Interactions Between Diet and the Intestinal Microbiota Alter Intestinal Permeability and Colitis Severity in Mice

Gastroenterology

Volumn 154, Issue 4, 2018, Pages 1037-1046.e2

  Llewellyn, Sean R ^a   Britton, Graham J ^a   Contijoch, Eduardo J ^a   Vennaro, Olivia H ^a   Mortha, Arthur ^a   Colombel, Jean Frederic ^a   Grinspan, Ari ^a   Clemente, Jose C ^a   Merad, Miriam ^a   Faith, Jeremiah J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

IBD; Microbiota; Mouse Models; Systems Biology

Indexed keywords

ANTIBIOTIC AGENT; CASEIN; CELLULOSE; CORN OIL; DNA 16S; EGG WHITE; FISH OIL; FRUCTOSE; GLUCOSE; INULIN; ISPAGULA; LARD; MALTODEXTRIN; METHYLCELLULOSE; MILK FAT; OLIVE OIL; PALM KERNEL OIL; PALM OIL; PECTIN; POTATO STARCH; SAFFLOWER OIL; SOYBEAN PROTEIN; STARCH; SUCROSE; THEOBROMA OIL; TRANSCRIPTOME; DEXTRAN SULFATE; HOMEODOMAIN PROTEIN; RAG-1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT CHANGE; CONTROLLED STUDY; DEXTRAN SULFATE SODIUM-INDUCED COLITIS; DIETARY FIBER; DIETARY INTAKE; DISEASE SEVERITY; DISEASE SEVERITY ASSESSMENT; DNA SEQUENCE; FECES MICROFLORA; FEEDING; FLAXSEED FLOUR; GERMFREE MOUSE; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MACRONUTRIENT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTAKE; ADMINISTRATION AND DOSAGE; ANIMAL; ANIMAL FOOD; BACTERIUM; C57BL MOUSE; CLASSIFICATION; COLITIS; COLON; COMPARATIVE STUDY; DIET; DISEASE MODEL; FECES; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; NUTRITIONAL STATUS; NUTRITIONAL VALUE; PATHOPHYSIOLOGY; PERMEABILITY; SEVERITY OF ILLNESS INDEX; TIME FACTOR;

ANIMAL FEED; ANIMALS; BACTERIA; CASEINS; COLITIS; COLON; DEXTRAN SULFATE; DIET; DIETARY FIBER; DIETARY PROTEINS; DISEASE MODELS, ANIMAL; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HOMEODOMAIN PROTEINS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUTRITIONAL STATUS; NUTRITIVE VALUE; PERMEABILITY; PSYLLIUM; SEVERITY OF ILLNESS INDEX; TIME FACTORS;

EID: 85042701019     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2017.11.030     Document Type: Article

References (58)

1. Lee, D., Baldassano, R.N., Otley, A.R., et al. Comparative effectiveness of nutritional and biological therapy in North American children with active Crohn's disease. Inflamm Bowel Dis 21 (2015), 1786–1793.
2. Lewis, J.D., Abreu, M.T., Diet as a trigger or therapy for inflammatory bowel diseases. Gastroenterology 152 (2017), 398–414.
3. Zachos, M., Tondeur, M., Griffiths, A.M., Enteral nutritional therapy for induction of remission in Crohn's disease. Cochrane Database Syst Rev(1), 2007, CD000542.
4. Faith, J.J., Guruge, J.L., Charbonneau, M., et al. The long-term stability of the human gut microbiota. Science, 341, 2013 1237439–1237439.
5. David, L.A., Maurice, C.F., Carmody, R.N., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2013), 559–563.
6. Walker, A.W., Ince, J., Duncan, S.H., et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5 (2011), 220–230.
7. Wu, G.D., Chen, J., Hoffmann, C., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108.
8. McNulty, N.P., Wu, M., Erickson, A.R., et al. Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol, 11, 2013, e1001637.
9. Holmes, A.J., Chew, Y.V., Colakoglu, F., et al. Diet-microbiome interactions in health are controlled by intestinal nitrogen source constraints. Cell Metab 25 (2017), 140–151.
10. Sonnenburg, E.D., Zheng, H., Joglekar, P., et al. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 141 (2010), 1241–1252.
11. Faith, J.J., McNulty, N.P., Rey, F.E., et al. Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333 (2011), 101–104.
12. Gevers, D., Kugathasan, S., Denson, L.A., et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15 (2014), 382–392.
13. Jacobs, J.P., Goudarzi, M., Singh, N., et al. A disease-associated microbial and metabolomics state in relatives of pediatric inflammatory bowel disease patients. C Cell Mol Gastroenterol Hepatol 2 (2016), 750–766.
14. Hansen, J.J., Sartor, R.B., Insights from animal models. Bernstein, C.N., (eds.) Inflammatory bowel disease yearbook, vol. 4, 2007, Remedica, Chicago, 19–55.
15. Moayyedi, P., Surette, M.G., Kim, P.T., et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149 (2015), 102–109.
16. Paramsothy, S., Kamm, M.A., Kaakoush, N.O., et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet 6736 (2017), 1–11.
17. Chassaing, B., Koren, O., Goodrich, J.K., et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519 (2015), 92–96.
18. Chassaing, B., Miles-Brown, J., Pellizzon, M., et al. Lack of soluble fiber drives diet-induced adiposity in mice. Am J Physiol Gastrointest Liver Physiol 309 (2015), G528–G541.
19. Earle, K.A., Billings, G., Sigal, M., et al. Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18 (2015), 478–488.
20. Desai, M.S., Seekatz, A.M., Koropatkin, N.M., et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167 (2016), 1339–1353.e21.
21. Turnbaugh, P.J., Ridaura, V.K., Faith, J.J., et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med, 1, 2009 6ra14.
22. Bylund-Fellenius, A., Landstrom, E., Axelsson, L., et al. Experimental colitis induced by dextran sulphate in normal and germfree mice. Microbioal Ecol Heal Dis 7 (1994), 207–215.
23. Maslowski, K.M., Vieira, A.T., Ng, A., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461 (2009), 1282–1286.
24. Chassaing, B., Srinivasan, G., Delgado, M.A., et al. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PLoS One, 7, 2012, e44328.
25. Efron, B., Hastie, T., Johnstone, I., et al. Least angle regression. Ann Stat 32 (2004), 407–499.
26. van der Logt, E.M.J., Blokzijl, T., van der Meer, R., et al. Westernized high-fat diet accelerates weight loss in dextran sulfate sodium-induced colitis in mice, which is further aggravated by supplementation of heme. J Nutr Biochem 24 (2013), 1159–1165.
27. Laroui, H., Ingersoll, S.A., Liu, H.C., et al. Dextran sodium sulfate (dss) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon. PLoS One, 7, 2012, e32084.
28. Hans, W., Schölmerich, J., Gross, V., et al. The role of the resident intestinal flora in acute and chronic dextran sulfate sodium-induced colitis in mice. Eur J Gastroenterol Hepatol 12 (2000), 267–273.
29. Khan, K.J., Ullman, T.A., Ford, A.C., et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 106 (2011), 661–673.
30. Rath, H.C., Schultz, M., Freitag, R., et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect Immun 69 (2001), 2277–2285.
31. Smith, P.M., Howitt, M.R., Panikov, N., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
32. Furusawa, Y., Obata, Y., Fukuda, S., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504 (2013), 446–450.
33. Arpaia, N., Campbell, C., Fan, X., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
34. Jowett, S.L., Seal, C.J., Pearce, M.S., et al. Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut 53 (2004), 1479–1484.
35. Ananthakrishnan, A.N., Khalili, H., Song, M.Y., et al. High school diet and risk of Crohn's disease and ulcerative colitis. Inflamm Bowel Dis 21 (2015), 2311–2319.
36. Brotherton, C.S., Martin, C.A., Long, M.D., et al. Avoidance of fiber is associated with greater risk of Crohn's disease flare in a 6-month period. Clin Gastroenterol Hepatol 14 (2016), 1130–1136.
37. Hallert, C., Kaldma, M., Petersson, B.G., Ispaghula husk may relieve gastrointestinal symptoms in ulcerative colitis in remission. Scand J Gastroenterol 26 (1991), 747–750.
38. Torres, J., Burisch, J., Riddle, M., et al. Pre-clinical disease and preventive strategies in IBD: perspectives, challenges and opportunities. Gut 65 (2016), 1061–1069.
39. Sartor, R.B., Wu, G.D., Roles for Intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology 152 (2017), 327–339.
40. Powrie, F., Leach, M.W., Mauze, S., et al. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5 (1993), 1461–1471.
41. Klimesova, K., Kverka, M., Zakostelska, Z., et al. Altered gut microbiota promotes colitis-associated cancer in IL-1 receptor-associated kinase M-deficient mice. Inflamm Bowel Dis 19 (2013), 1266–1277.
42. Kwon, H.S., Oh, S.M., Kim, J.K., Glabridin, a functional compound of liquorice, attenuates colonic inflammation in mice with dextran sulphate sodium-induced colitis. Clin Exp Immunol 151 (2008), 165–173.
43. Abe, K., Nguyen, K.P., Fine, S.D., et al. Conventional dendritic cells regulate the outcome of colonic inflammation independently of T cells. Proc Natl Acad Sci U S A 104 (2007), 17022–17027.
44. Chassaing, B., Srinivasan, G., Delgado, M.A., et al. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PLoS One, 7, 2012, e44328.
45. Faith, J.J., Guruge, J.L., Charbonneau, M., et al. The long-term stability of the human gut microbiota. Science, 341, 2013 1237439–1237439.
46. Reyes, A., Wu, M., McNulty, N.P., et al. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc Natl Acad Sci U S A 110 (2013), 20236–20241.
47. Caporaso, J.G., Kuczynski, J., Stombaugh, J., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
48. McDonald, D., Price, M.N., Goodrich, J., et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6 (2012), 610–618.
49. Segata, N., Izard, J., Waldron, L., et al. Metagenomic biomarker discovery and explanation. Genome Biol 12 (2011), 1–18.
50. Smith, P.M., Howitt, M.R., Panikov, N., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
51. Kashyap, P.C., Marcobal, A., Ursell, L.K., et al. Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 144 (2013), 967–977.
52. Kim, D., Langmead, B., Salzberg, S.L., HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12 (2015), 357–360.
53. Pertea, M., Kim, D., Pertea, G.M., et al. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11 (2016), 1650–1667.
54. Pertea, M., Pertea, G.M., Antonescu, C.M., et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33 (2015), 290–295.
55. Frazee, A.C., Pertea, G., Jaffe, A.E., et al. Ballgown bridges the gap between transcriptome assembly and expression analysis. Nat Biotechnol 33 (2015), 243–246.
56. Huang, D.W., Lempicki, R.A., Sherman, B.T., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4 (2009), 44–57.
57. Matsunaga, H., Hokari, R., Kurihara, C., et al. Omega-3 fatty acids exacerbate DSS-induced colitis through decreased adiponectin in colonic subepithelial myofibroblasts. Inflamm Bowel Dis 14 (2008), 1348–1357.
58. Feagan, B.G., Sandborn, W.J., Mittmann, U., et al. Omega-3 free fatty acids for the maintenance of remission in Crohn disease: the EPIC randomized controlled trials. JAMA 299 (2008), 1690–1697.