An essential role of Ffar2 (Gpr43) in dietary fibre-mediated promotion of healthy composition of gut microbiota and suppression of intestinal carcinogenesis

Oncogenesis

Volumn 5, Issue 6, 2016, Pages

  Sivaprakasam, S ^a,b   Gurav, A ^a   Paschall, A V ^a   Coe, G L ^a   Chaudhary, K ^a   Cai, Y ^a   Kolhe, R ^a   Martin, P ^a   Browning, D ^a   Huang, L ^a   Shi, H ^a   Sifuentes, H ^a   Vijay Kumar, M ^c   Thompson, S A ^a   Munn, D H ^a   Mellor, A ^d   McGaha, T L ^e   Shiao, P ^f   Cutler, C W ^f   Liu, K ^a   Ganapathy, V ^b   Li, H ^a   Singh, N ^a   more..

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF TORONTO   (Canada)

^f AUGUSTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84997629668     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/ONCSIS.2016.38     Document Type: Article

References (47)

1. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 2008; 27: 104–119.
2. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 2012; 6: 320–329.
3. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007; 104: 13780–13785.
4. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003; 278: 11312–11319.
5. Taggart AK, Kero J, Gan X, Cai TQ, Cheng K, Ippolito M et al. (D)-beta-Hydroxybutyrate inhibits adipocyte lipolysis via the nicotinic acid receptor PUMA-G. J Biol Chem 2005; 280: 26649–26652.
6. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504: 451–455.
7. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504: 446–450.
8. Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014; 40: 128–139.
9. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341: 569–573.
10. Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota-and butyrate-dependent manner. Cancer Discov 2014; 4: 1387–1397.
11. Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell 2014; 158: 288–299.
12. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009; 461: 1282–1286.
13. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014; 20: 159–166.
14. Kim MH, Kang SG, Park JH, Yanagisawa M, Kim CH. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013; 145: 396–406 e1-10.
15. Sina C, Gavrilova O, Forster M, Till A, Derer S, Hildebrand F et al. G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation. J Immunol 2009; 183: 7514–7522.
16. Tang Y, Chen Y, Jiang H, Robbins GT, Nie D. G-protein-coupled receptor for short-chain fatty acids suppresses colon cancer. Int J Cancer 2011; 128: 847–856.
17. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313–323.
18. Shanahan F, Quigley EM. Manipulation of the microbiota for treatment of IBS and IBD-challenges and controversies. Gastroenterology 2014; 146: 1554–1563.
19. Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients 2013; 5: 1417–1435.
20. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011; 469: 543–547.
21. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 2014; 146: 1564–1572.
22. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013; 13: 800–812.
23. Kim JE, Kim JY, Lee KW, Lee HJ. Cancer chemopreventive effects of lactic acid bacteria. J Microbiol Biotechnol 2007; 17: 1227–1235.
24. Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A et al. Dietary prebiotics: current status and new definition. Food Sci Tech Bull Funct Foods 2010; 7: 1–19.
25. Davis LM, Martinez I, Walter J, Goin C, Hutkins RW. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS ONE 2011; 6: e25200.
26. Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS ONE 2011; 6: e16393.
27. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013; 14: 207–215.
28. Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 2015; 42: 344–355.
29. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut (e-pub ahead of print 26 August 2015; doi:10.1136/gutjnl-2015-310101).
30. Kapatral V, Anderson I, Ivanova N, Reznik G, Los T, Lykidis A et al. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 2002; 184: 2005–2018.
31. Falony G, Vlachou A, Verbrugghe K, De Vuyst L. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 2006; 72: 7835–7841.
32. O’Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun 2015; 6: 6342.
33. Thangaraju M, Cresci GA, Liu K, Ananth S, Gnanaprakasam JP, Browning DD et al. GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 2009; 69: 2826–2832.
34. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996; 87: 159–170.
35. Le Bourgot C, Ferret-Bernard S, Le Normand L, Savary G, Menendez-Aparicio E, Blat S et al. Maternal short-chain fructooligosaccharide supplementation influences intestinal immune system maturation in piglets. PLoS ONE 2014; 9: e107508.
36. Blaser MJ. The microbiome revolution. J Clin Invest 2014; 124: 4162–4165.
37. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012; 489: 220–230.
38. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010; 11: 76–83.
39. Eslinger AJ, Eller LK, Reimer RA. Yellow pea fiber improves glycemia and reduces Clostridium leptum in diet-induced obese rats. Nutr Res 2014; 34: 714–722.
40. Koleva PT, Valcheva RS, Sun X, Ganzle MG, Dieleman LA. Inulin and fructo-oligosaccharides have divergent effects on colitis and commensal microbiota in HLA-B27 transgenic rats. Br J Nutr 2012; 108: 1633–1643.
41. Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun 2015; 6: 6734.
42. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559–563.
43. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R et al. Human genetics shape the gut microbiome. Cell 2014; 159: 789–799.
44. Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol 2015; 6: 20.
45. Ang Z, Er JZ, Ding JL. The short-chain fatty acid receptor GPR43 is transcriptionally regulated by XBP1 in human monocytes. Sci Rep 2015; 5: 8134.
46. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145: 745–757.
47. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337–341.