Diet, gut microbes, and genetics in immune function: Can we leverage our current knowledge to achieve better outcomes in inflammatory bowel diseases?

Current Opinion in Immunology

Volumn 31, Issue , 2014, Pages 16-23

  Leone, Vanessa A ^a   Cham, Candace M ^a   Chang, Eugene B ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNITY; CARBOHYDRATE DIET; CROHN DISEASE; DIETARY INTAKE; DYSBIOSIS; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOGENETICS; INTESTINE FLORA; LIPID DIET; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; ULCERATIVE COLITIS; WESTERN DIET; ANIMAL; DIET; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; INTESTINE; MICROBIOLOGY; MICROFLORA; PATHOLOGY;

ANIMALS; AUTOIMMUNITY; DIET; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINES; MICROBIOTA;

EID: 84919825746     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.08.004     Document Type: Review

References (79)

1. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
2. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics. CA Cancer J Clin 2005, 55:74-108.
3. Loftus E.V. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 2004, 126:1504-1517.
4. Molodecky N.A., Soon I.S., Rabi D.M., Ghali W.A., Ferris M., Chernoff G., Benchimol E.I., Panaccione R., Ghosh S., Barkema H.W. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012, 142:46-54.
5. Tobon G.J., Youinou P., Saraux A. The environment, geo-epidemiology, and autoimmune disease: Rheumatoid arthritis. J Autoimmun 2010, 9:10-14.
6. Vehik K., Dabelea D. The changing epidemiology of type 1 diabetes: why is it going through the roof. Diabetes Metab Res Rev 2011, 27:3-13.
7. Koch-Henriksen N., Sorensen P.S. The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol 2010, 9:520-532.
8. Montgomery S.M., Ekbom A. Epidemiology of inflammatory bowel disease. Curr Opin Gastroenterol 2002, 18:416-420.
9. deSouza R.J., Swain J.F., Appel L.J., Sacks F.M. Alternatives for the macronutrient intake and chronic disease: a comparison of the OmniHeart diets with popular diets and with dietary recommendations. Am J Clin Nutr 2008, 88:1-11.
10. Turnbaugh P., Bäckhed F., Fulton L., Gordon J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3:213-223.
11. Turnbaugh P., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2008, 1:6-14.
12. Hildebrandt M.A., Hoffman C., Sherrill-Mix S.A., Keilbaugh S.A., Hamady M., Chen Y., Knight R., Ahima R.S., Bushman R., Wu G.D. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009, 137:1716-1724.
13. Walter J., Ley R. The human gut microbiome: ecology and recent evolutionary changes. Annu Rev Microbiol 2011, 65:411-429.
14. Kirsner J.B. Historical aspects of inflammatory bowel disease. J Clin Gastroenterol 1988, 10:286-297.
15. Ott S.J., Musfeldt M., Wenderoth D.F., Hampe J., Brant O., Folsch U.R., Timmis K.N., Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004, 53:685-693.
16. Lepage P., Seksik P., Sutren M., delaCochetiere M., Jian R., Marteau P., Dore J. Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm Bowel Dis 2006, 11:473-480.
17. Manichanh C., Rigottier-Gois L., Bonnaud E., Gloux J., Pelletier E., Frangeul L., Nalin R., Jarrin C., Chardon P., Marteau P. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006, 55:205-211.
18. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007, 104:13780-13785.
19. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009, 9:313-323.
20. Podolsky D.K. Inflammatory bowel disease. N Engl J Med 2002, 347:417-429.
21. Kang S.S., Bloom S.M., Norian L.A., Geske M.J., Flavell R.A., Stappenbeck T.S. An antibiotic-responsive mouse model of fulminant ulcerative colitis. PLoS Med 2008, e41.
22. Vucelic B. Inflammatory bowel diseases: controversies in the use of diagnostic procedures. Dig Dis 2009, 27:269-277.
23. Jostins L., Ripke S., Weersma R.K., Duerr R.H., McGovern D.P., Hui K.Y., Lee J.C., Schumm L.P., Sharma Y., Anderson C.A. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012, 491:119-124.
24. Anderson C.A., Boucher G., Lees C.W., Franke A., D'Amato M., Taylor K.D., Lee J.C., Goyette P., Imielinski M., Latiano A. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 2011, 43:246-252.
25. Franke A., McGovern D.P.B., Barrett J.C., Wang K., Radford-Smith G.L., Ahmad T., Lees C.W., Balschun T., Lee J., Roberts R. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010, 42:1118-1125.
26. Ventham N.T., Kennedy N.A., Nimmo E.R., Satsangi J. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology 2013, 145:293-308.
27. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., Britton H., Moran T., Karaliuskas R., Duerr R.H. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411:603-606.
28. Hugot J.P., Chamaillard M., Zouali H., Lesage S., Cezard J.P., Belaiche J., Almer S., Tysk C., O'Morian C.A., Gassull M. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
29. Wehkamp J., Weichenthal M., Schwab M., Schaffeler E., Schlee M., Herrlinger K.R., Stallmach A., Noack F., Fritz P., Schroder J.M. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 2004, 53:1658-1664.
30. Frank D.N., Robertson C.E., Hamm C.M., Kpadeh Z., Zhang T., Chen H., Zhu W., Sartor R.B., Boedeker E.C., Harpaz N. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel disease. Inflamm Bowel Dis 2011, 17:179-184.
31. Li E., Hamm C.M., Gulati A.S., Sartor R.B., Chen H., Wu X., Zhang T., Rohlf F.J., Zhu W., Gu C. Inflammatory bowel diseases phenotype, C. difficile and NOD2 genotype are associated with shifts in human ileum associated microbial composition. PLoS ONE 2012, 7:e26284.
32. Petnicki-Ocwieja T., Hrncir T., Liu Y.J., Biswas A., Hudcovic T., Tlaskalova-Hogenova H., Kobyashi K.S. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A 2009, 106:15813-15818.
33. Couturier-Maillard A., Secher T., Rehman A., Normand S., DeArcangelis A., Haesler R., Huot L., Grandjean T., Bressenot A., Delanoye-Crespin A. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013, 123:700-711.
34. Uhlig H.H., McKenzie B.S., Hue S., Thompson C., Joyce-Shaikh B., Stepankova R., Robinson N., Buonocore S., Tlaskalova-Hogenova H., Cua D.J. Differential activity of IL-12 and IL-23 in mucosal and systemic inane immune pathology. Immunity 2006, 25:309-318.
35. Kullberg M.C., Jankovic D., Feng C.G., Hue S., Gorelick P.L., McKenzie B.S., Cua D.J., Powrie F., Cheever A.W., Maloy K.J. IL-23 plays a key role in Helicobacter hepaticus-induced T-cell-dependent colitis. J Exp Med 2006, 203:2485-2494.
36. Yen D., Chueng J., Scheerens H., Poulet F., McClanahan T., McKenzie B., Kleinschek M.A., Owyang A., Mattson J., Blumenschein W. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006, 116:1310-1316.
37. Rio-Blanco L., Lazarevic V., Awasthi A., Mitsdoerffer M., Wilson B.S., Croxford A., Waisman A., Kuchroo V.K., Glimcher L.H., Oukka M. IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J Immunol 2010, 184:1710-1720.
38. Spehlmann M.E., Begun A.Z., Burghardt J., Lepage P., Raedler A., Schreiber S. Epidemiology of inflammatory bowel disease in a German twin cohort: results of a nationwide study. Inflamm Bowel Dis 2008, 14:968-976.
39. Orholm M., Binder V., Sorensen T.I., Rasmussen L.P., Kyvik K.O. Concordance of inflammatory bowel disease among Danish twins: results of a nationwide study. Scand J Gastroenterol 2000, 35:1075-1081.
40. Halfvarson J., Bodin L., Tysk C., Lindberg E., Jarnerot G. Inflammatory bowel disease in a Swedish twin cohort: a long-term follow-up of concordance and clinical characteristics. Gastroenterology 2003, 124:1767-1773.
41. Prescott N.J., Fisher S.A., Franke A., Hampe J., Onnie C.M., Soars D., Bagnall R., Mirza M.M., Sanderson J., Mansfield J.C. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology 2007, 132:1665-1671.
42. Cadwell K., Patel K.K., Maloney N.S., Liu T.C., Ng A.C., Storer C.E., Head R.D., Xavier R., Stappenbeck T.S., Virgin H.W. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 2010, 141:1135-1145.
43. Sellon R.K., Tonkonogy S., Schultz M., Dieleman L.A., Grenther W., Balish E., Rennic D.M., Sartor R.B. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10 deficient mice. Infect Immun 1998, 66:5224-5231.
44. Kullberg M.C., Ward J.M., Gorelick P.L., Caspar P., Hieny S., Cheever A., Jankovic D., Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect Immun 1998, 66:5157-5166.
45. Devkota S.D., Wang Y., Musch M.W., Leone V.L., Fehlner-Peach H., Nadimpalli A., Antonopoulos D.A., Jabri B., Chang E.B. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012, 487:104-108.
46. Ward J.M., Anver M.R., Haines D.C., Melhorn J.M., Gorelick P., Yan L., Fox J.G. Inflammatory large bowel disease in immunodeficient mice naturally infected with Helicobacter hepaticus. Lab Anim Sci 1996, 46:15-20.
47. Balish E., Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 2002, 160:2253-2257.
48. Kim S.C., Tonkonogy S.L., Albright C.A., Tsang K., Balish E.J., Braun J., Huycke M.M., Sartor R.B. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 2005, 128:891-906.
49. Sartor R.B. Microbial influences in inflammatory bowel disease: role in pathogenesis and clinical implications. In Kirsner's Inflammatory Bowel Diseases. 2004, 138-162. Elsevier., Philadelphia. R.B. Sartor, W.J. Sandborn (Eds.).
50. Moran J.P., Walter J., Tannock G.W., Tonkonogy S.L., Sartor R.B. Bifidobacterium animalis causes extensive duodenitis and mild colonic inflammation in monoassociated interleukin-10-deficient mice. Inflamm Bowel Dis 2009, 15:1022-1031.
51. Powrie F., Leach M.W., Mauze S., Baddle L.B., Coffman R.L. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 SCID mice. Int Immunol 1993, 5:1461-1471.
52. Powrie F., Leach M.W., Mauze S., Menon S., Caddle L.B., Coffman R.L. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1994, 1:553-562.
53. Aranda R., Sydora R., McAllister B.C., Binder P.L., Yang S.W., Targan H.Y., Kronenberg S.R.M. Analysis of intestinal lymphocytes in mouse colitis mediated by transfer of CD4+, CD45RBhigh T cells to SCID recipients. J Immunol 1997, 158:3464-3473.
54. Stepankova R., Powrie F., Kofronova O., Kozakova H., Hudcovic T., Hrncir T., Uhlig H., Read S., Rehakova Z., Benada O. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis 2007, 13:1202-1211.
55. Cong Y., Weaver C.T., Lazenby A., Elson C.O. Colitis induced by enteric bacterial antigen-specific CD4+ T cells requires CD40-CD40 ligand interactions for sustained increase in mucosal IL-12. J Immunol 2000, 165:2173-2182.
56. Cong Y., Weaver C.T., Lazenby A., Elson C.O. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J Immunol 2002, 169:6112-6119.
57. Lodes M.J., Cong Y., Elson C.O., Mohamath R., Landers C.J., Targan S.R., Fort M., Hershberg R.M. Bacterial flagellin is a dominant antigen in Crohn's disease. J Clin Invest 2004, 113:1296-1306.
58. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010, 107:14691-14696.
59. Roediger W.E., Moore J., Babidge W. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci 1997, 42:1571-1579.
60. Levine J., Ellis C.J., Furne J.K., Springfield J., Levitt M.D. Fecal hydrogen sulfide production in ulcerative colitis. Am J Gastroenterol 1998, 93:83-87.
61. Attene-Ramos M.S., Nava G.M., Muellner M.G., Wagner E.D., Plewa M.J., Gaskins H.R. DNA damage and toxicogenomic analyses of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells. Environ Mol Mutagen 2010, 51:304-314.
62. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505:559-563.
63. Erickson A.R., Cantarel B.L., Lamendella R., Darzi Y., Mongodin E.F., Pan C., Shah M., Halfvarson J., Tysk C., Raes J. Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease. PLoS ONE 2012, 7:e49138.
64. Morgan X.C., Tickle T.L., Sokol H., Gevers D., Devaney K.L., Ward D.V., Reyes J.A., Shah S.A., LeLeiko N., Snapper S.B. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012, 13:R79.
65. Vital M., Penton C.R., Wang Q., Young V.B., Antonopoulos D.A., Sogin M.L., Morrison H.G., Raffals L., Chang E.B., Huffnagle G.B. A gene-targeted approach to investigate the intestinal butyrate-producing bacterial community. Microbiome 2013, 1:8.
66. Atarashi K., Tanoue T., Oshima K., Suda W., Nagano Y., Nishikawa H., Fukuda S., Saito T., Narushima S., Hase K. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013, 500:232-236.
67. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Glickman J.N., Bohlooly Y.M., Garrett W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
68. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierror F., Yu D., Schitler H.C., Rolph M.S., Mackay F., Artis D. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
69. Rossi M., Corradini C., Amaretti A., Nicolini M., Pompei A., Zanoni S., Matteuzzi D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study of pure and fecal cultures. Appl Environ Microbiol 2005, 71:6150-6158.
70. Dewulf E.M., Cani P.D., Claus S.P., Fuentes S., Puylaert P.G., Neyrinck A.M., Bindels L.B., de Vos W.M., Gibson G.R., Thissen J.P. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 2013, 62:1112-1121.
71. Watson D., O'Connell Motherway M., Schoterman M.H., van Neerven R.J., Nauta A., van Sinderen D. Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol 2013, 114:1132-1146.
72. Fukumoto S., Toshimitsu T., Matsuoka S., Maruyama A., Oh-Oka K., Takamura T., Nakamura Y., Ishimaru K., Fujii-Kuriyama, Ikegami S. Identification of a probiotic bacteria-derived activator of the aryl hydrocarbon receptor that inhibits colitis. Immunol Cell Biol 2014, 92:460-465.
73. Monteleone I., Macdonald T.T., Pallone F., Monteleone G. The aryl hydrocarbon receptor in inflammatory bowel disease: linking the environment to disease pathogenesis. Curr Opin Gastroenterol 2012, 28:310-313.
74. Takamura T., Harama D., Matsuoka S., Shimokawa N., Nakamura Y., Okumura K., Ogawa H., Kitamura M., Nakao A. Activation of the aryl hydrocarbon receptor pathway may ameliorate dextran sodium sulfate-induced colitis in mice. Immunol Cell Biol 2010, 88:685-689.
75. Monteleone I., Rizzo A., Sarra M., Sica G., Sileri P., Biancone L., MacDonald T.T., Pallone F., Monteleone G. Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 2011, 141:237-248.
76. Zelante T., Iannitti R.G., Cunha C., De Luca A., Giovannini G., Pieraccini G., Zecchi R., D'Angelo C., Massi-Benedetti C., Fallarino F. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013, 39:372-385.
77. Hashimoto T., Perlot T., Rehman A., Trichereau J., Ishiguro H., Paolino M., Sigl V., Hanada T., Hanada R., Lipinski S. ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 2012, 487:477-481.
78. Nguyen N.T., Kimura A., Nakahama T., Chinen I., Masuda K., Nohara K., Fujii-Kuriyama Y., Kishimoto T. Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci U S A 2010, 107:19961-19966.
79. Haiser H.J., Gootenberg D.B., Chatman K., Sirasani G., Balskus E.P., Turnbaugh P.J. Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 2013, 341:295-298.