Bacteroides thetaiotaomicron ameliorates colon inflammation in preclinical models of Crohn's disease

Inflammatory Bowel Diseases

Volumn 25, Issue 1, 2019, Pages 85-96

  Delday, Margaret ^a,b   Mulder, Imke ^a,c   Logan, Elizabeth T ^a,b   Grant, George ^a,b  

^a Life Sciences Innovation Building   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c NONE   (United States)

Author keywords

Bacteroides thetaiotaomicron; Crohn's disease; dextran sodium sulphate; inflammatory bowel disease; knockout

Indexed keywords

CELL PROTEIN; DEXTRAN SULFATE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; PIRIN LIKE PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; IL10 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTEROIDES THETAIOTAOMICRON; BODY WEIGHT GAIN; BODY WEIGHT LOSS; CACO-2 CELL LINE; CELL INFILTRATION; CLINICAL EFFECTIVENESS; COLITIS; COLON SHORTENING; CROHN DISEASE; CXCL10 GENE; DIGESTIVE TRACT PARAMETERS; DOWN REGULATION; FEMALE; FREEZE DRYING; GENE EXPRESSION; HISTOPATHOLOGY; IL1B GENE; IL6 GENE; IMMUNITY; INTESTINE EPITHELIUM CELL; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; TNFA GENE; ANIMAL; C57BL MOUSE; DISEASE MODEL; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BACTEROIDES THETAIOTAOMICRON; CACO-2 CELLS; COLITIS; CROHN DISEASE; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-10; MICE, INBRED C57BL; MICE, KNOCKOUT; RATS;

EID: 85058605521     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1093/ibd/izy281     Document Type: Article

References (57)

1. Lichtenstein GR, Hanauer SB, Sandborn WJ. Management of Crohn's disease in adults. Am J Gastroenterol. 2009;104:465-483.
2. Colombel JF, Narula N, Peyrin-Biroulet L. Management strategies to improve outcomes of patients with Inflammatory Bowel Diseases. Gastroenterology. 2017;152:351-361.e5.
3. Gasparetto M, Guariso G. Crohn's disease and growth deficiency in children and adolescents. World J Gastroenterol. 2014;20:13219-13233.
4. Tadbiri S, Peyrin-Biroulet L, Serrero M, et al., GETAID OBSERV-IBD study group. Impact of vedolizumab therapy on extra-intestinal manifestations in patients with inflammatory bowel disease: A multicentre cohort study nested in the OBSERV-IBD cohort. Aliment Pharmacol Ther. 2018;47:485-493.
5. Harbord M, Annese V, Vavricka SR, et al., European Crohn's and Colitis Organisation. The first European evidence-based consensus on extra-intestinal manifestations in inflammatory bowel disease. J Crohns Colitis. 2016;10:239-254.
6. Cosnes J, Gowerrousseau C, Seksik P, et al., Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology. 2011;140:1785-1794.
7. Diefenbach K-A, Breuer C-K. Pediatric inflammatory bowel disease. World J Gastroenterol. 2006;12:3204-3212.
8. Baldwin KR, Kaplan JL. Medical management of pediatric inflammatory bowel disease. Semin Pediatr Surg. 2017;26:360-366.
9. Rigoli L, Caruso RA. Inflammatory bowel disease in pediatric and adolescent patients: A biomolecular and histopathological review. World J Gastroenterol. 2014;20:10262-10278.
10. Blotière PO, Rudant J, Barré A, et al., Conditions of prescription of anti-TNF agents in newly treated patients with inflammatory bowel disease in France (2011-2013). Dig Liver Dis. 2016;48:620-625.
11. Thai A, Prindiville T. Hepatosplenic T-cell lymphoma and inflammatory bowel disease. J Crohn's Colitis. 2010;4:511-522.
12. Walters TD, Hyams JS. Can early anti-TNF-treatment be an effective therapeutic strategy in children with Crohn's disease Immunotherapy. 2014;6:799-802.
13. Walters TD, Kim MO, Denson LA, et al., PRO-KIIDS Research Group. Increased effectiveness of early therapy with anti-tumor necrosis factor-vs an immunomodulator in children with Crohn's disease. Gastroenterology. 2014;146:383-391.
14. Gevers D, Kugathasan S, Denson LA, et al., The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014;15:382-392.
15. Manichanh C, Rigottier-Gois L, Bonnaud E, et al., Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 2006;55:205-211.
16. Ott SJ, Musfeldt M, Wenderoth DF, et al., Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685-693.
17. Pascal V, Pozuelo M, Borruel N, et al., A microbial signature for Crohn's disease. Gut. 2017;66:813-822.
18. Zhou Y, Zhi F. Lower level of bacteroides in the gut microbiota is associated with inflammatory bowel disease: A meta-analysis. Biomed Res Int. 2016;2016:5828959.
19. Hooper LV, Wong MH, Thelin A, et al., Molecular analysis of commensal host-microbial relationships in the intestine. Science. 2001;291:881-884.
20. Wrzosek L, Miquel S, Noordine ML, et al., Bacteroides thetaiotaomicron and faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 2013;11:61.
21. Kelly D, Campbell JI, King TP, et al., Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and rela. Nat Immunol. 2004;5:104-112.
22. Bowcutt R, Forman R, Glymenaki M, et al., Heterogeneity across the murine small and large intestine. World J Gastroenterol. 2014;20:15216-15232.
23. Berg DJ, Davidson N, Kuhn R, et al., Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest. 1996;98:1010-1020.
24. Kiesler P, Fuss IJ, Strober W. Experimental models of inflammatory bowel diseases. Med Hyg (Geneve). 2001;59:241-248.
25. Wang H, Shi P, Zuo L, et al., Dietary non-digestible polysaccharides ameliorate intestinal epithelial barrier dysfunction in IL-10 knockout mice. J Crohns Colitis. 2016;10:1076-1086.
26. Zhao J, Wang H, Shi P, et al., GPR120, a potential therapeutic target for experimental colitis in IL-10 deficient mice. Oncotarget. 2017;8:8397-8405.
27. Hughes PA, Brierley SM, Castro J, et al., Experimental colitis models. In: Szallasi A, Biro T, eds. TRP Channels in Drug Discovery. Methods in Pharmacology and Toxicology. Totowa. NJ: Humana Press, 2012.
28. Liu F, Rehmani I, Esaki S, et al., Pirin is an iron-dependent redox regulator of NF-B. Proc Natl Acad Sci. 2013;110:9722-9727.
29. Qin J, Li R, Raes J, et al., MetaHIT Consortium. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59-65.
30. Zocco MA, Ainora ME, Gasbarrini G, et al., Bacteroides thetaiotaomicron in the gut: Molecular aspects of their interaction. Dig Liver Dis. 2007;39:707-712.
31. Sonnenburg JL, Xu J, Leip DD, et al., Glycan foraging in vivo by an intestine- A dapted bacterial symbiont. Science. 2005;307:1955-1959.
32. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via paneth cells. Proc Natl Acad Sci USA. 2002;99:15451-15455.
33. Hooper LV, Stappenbeck TS, Hong CV, et al., Angiogenins: A new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003;4:269-273.
34. Resta-Lenert S, Barrett KE. Probiotics and commensals reverse TNF-alphaand IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology. 2006;130:731-746.
35. Hoffmann TW, Pham HP, Bridonneau C, et al., Microorganisms linked to inflammatory bowel disease-associated dysbiosis differentially impact host physiology in gnotobiotic mice. ISME J. 2016;10:460-477.
36. Schreiber S, Nikolaus S, Hampe J. Activation of nuclear factor kappa B inflammatory bowel disease. Gut. 1998;42:477-484.
37. Baert F, Moortgat L, Van Assche G, et al., Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology. 2010;138:463-468.
38. Scheinin T, Butler DM, Salway F, et al., Validation of the interleukin-10 knockout mouse model of colitis: Antitumour necrosis factor-antibodies suppress the progression of colitis. Clin Exp Immunol. 2003;133:38-43.
39. Wirtz S, Popp V, Kindermann M, et al., Chemically induced mouse models of acute and chronic intestinal inflammation. Nat Protoc. 2017;12:1295-1309.
40. Akazawa Y, Kubo M, Zhang R, et al., Inhibition of arginase ameliorates experimental ulcerative colitis in mice. Free Radic Res. 2013;47:137-145.
41. Melgar S, Karlsson A, Michaëlsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: Correlation between symptoms and inflammation. Am J Physiol Gastrointest Liver Physiol. 2005;288:G1328-G1338.
42. Mähler M, Bristol IJ, Leiter EH, et al., Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am J Physiol. 1998;274:G544-G551.
43. Solomon L, Mansor S, Mallon P, et al., The dextran sulphate sodium (DSS) model of colitis: An overview. Comp Clin Path. 2010;19:235-239.
44. Zhu L, Shi T, Zhong C, et al., IL-10 and il-10 receptor mutations in very early onset Inflammatory Bowel Disease. Gastroenterol Res. 2017;10:65-69.
45. Beser OF, Conde CD, Serwas NK, et al., Clinical features of interleukin 10 receptor gene mutations in children with very early-onset inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2015;60:332-338.
46. Shouval DS, Konnikova L, Griffith AE, et al., Enhanced TH17 responses in patients with IL10 receptor deficiency and infantile-onset IBD. Inflamm Bowel Dis. 2017;23:1950-1961.
47. Erben U, Loddenkemper C, Doerfel K, et al., Original Article A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol. 2014;7:4557-4576.
48. Gersemann M, Wehkamp J, Stange EF. Innate immune dysfunction in inflammatory bowel disease. J Intern Med. 2012;271:421-428.
49. Horowitz S, Binion DG, Nelson VM, et al., Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease. AJP Gastrointest. Liver Physiol. 2006;292:G1323-G1336.
50. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol. 2014;14:329-342.
51. Chen F, Liu H, Shen Q, et al., Osteopontin: Participation in inflammation or mucosal protection in inflammatory bowel diseases Dig Dis Sci. 2013;58:1569-1580.
52. Komine-Aizawa S, Masuda H, Mazaki T, et al., Plasma osteopontin predicts inflammatory bowel disease activities. Int Surg. 2015;100:38-43.
53. Uronis JM, Muhlbauer M, Herfarth HH, et al., Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS One. 2009;4:e6026.
54. Hudcovic T, Kozáková H, Kolínská J, et al., Monocolonization with bacteroides ovatus protects immunodeficient SCID mice from mortality in chronic intestinal inflammation caused by long-lasting dextran sodium sulfate treatment. Physiol Res. 2009;58:101-110.
55. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620-625.
56. Chang YC, Ching YH, Chiu CC, et al., TLR2 and interleukin-10 are involved in bacteroides fragilis-mediated prevention of DSS-induced colitis in gnotobiotic mice. Plos One. 2017;12:e0180025.
57. Chu H, Khosravi A, Kusumawardhani IP, et al., Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science. 2016;352:1116-1120.