Manipulation of the gut microbiota using resistant starch is associated with protection against colitis-associated colorectal cancer in rats

Carcinogenesis

Volumn 37, Issue 4, 2015, Pages 366-375

  Hu, Ying ^a   Le Leu, Richard K ^a,b   Christophersen, Claus T ^b,c   Somashekar, Roshini ^a   Conlon, Michael A ^b   Meng, Xing Q ^d   Winter, Jean M ^a   Woodman, Richard J ^d   McKinnon, Ross ^a   Young, Graeme P ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b CSIRO   (Australia)

^c EDITH COWAN UNIVERSITY   (Australia)

^d FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ANTINEOPLASTIC AGENT; AZOXYMETHANE; BUTYRIC ACID; CYCLOOXYGENASE 2; DEXTRAN SULFATE; DRINKING WATER; G PROTEIN COUPLED RECEPTOR 54; GREEN TEA EXTRACT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; PROPIONIC ACID; RESISTANT STARCH; SHORT CHAIN FATTY ACID; STARCH; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM; BARNESIELLA; BIFIDOBACTERIUM; CANCER MODEL; CANCER PREVENTION; CELL PROLIFERATION; COLITIS; COLITIS ASSOCIATED COLORECTAL CANCER; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG MECHANISM; EPIGENETICS; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTESTINE FLORA; MALE; MARVINBRYANTIA; MICROBIAL DIVERSITY; MUCUS SECRETION; NONHUMAN; PARABACTEROIDES; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RAT MODEL; REAL TIME POLYMERASE CHAIN REACTION; RUMINOCOCCUS; ANIMAL; COLORECTAL NEOPLASMS; COMPLICATION; INTESTINE; METABOLISM; MICROBIOLOGY;

ANIMALS; COLITIS; COLORECTAL NEOPLASMS; INTESTINES; RATS; STARCH;

EID: 84963615071     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgw019     Document Type: Article

References (50)

1. Farraye, F. A. et al. (2010) AGA technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology, 138, 746-774.
2. Maresso, K. C. et al. (2015) Molecular cancer prevention: Current status and future directions CA Cancer J. Clin., 65, 345-383.
3. Feng, Q. et al. (2015) Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun., 6, 6528.
4. Machiels, K. et al. (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut, 63, 1275-1283.
5. Jostins, L. et al. (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature, 491, 119-124.
6. Aune, D. et al. (2011) Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ, 343, d6617.
7. Bingham, S.A. et al. (2003) Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet, 361, 1496-1501.
8. McIntyre, A. et al. (1993) Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut, 34, 386-391.
9. Englyst, H.N. et al. (1992) Classification and measurement of nutritionally important starch fractions. Eur. J. Clin. Nutr., 46, S33-S50.
10. Fung, K.Y. et al. (2012) A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate. Br. J. Nutr., 108, 820-831.
11. Le Leu, R.K. et al. (2013) Dietary red meat aggravates dextran sulfate sodium-induced colitis in mice whereas resistant starch attenuates inflammation. Dig. Dis. Sci., 58, 3475-3482.
12. Le Leu, R.K. et al. (2007) Effect of dietary resistant starch and protein on colonic fermentation and intestinal tumourigenesis in rats. Carcinogenesis, 28, 240-245.
13. Clarke, J.M. et al. (2008) Effects of high-amylose maize starch and butyrylated high-amylose maize starch on azoxymethane-induced intestinal cancer in rats. Carcinogenesis, 29, 2190-2194.
14. Mishiro, T. et al. (2013) Butyric acid attenuates intestinal inflammation in murine DSS-induced colitis model via milk fat globule-EGF factor 8. Lab. Invest., 93, 834-843.
15. Humphreys, K.J. et al. (2014) Dietary manipulation of oncogenic micro- RNA expression in human rectal mucosa: a randomized trial. Cancer Prev. Res. (Phila)., 7, 786-795.
16. Dronamraju, S.S. et al. (2009) Cell kinetics and gene expression changes in colorectal cancer patients given resistant starch: a randomised controlled trial. Gut, 58, 413-420.
17. Burn, J. et al. (2008) Effect of aspirin or resistant starch on colorectal neoplasia in the Lynch syndrome. N. Engl. J. Med., 359, 2567-2578.
18. Bruckner, M. et al. (2012) Green tea polyphenol epigallocatechin-3-gallate shows therapeutic antioxidative effects in a murine model of colitis. J. Crohn's Colitis, 6, 226-235.
19. Hu, Y. et al. (2008) Suppression of colorectal oncogenesis by seleniumenriched milk proteins: apoptosis and K-ras mutations. Cancer Res., 68, 4936-4944.
20. Le Leu, R.K. et al. (2009) Effect of high amylose maize starches on colonic fermentation and apoptotic response to DNA-damage in the colon of rats. Nutr. Metab., 6, 11.
21. James, S.L. et al. (2015) Abnormal fibre usage in UC in remission. Gut, 64, 562-570.
22. DeSantis, T.Z. et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol., 72, 5069-5072.
23. Hu, Y. et al. (2013) Combination of selenium and green tea improves the efficacy of chemoprevention in a rat colorectal cancer model by modulating genetic and epigenetic biomarkers. PLoS One, 8, e64362.
24. McArdle, B.H. et al. (2001) Anderson MJ. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology, 82, 290-297.
25. Haenen, D. et al. (2013) Resistant starch induces catabolic but suppresses immune and cell division pathways and changes the microbiome in the proximal colon of male pigs. J. Nutr., 143, 1889-1898.
26. Zackular, J.P. et al. (2013) The gut microbiome modulates colon tumorigenesis. MBio, 4, e00692-e00613.
27. Vannucci, L. et al. (2008) Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int. J. Oncol., 32, 609-617.
28. Schulz, M.D. et al. (2014) High-fat-diet-mediated dysbiosis promotes intestinal carcinogenesis independently of obesity. Nature, 514, 508-512.
29. Donohoe, D.R. et al. (2014) A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota- and butyrate-dependent manner. Cancer Discov., 4, 1387-1397.
30. Zhu, Q. et al. (2014) Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS One, 9, e90849.
31. Louis, P. et al. (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol., 12, 661-672.
32. Wong, V.W. et al. (2013) Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis-a longitudinal study. PLoS One, 8, e62885.
33. Nava, G.M. et al. (2011) Diversity of the autochthonous colonic microbiota. Gut Microbes, 2, 99-104.
34. Ubeda, C. et al. (2013) Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization. Infect. Immun., 81, 965-973.
35. Wang, T. et al. (2012) Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J., 6, 320-329.
36. Boutron-Ruault, M. C. et al. (2005) Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutr. Cancer, 53, 160-168.
37. Devkota, S. et al. (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature, 487, 104-108.
38. Lau, S.K. et al. (2006) Bacteraemia caused by Anaerotruncus colihominis and emended description of the species. J. Clin. Pathol., 59, 748-752.
39. Sebastián, C. et al. (2014) Untangling the fiber yarn: butyrate feeds Warburg to suppress colorectal cancer. Cancer Discov., 4, 1368-1370.
40. Tang, Y. et al. (2011) G-protein-coupled receptor for short-chain fatty acids suppresses colon cancer. Int. J. Cancer, 128, 847-856.
41. Maslowski, K.M. et al. (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature, 461, 1282-1286.
42. Macia, L. et al. (2015) Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun., 6, 6734.
43. Smith, P.M. et al. (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science (New York, N.Y.), 341, 569-573.
44. Saldanha, S.N. et al. (2014) Molecular mechanisms for inhibition of colon cancer cells by combined epigenetic-modulating epigallocatechin gallate and sodium butyrate. Exp. Cell Res., 324, 40-53.
45. Fukuda, S. et al. (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature, 469, 543-547.
46. Kohlmeier, L. et al. (1997) Tea and cancer prevention: an evaluation of the epidemiologic literature. Nutr. Cancer, 27, 1-13.
47. Kim, M. et al. (2010) The modifying effects of green tea polyphenols on acute colitis and inflammation-associated colon carcinogenesis in male ICR mice. BioFactors (Oxford, England), 36, 43-51.
48. Weisburger, J. H. et al. (1998) Effect of tea extracts, polyphenols, and epigallocatechin gallate on azoxymethane-induced colon cancer. Proc. Soc. Exp. Biol. Med., 217, 104-108.
49. Volate, S.R. et al. (2009) Epigenetic modulation of the retinoid X receptor alpha by green tea in the azoxymethane-Apc Min/+ mouse model of intestinal cancer. Mol. Carcin., 48, 920-933.
50. Zhou, P. et al. (2012) Combination chemoprevention: future direction of colorectal cancer prevention. Eur. J. Cancer Prev., 21, 231-240.