowel disease. Annu Rev Immunol28: 573–621. doi: 10.1146/annurev-immunol-030409-10122520192811
2. Huttenhower C, Kostic AD, Xavier RJ, (2014) Inflammatory bowel disease as a model for translating the microbiome. Immunity40: 843–854. doi: 10.1016/j.immuni.2014.05.01324950204
3. Scupham AJ, Presley LL, Wei B, Bent E, Griffith N, et al. (2006) Abundant and diverse fungal microbiota in the murine intestine. Appl Environ Microbiol72: 793–801. 16391120
4. Ott SJ, Kuhbacher T, Musfeldt M, Rosenstiel P, Hellmig S, et al. (2008) Fungi and inflammatory bowel diseases: Alterations of composition and diversity. Scand J Gastroenterol43: 831–841. doi: 10.1080/0036552080193543418584522
5. Santelmann H, Howard JM, (2005) Yeast metabolic products, yeast antigens and yeasts as possible triggers for irritable bowel syndrome. Eur J Gastroenterol Hepatol17: 21–26. 15647635
6. Ramaswamy K, Correa M, Koshy A, (2007) Non-healing gastric ulcer associated with Candida infection. Indian J Med Microbiol25: 57–58. 17377355
7. Stringer AM, Gibson RJ, Logan RM, Bowen JM, Yeoh AS, et al. (2009) Gastrointestinal microflora and mucins may play a critical role in the development of 5-Fluorouracil-induced gastrointestinal mucositis. Exp Biol Med (Maywood)234: 430–441.
8. Mukherjee PK, Sendid B, Hoarau G, Colombel JF, Poulain D, et al. (2015) Mycobiota in gastrointestinal diseases. Nat Rev Gastroenterol Hepatol12: 77–87. doi: 10.1038/nrgastro.2014.18825385227
9. Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, et al. (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science336: 1314–1317. doi: 10.1126/science.122178922674328
10. Iliev ID, (2015) Dectin-1 Exerts Dual Control in the Gut. Cell Host Microbe18: 139–141. doi: 10.1016/j.chom.2015.07.01026269949
11. Tang C, Kamiya T, Liu Y, Kadoki M, Kakuta S, et al. (2015) Inhibition of Dectin-1 Signaling Ameliorates Colitis by Inducing Lactobacillus-Mediated Regulatory T Cell Expansion in the Intestine. Cell Host Microbe18: 183–197. doi: 10.1016/j.chom.2015.07.00326269954
12. Zhu LL, Zhao XQ, Jiang C, You Y, Chen XP, et al. (2013) C-type lectin receptors Dectin-3 and Dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity39: 324–334. doi: 10.1016/j.immuni.2013.05.01723911656
13. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, et al. (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med196: 407–412. 12163569
14. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, et al. (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol8: 31–38. 17159984
15. Saijo S, Fujikado N, Furuta T, Chung SH, Kotaki H, et al. (2007) Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol8: 39–46. 17159982
16. Sato K, Yang XL, Yudate T, Chung JS, Wu J, et al. (2006) Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem281: 38854–38866. 17050534
17. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, et al. (2010) Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity32: 681–691. doi: 10.1016/j.immuni.2010.05.00120493731
18. Bugarcic A, Hitchens K, Beckhouse AG, Wells CA, Ashman RB, et al. (2008) Human and mouse macrophage-inducible C-type lectin (Mincle) bind Candida albicans. Glycobiology18: 679–685. doi: 10.1093/glycob/cwn04618509109
19. Arce I, Martinez-Munoz L, Roda-Navarro P, Fernandez-Ruiz E, (2004) The human C-type lectin CLECSF8 is a novel monocyte/macrophage endocytic receptor. Eur J Immunol34: 210–220. 14971047
20. Graham LM, Gupta V, Schafer G, Reid DM, Kimberg M, et al. (2012) The C-type lectin receptor CLECSF8 (CLEC4D) is expressed by myeloid cells and triggers cellular activation through Syk kinase. J Biol Chem287: 25964–25974. doi: 10.1074/jbc.M112.38416422689578
21. Gross O, Gewies A, Finger K, Schafer M, Sparwasser T, et al. (2006) Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature442: 651–656. 16862125
22. Miyake Y, Toyonaga K, Mori D, Kakuta S, Hoshino Y, et al. (2013) C-type lectin MCL is an FcRgamma-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity38: 1050–1062. doi: 10.1016/j.immuni.2013.03.01023602766
23. Zhao XQ, Zhu LL, Chang Q, Jiang C, You Y, et al. (2014) C-type lectin receptor dectin-3 mediates trehalose 6,6'-dimycolate (TDM)-induced Mincle expression through CARD9/Bcl10/MALT1-dependent nuclear factor (NF)-kappaB activation. J Biol Chem289: 30052–30062. doi: 10.1074/jbc.M114.58857425202022
24. Wilson GJ, Marakalala MJ, Hoving JC, van Laarhoven A, Drummond RA, et al. (2015) The C-type lectin receptor CLECSF8/CLEC4D is a key component of anti-mycobacterial immunity. Cell Host Microbe17: 252–259. doi: 10.1016/j.chom.2015.01.00425674984
25. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, et al. (2009) IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell15: 103–113. doi: 10.1016/j.ccr.2009.01.00119185845
26. Hara H, Ishihara C, Takeuchi A, Imanishi T, Xue L, et al. (2007) The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-associated and Toll-like receptors. Nat Immunol8: 619–629. 17486093
27. Bi L, Gojestani S, Wu W, Hsu YM, Zhu J, et al. (2010) CARD9 mediates dectin-2-induced IkappaBalpha kinase ubiquitination leading to activation of NF-kappaB in response to stimulation by the hyphal form of Candida albicans. J Biol Chem285: 25969–25977. doi: 10.1074/jbc.M110.13130020538615
28. Kim SC, Tonkonogy SL, Karrasch T, Jobin C, Sartor RB, (2007) Dual-association of gnotobiotic IL-10-/- mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis. Inflamm Bowel Dis13: 1457–1466. 17763473
29. Terzic J, Grivennikov S, Karin E, Karin M, (2010) Inflammation and colon cancer. Gastroenterology138: 2101–2114 e2105. doi: 10.1053/j.gastro.2010.01.05820420949
30. Dennis A, Kudo T, Kruidenier L, Girard F, Crepin VF, et al. (2008) The p50 subunit of NF-kappaB is critical for in vivo clearance of the noninvasive enteric pathogen Citrobacter rodentium. Infect Immun76: 4978–4988. doi: 10.1128/IAI.00736-0818694964
31. Steinbrecher KA, Harmel-Laws E, Sitcheran R, Baldwin AS, (2008) Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J Immunol180: 2588–2599. 18250470
32. Vautier S, Sousa Mda G, Brown GD, (2010) C-type lectins, fungi and Th17 responses. Cytokine Growth Factor Rev21: 405–412. doi: 10.1016/j.cytogfr.2010.10.00121075040
33. Salcedo R, Worschech A, Cardone M, Jones Y, Gyulai Z, et al. (2010) MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J Exp Med207: 1625–1636. doi: 10.1084/jem.2010019920624890
34. Wirtz S, Neufert C, Weigmann B, Neurath MF, (2007) Chemically induced mouse models of intestinal inflammation. Nat Protoc2: 541–546. 17406617
35. Landers CJ, Cohavy O, Misra R, Yang H, Lin YC, et al. (2002) Selected loss of tolerance evidenced by Crohn's disease-associated immune responses to auto- and microbial antigens. Gastroenterology123: 689–699. 12198693