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Digestive Diseases and Sciences
Published in: Digestive Diseases and Sciences 3/2020

01-03-2020 | Colorectal Cancer | Review

Diet and Gut Microbes Act Coordinately to Enhance Programmed Cell Death and Reduce Colorectal Cancer Risk

Authors: Robert S. Chapkin, Sandi L. Navarro, Meredith A. J. Hullar, Johanna W. Lampe

Published in: Digestive Diseases and Sciences | Issue 3/2020

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Abstract

Diet is an important risk factor for colorectal cancer (CRC), and several dietary constituents implicated in CRC are modified by gut microbial metabolism. Microbial fermentation of dietary fiber produces short-chain fatty acids, e.g., acetate, propionate, and butyrate. Dietary fiber has been shown to reduce colon tumors in animal models, and, in vitro, butyrate influences cellular pathways important to cancer risk. Furthermore, work from our group suggests that the combined effects of butyrate and omega-3 polyunsaturated fatty acids (n-3 PUFA) may enhance the chemopreventive potential of these dietary constituents. We postulate that the relatively low intakes of n-3 PUFA and fiber in Western populations and the failure to address interactions between these dietary components may explain why chemoprotective effects of n-3 PUFA and fermentable fibers have not been detected consistently in prospective cohort studies. In this review, we summarize the evidence outlining the effects of n-3 long-chain PUFA and highly fermentable fiber with respect to alterations in critical pathways important to CRC prevention, particularly intrinsic mitochondrial-mediated programmed cell death resulting from the accumulation of lipid reactive oxygen species (ferroptosis), and epigenetic programming related to lipid catabolism and beta-oxidation-associated genes.
Literature
1.
Trock B, Lanza E, Greenwald P. Dietary fiber, vegetables, and colon cancer: critical review and meta-analyses of the epidemiologic evidence. Natl Cancer Inst. 2018;1990:650–661.
2.
Ben Q, Sun Y, Chai R, Qian A, Xu B, Yuan Y. Dietary fiber intake reduces risk for colorectal adenoma: a meta-analysis. Gastroenterology. 2014;146(689–699):e686.
3.
Perez-Cueto FJ, Verbeke W. Consumer implications of the WCRF’s permanent update on colorectal cancer. Meat Sci. 2012;90:977–978.PubMedCrossRef
4.
5.
Schatzkin A, Mouw T, Park Y, et al. Dietary fiber and whole-grain consumption in relation to colorectal cancer in the NIH-AARP Diet and Health Study. Am J Clin Nutr. 2007;85:1353–1360.PubMedCrossRef
6.
Murphy N, Norat T, Ferrari P, et al. Dietary fibre intake and risks of cancers of the colon and rectum in the European prospective investigation into cancer and nutrition (EPIC). PLoS One. 2012;7:e39361.PubMedPubMedCentralCrossRef
7.
Aune D, Chan DS, Lau R, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ. 2011;343:d6617.PubMedPubMedCentralCrossRef
8.
Navarro SL, Neuhouser ML, Cheng TD, et al. The interaction between dietary fiber and fat and risk of colorectal cancer in the women’s health initiative. Nutrients. 2016;8:779.PubMedCentralCrossRef
9.
10.
11.
Young GP, Hu Y, Le Leu RK, Nyskohus L. Dietary fibre and colorectal cancer: a model for environment–gene interactions. Mol Nutr Food Res. 2005;49:571–584.PubMedCrossRef
12.
13.
Chen T, Long W, Zhang C, Liu S, Zhao L, Hamaker BR. Fiber-utilizing capacity varies in Prevotella- versus Bacteroides-dominated gut microbiota. Sci Rep. 2017;7:2594.PubMedPubMedCentralCrossRef
14.
Donohoe DR, Bultman SJ. Metaboloepigenetics: interrelationships between energy metabolism and epigenetic control of gene expression. J Cell Physiol. 2012;227:3169–3177.PubMedPubMedCentralCrossRef
15.
Donohoe DR, Garge N, Zhang X, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13:517–526.PubMedPubMedCentralCrossRef
16.
Wang T, Cai G, Qiu Y, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012;6:320–329.PubMedCrossRef
17.
Wu N, Yang X, Zhang R, et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 2013;66:462–470.PubMedCrossRef
18.
Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL, Ryan EP. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One. 2013;8:e70803.PubMedPubMedCentralCrossRef
19.
Patnode ML, Beller ZW, Han ND, et al. Interspecies competition impacts targeted manipulation of human gut bacteria by fiber-derived. Glycans Cell. 2019;179(59–73):e13.
20.
Makki K, Deehan EC, Walter J, Backhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe. 2018;23:705–715.PubMedCrossRef
21.
Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915–923.PubMedCrossRef
22.
Uchida K, Kono S, Yin G, et al. Dietary fiber, source foods and colorectal cancer risk: the Fukuoka Colorectal Cancer Study. Scand J Gastroenterol. 2010;45:1223–1231.PubMedCrossRef
23.
Wakai K, Date C, Fukui M, et al. Dietary fiber and risk of colorectal cancer in the Japan collaborative cohort study. Cancer Epidemiol Biomarkers Prev. 2007;16:668–675.PubMedCrossRef
24.
Levi F, Pasche C, Lucchini F, La Vecchia C. Dietary fibre and the risk of colorectal cancer. Eur J Cancer. 2001;37:2091–2096.PubMedCrossRef
25.
Freudenheim JL, Graham S, Horvath PJ, Marshall JR, Haughey BP, Wilkinson G. Risks associated with source of fiber and fiber components in cancer of the colon and rectum. Cancer Res. 1990;50:3295–3300.PubMed
26.
Le Marchand L, Hankin JH, Wilkens LR, Kolonel LN, Englyst HN, Lyu LC. Dietary fiber and colorectal cancer risk. Epidemiology. 1997;8:658–665.PubMedCrossRef
27.
Negri E, Franceschi S, Parpinel M, La Vecchia C. Fiber intake and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev.. 1998;7:667–671.PubMed
28.
Sellem L, Srour B, Gueraud F, et al. Saturated, mono- and polyunsaturated fatty acid intake and cancer risk: results from the French prospective cohort. NutriNet-Sante Eur J Nutr.. 2019;58:1515–1527.PubMedCrossRef
29.
30.
Simopoulos AP. Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet. World Rev Nutr Diet. 2011;102:10–21.PubMedCrossRef
31.
Skender B, Vaculova AH, Hofmanova J. Docosahexaenoic fatty acid (DHA) in the regulation of colon cell growth and cell death: a review. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub.. 2012;156:186–199.PubMedCrossRef
32.
Azer SS. Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development. Eur J Gastroenterol Hepatol.. 2012;25:271–281.CrossRef
33.
Cockbain AJ, Toogood GJ, Hull MA. Omega-3 polyunsaturated fatty acids for the treatment and prevention of colorectal cancer. Gut. 2012;61:135–149.PubMedCrossRef
34.
Chang WC, Chapkin RS, Lupton JR. Predictive value of proliferation, differentiation and apoptosis as intermediate markers for colon tumorigenesis. Carcinogenesis. 1997;18:721–730.PubMedCrossRef
35.
Hou TY, Davidson LA, Kim E, et al. Nutrient-gene interaction in colon cancer, from the membrane to cellular physiology. Annu Rev Nutr. 2016;36:543–570.PubMedPubMedCentralCrossRef
36.
37.
Fuentes NR, Mlih M, Barhoumi R, et al. Long-chain n-3 fatty acids attenuate oncogenic KRas-driven proliferation by altering plasma membrane nanoscale proteolipid composition. Cancer Res. 2018;78:3899–3912.PubMedPubMedCentralCrossRef
38.
Wu S, Feng B, Li K, et al. Fish consumption and colorectal cancer risk in humans: a systematic review and meta-analysis. Am J Med.. 2012;125(551–559):e555.
39.
Geelen A, Schouten JM, Kamphuis C, et al. Fish consumption, n-3 fatty acids, and colorectal cancer: a meta-analysis of prospective cohort studies. Am J Epidemiol. 2007;166:1116–1125.PubMedCrossRef
40.
MacLean CH, Newberry SJ, Mojica WA, et al. Effects of omega-3 fatty acids on cancer risk: a systematic review. JAMA. 2006;295:403–415.PubMedCrossRef
41.
Gerber M. Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies. Br J Nutr. 2012;107:S228–S239.PubMedCrossRef
42.
Song M, Chan AT, Fuchs CS, et al. Dietary intake of fish, omega-3 and omega-6 fatty acids and risk of colorectal cancer: a prospective study in U.S. men and women. Int J Cancer. 2014;135:2413–2423.PubMedPubMedCentralCrossRef
43.
Song M, Nishihara R, Cao Y, et al. Marine omega-3 polyunsaturated fatty acid intake and risk of colorectal cancer characterized by tumor-infiltrating T cells. JAMA Oncol. 2016;2:1197–1206.PubMedPubMedCentralCrossRef
44.
Kantor ED, Lampe JW, Peters U, Vaughan TL, White E. Long-chain omega-3 polyunsaturated fatty acid intake and risk of colorectal cancer. Nutr Cancer.. 2014;66:716–727.PubMedCrossRef
45.
Van Blarigan EL, Fuchs CS, Niedzwiecki D, et al. Marine omega-3 polyunsaturated fatty acid and fish intake after colon cancer diagnosis and survival: CALGB 89803 (alliance). Cancer Epidemiol Biomarkers Prev. 2018;27:438–445.PubMedPubMedCentralCrossRef
46.
Chapkin RS, Fan Y, Lupton JR. Effect of diet on colonic-programmed cell death: molecular mechanism of action. Toxicol Lett.. 2000;112–113:411–414.PubMedCrossRef
47.
Cho Y, Turner ND, Davidson LA, Chapkin RS, Carroll RJ, Lupton JR. Colon cancer cell apoptosis is induced by combined exposure to the n-3 fatty acid docosahexaenoic acid and butyrate through promoter methylation. Exp Biol Med (Maywood). 2014;239:302–310.CrossRef
48.
Kolar S, Barhoumi R, Jones CK, et al. Interactive effects of fatty acid and butyrate-induced mitochondrial Ca(2)(+) loading and apoptosis in colonocytes. Cancer. 2011;117:5294–5303.PubMedCrossRef
49.
Kansal S, Negi AK, Bhatnagar A, Agnihotri N. Ras signaling pathway in the chemopreventive action of different ratios of fish oil and corn oil in experimentally induced colon carcinogenesis. Nutr Cancer.. 2012;64:559–568.PubMedCrossRef
50.
Sarotra P, Kansal S, Sandhir R, Agnihotri N. Chemopreventive effect of different ratios of fish oil and corn oil on prognostic markers, DNA damage and cell cycle in colon carcinogenesis. Eur J Cancer Prev. 2012;21:147–154.PubMedCrossRef
51.
Kolar SS, Barhoumi R, Callaway ES, et al. Synergy between docosahexaenoic acid and butyrate elicits p53-independent apoptosis via mitochondrial Ca(2 +) accumulation in colonocytes. Am J Physiol Gastrointest Liver Physiol.. 2007;293:G935–G943.PubMedCrossRef
52.
53.
O’Keefe SJ, Li JV, Lahti L, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;6:6342.PubMedCrossRef
54.
Kraja B, Muka T, Ruiter R, et al. Dietary fiber intake modifies the positive association between n-3 PUFA intake and colorectal cancer risk in a caucasian population. J Nutr.. 2015;145:1709–1716.PubMedCrossRef
55.
Sanders LM, Henderson CE, Hong MY, et al. An increase in reactive oxygen species by dietary fish oil coupled with the attenuation of antioxidant defenses by dietary pectin enhances rat colonocyte apoptosis. J Nutr. 2004;134:3233–3238.PubMedCrossRef
56.
Vanamala J, Glagolenko A, Yang P, et al. Dietary fish oil and pectin enhance colonocyte apoptosis in part through suppression of PPARdelta/PGE2 and elevation of PGE3. Carcinogenesis. 2008;29:790–796.PubMedCrossRef
57.
Crim KC, Sanders LM, Hong MY, et al. Upregulation of p21Waf1/Cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. Carcinogenesis. 2008;29:1415–1420.PubMedPubMedCentralCrossRef
58.
Cho Y, Kim H, Turner ND, et al. A chemoprotective fish oil- and pectin-containing diet temporally alters gene expression profiles in exfoliated rat colonocytes throughout oncogenesis. J Nutr. 2011;141:1029–1035.PubMedPubMedCentralCrossRef
59.
Chapkin RS, DeClercq V, Kim E, Fuentes NR, Fan YY. Mechanisms by Which Pleiotropic Amphiphilic n-3 PUFA Reduce Colon Cancer Risk. Curr Colorectal Cancer Rep. 2014;10:442–452.PubMedPubMedCentralCrossRef
60.
Triff K, Kim E, Chapkin RS. Chemoprotective epigenetic mechanisms in a colorectal cancer model: Modulation by n-3 PUFA in combination with fermentable fiber. Curr Pharmacol Rep. 2015;1:11–20.PubMedPubMedCentralCrossRef
61.
Kolar SS, Barhoumi R, Lupton JR, Chapkin RS. Docosahexaenoic acid and butyrate synergistically induce colonocyte apoptosis by enhancing mitochondrial Ca2 + accumulation. Cancer Res. 2007;67:5561–5568.PubMedCrossRef
62.
Jiang YH, Lupton JR, Chapkin RS. Dietary fat and fiber modulate the effect of carcinogen on colonic protein kinase C lambda expression in rats. J Nutr.. 1997;127:1938–1943.PubMedCrossRef
63.
Triff K, McLean MW, Callaway E, Goldsby J, Ivanov I, Chapkin RS. Dietary fat and fiber interact to uniquely modify global histone post-translational epigenetic programming in a rat colon cancer progression model. Int J Cancer. 2018;143:1402–1415.PubMedPubMedCentralCrossRef
64.
Zimmerman MA, Singh N, Martin PM, et al. Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1405–G1415.PubMedPubMedCentralCrossRef
65.
Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell.. 2012;48:612–626.PubMedPubMedCentralCrossRef
66.
Bultman SJ. Molecular pathways: gene-environment interactions regulating dietary fiber induction of proliferation and apoptosis via butyrate for cancer prevention. Clin Cancer Res. 2014;20:799–803.PubMedCrossRef
67.
Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology. 1982;83:424–429.PubMedCrossRef
68.
Ng Y, Barhoumi R, Tjalkens RB, et al. The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes. Carcinogenesis. 2005;26:1914–1921.PubMedCrossRef
69.
Fan YY, Zhan Y, Aukema HM, et al. Proapoptotic effects of dietary (n-3) fatty acids are enhanced in colonocytes of manganese-dependent superoxide dismutase knockout mice. J Nutr. 2009;139:1328–1332.PubMedPubMedCentralCrossRef
70.
Fan YY, Ran Q, Toyokuni S, et al. Dietary fish oil promotes colonic apoptosis and mitochondrial proton leak in oxidatively stressed mice. Cancer Prev Res (Phila).. 2011;4:1267–1274.PubMedPubMedCentralCrossRef
71.
Kelso GF, Porteous CM, Coulter CV, et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem.. 2001;276:4588–4596.PubMedCrossRef
72.
Lyn PC, Lim TH. Listeria meningitis resistant to ampicillin. J Singapore Paediatr Soc.. 1986;28:247–249.PubMed
73.
Stockwell BR, Friedmann Angeli JP, Bayir H, et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell. 2017;171:273–285.PubMedPubMedCentralCrossRef
74.
Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol. 2003;4:552–565.PubMedCrossRef
75.
Bedi A, Pasricha PJ, Akhtar AJ, et al. Inhibition of apoptosis during development of colorectal cancer. Cancer Res. 1995;55:1811–1816.PubMed
76.
Shah MS, Kim E, Davidson LA, et al. Comparative effects of diet and carcinogen on microRNA expression in the stem cell niche of the mouse colonic crypt. Biochim Biophys Acta. 1862;2016:121–134.
77.
Litvak Y, Byndloss MX, Tsolis RM, Baumler AJ. Dysbiotic proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6.PubMedCrossRef
78.
79.
Kelly CJ, Zheng L, Campbell EL, et al. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe. 2015;17:662–671.PubMedPubMedCentralCrossRef
80.
81.
Lampe JW, Kim E, Levy L, et al. Colonic mucosal and exfoliome transcriptomic profiling and fecal microbiome response to a flaxseed lignan extract intervention in humans. Am J Clin Nutr. 2019;110:377–390.PubMedPubMedCentralCrossRef
82.
David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563.PubMedCrossRef
83.
Hooda S, Boler BM, Serao MC, et al. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. J Nutr.. 2012;142:1259–1265.PubMedCrossRef
84.
Ross AB, Bruce SJ, Blondel-Lubrano A, et al. A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects. Br J Nutr. 2011;105:1492–1502.PubMedCrossRef
85.
Costabile A, Klinder A, Fava F, et al. Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr. 2008;99:110–120.PubMedCrossRef
86.
Finley JW, Burrell JB, Reeves PG. Pinto bean consumption changes SCFA profiles in fecal fermentations, bacterial populations of the lower bowel, and lipid profiles in blood of humans. J Nutr. 2007;137:2391–2398.PubMedCrossRef
87.
Smith SC, Choy R, Johnson SK, Hall RS, Wildeboer-Veloo AC, Welling GW. Lupin kernel fiber consumption modifies fecal microbiota in healthy men as determined by rRNA gene fluorescent in situ hybridization. Eur J Nutr. 2006;45:335–341.PubMedCrossRef
88.
Johnson SK, Chua V, Hall RS, Baxter AL. Lupin kernel fibre foods improve bowel function and beneficially modify some putative faecal risk factors for colon cancer in men. Br J Nutr. 2006;95:372–378.PubMedCrossRef
89.
Tuohy KM, Kolida S, Lustenberger AM, Gibson GR. The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides–a human volunteer study. Br J Nutr.. 2001;86:341–348.PubMedCrossRef
90.
Hylla S, Gostner A, Dusel G, et al. Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. Am J Clin Nutr. 1998;67:136–142.PubMedCrossRef
91.
92.
Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol. 2012;10:538–550.PubMedCrossRef
93.
94.
Lozupone C, Faust K, Raes J, et al. Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res. 2012;22:1974–1984.PubMedPubMedCentralCrossRef
95.
Bolca S, Van de Wiele T, Possemiers S. Gut metabotypes govern health effects of dietary polyphenols. Curr Opin Biotechnol. 2013;24:220–225.PubMedCrossRef
96.
Heinzmann SS, Merrifield CA, Rezzi S, et al. Stability and robustness of human metabolic phenotypes in response to sequential food challenges. J Proteome Res. 2012;11:643–655.PubMedCrossRef
97.
Walker AW, Ince J, Duncan SH, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–230.PubMedCrossRef
98.
Weickert MO, Arafat AM, Blaut M, et al. Changes in dominant groups of the gut microbiota do not explain cereal-fiber induced improvement of whole-body insulin sensitivity. Nutr Metab (Lond). 2011;8:90.CrossRef
99.
Russell WR, Gratz SW, Duncan SH, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr.. 2011;93:1062–1072.PubMedCrossRef
100.
Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007;73:1073–1078.PubMedCrossRef
101.
Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature.. 2006;444:1022–1023.PubMedCrossRef
102.
Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28:1221–1227.PubMedPubMedCentralCrossRef
103.
Louis P, McCrae SI, Charrier C, Flint HJ. Organization of butyrate synthetic genes in human colonic bacteria: phylogenetic conservation and horizontal gene transfer. FEMS Microbiol Lett.. 2007;269:240–247.PubMedCrossRef
104.
Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007;102:1197–1208.PubMedCrossRef
105.
Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol. 2008;6:776–788.PubMedPubMedCentralCrossRef
106.
107.
108.
Barcenilla A, Pryde SE, Martin JC, et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol. 2000;66:1654–1661.PubMedPubMedCentralCrossRef
109.
Matthies C, Schink B. Fermentative degradation of glutarate via decarboxylation by newly isolated strictly anaerobic bacteria. Arch Microbiol. 1992;157:290–296.PubMedCrossRef
110.
Matthies C, Schink B. Reciprocal isomerization of butyrate and isobutyrate by the strictly anaerobic bacterium strain WoG13 and methanogenic isobutyrate degradation by a defined triculture. Appl Environ Microbiol.. 1992;58:1435–1439.PubMedPubMedCentralCrossRef
111.
112.
Gharbia SE, Shah HN. Pathways of glutamate catabolism among Fusobacterium species. J Gen Microbiol. 1991;137:1201–1206.PubMedCrossRef
113.
Gerhardt A, Cinkaya I, Linder D, Huisman G, Buckel W. Fermentation of 4-aminobutyrate by Clostridium aminobutyricum: cloning of two genes involved in the formation and dehydration of 4-hydroxybutyryl-CoA. Arch Microbiol.. 2000;174:189–199.PubMedCrossRef
114.
Buckel W. Unusual enzymes involved in five pathways of glutamate fermentation. Appl Microbiol Biotechnol. 2001;57:263–273.PubMedCrossRef
115.
Kreimeyer A, Perret A, Lechaplais C, et al. Identification of the last unknown genes in the fermentation pathway of lysine. J Biol Chem. 2007;282:7191–7197.PubMedCrossRef
116.
Potrykus J, White RL, Bearne SL. Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium. Proteomics. 2008;8:2691–2703.PubMedCrossRef
117.
Uematsu H, Hoshino E. Degradation of arginine and other amino acids by Eubacterium nodatum ATCC 33099. Microb Ecol Health Dis.. 1996;9:305–311.CrossRef
118.
Hippe B, Zwielehner J, Liszt K, Lassl C, Unger F, Haslberger AG. Quantification of butyryl CoA:acetate CoA-transferase genes reveals different butyrate production capacity in individuals according to diet and age. FEMS Microbiol Lett. 2011;316:130–135.PubMedCrossRef
119.
Louis P, Young P, Holtrop G, Flint HJ. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol.. 2010;12:304–314.PubMedCrossRef
120.
Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294:1–8.PubMedCrossRef
121.
Duncan SH, Barcenilla A, Ste wart CS, Pryde SE, Flint HJ. Acetate utilization and butyryl coenzyme A, :acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl Environ Microbiol.. 2002;68:5186–5190.PubMedPubMedCentralCrossRef
122.
Vital M, Gao J, Rizzo M, Harrison T, Tiedje JM. Diet is a major factor governing the fecal butyrate-producing community structure across mammalia, aves and reptilia. ISME J.. 2015;9:832–843.PubMedCrossRef
123.
Fernandes J, Wang A, Su W, et al. Age, dietary fiber, breath methane, and fecal short chain fatty acids are interrelated in Archaea-positive humans. J Nutr. 2013;143:1269–1275.PubMedCrossRef
124.
Guy CJ. Abell MACALM. Methanogenic archaea in adult human faecal samples are inversely related to butyrate concentration. Microb Ecol Health Dis. 2006;18:154–160.
125.
126.
Cheng J, Ogawa K, Kuriki K, et al. Increased intake of n-3 polyunsaturated fatty acids elevates the level of apoptosis in the normal sigmoid colon of patients polypectomized for adenomas/tumors. Cancer Lett.. 2003;193:17–24.PubMedCrossRef
127.
Courtney ED, Matthews S, Finlayson C, et al. Eicosapentaenoic acid (EPA) reduces crypt cell proliferation and increases apoptosis in normal colonic mucosa in subjects with a history of colorectal adenomas. Int J Colorectal Dis.. 2007;22:765–776.PubMedCrossRef
128.
Lochhead P, Chan AT, Nishihara R, et al. Etiologic field effect: reappraisal of the field effect concept in cancer predisposition and progression. Mod Pathol. 2015;28:14–29.PubMedCrossRef
129.
130.
131.
132.
O’Keefe SJ. Nutrition and colonic health: the critical role of the microbiota. Curr Opin Gastroenterol. 2008;24:51–58.PubMedCrossRef
133.
Patterson E, O’Doherty RM, Murphy EF, et al. Impact of dietary fatty acids on metabolic activity and host intestinal microbiota composition in C57BL/6 J mice. Br J Nutr.. 2014;111:1905–1917.PubMedCrossRef
134.
Tabbaa M, Golubic M, Roizen MF, Bernstein AM. Docosahexaenoic acid, inflammation, and bacterial dysbiosis in relation to periodontal disease, inflammatory bowel disease, and the metabolic syndrome. Nutrients. 2013;5:3299–3310.PubMedPubMedCentralCrossRef
135.
Urwin HJ, Miles EA, Noakes PS, et al. Effect of salmon consumption during pregnancy on maternal and infant faecal microbiota, secretory IgA and calprotectin. Br J Nutr. 2014;111:773–784.PubMedCrossRef
136.
Geier MS, Torok VA, Allison GE, et al. Dietary omega-3 polyunsaturated fatty acid does not influence the intestinal microbial communities of broiler chickens. Poult Sci.. 2009;88:2399–2405.PubMedCrossRef
137.
Yu HN, Zhu J, Pan WS, Shen SR, Shan WG, Das UN. Effects of fish oil with a high content of n-3 polyunsaturated fatty acids on mouse gut microbiota. Arch Med Res.. 2014;45:195–202.PubMedCrossRef
138.
Sun M, Zhou Z, Dong J, Zhang J, Xia Y, Shu R. Antibacterial and antibiofilm activities of docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) against periodontopathic bacteria. Microb Pathog.. 2016;99:196–203.PubMedCrossRef
139.
Rodes L, Khan A, Paul A, et al. Effect of probiotics Lactobacillus and Bifidobacterium on gut-derived lipopolysaccharides and inflammatory cytokines: an in vitro study using a human colonic microbiota model. J Microbiol Biotechnol. 2013;23:518–526.PubMedCrossRef
140.
Elmadfa I, Klein P, Meyer AL. Immune-stimulating effects of lactic acid bacteria in vivo and in vitro. Proc Nutr Soc. 2010;69:416–420.PubMedCrossRef
141.
Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–1481.PubMedCrossRef
142.
Karlsson H, Larsson P, Wold AE, Rudin A. Pattern of cytokine responses to gram-positive and gram-negative commensal bacteria is profoundly changed when monocytes differentiate into dendritic cells. Infect Immun. 2004;72:2671–2678.PubMedPubMedCentralCrossRef
143.
Desbois AP, Smith VJ. Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol.. 2010;85:1629–1642.PubMedCrossRef
144.
Mima K, Cao Y, Chan AT, et al. Fusobacterium nucleatum in colorectal carcinoma tissue according to tumor location. Clin Transl Gastroenterol. 2016;7:e200.PubMedPubMedCentralCrossRef
145.
Mehta RS, Nishihara R, Cao Y, et al. Association of Dietary Patterns With Risk of Colorectal Cancer Subtypes Classified by Fusobacterium nucleatum in Tumor Tissue. JAMA Oncol. 2017;3:921–927.PubMedPubMedCentralCrossRef
146.
Barone M, Notarnicola M, Caruso MG, et al. Olive oil and omega-3 polyunsaturated fatty acids suppress intestinal polyp growth by modulating the apoptotic process in ApcMin/+ mice. Carcinogenesis. 2014;35:1613–1619.PubMedCrossRef
147.
Piazzi G, D’Argenio G, Prossomariti A, et al. Eicosapentaenoic acid free fatty acid prevents and suppresses colonic neoplasia in colitis-associated colorectal cancer acting on Notch signaling and gut microbiota. Int J Cancer.. 2014;135:2004–2013.PubMedCrossRef
148.
Han YM, Park JM, Cha JY, Jeong M, Go EJ, Hahm KB. Endogenous conversion of omega-6 to omega-3 polyunsaturated fatty acids in fat-1 mice attenuated intestinal polyposis by either inhibiting COX-2/beta-catenin signaling or activating 15-PGDH/IL-18. Int J Cancer.. 2016;138:2247–2256.PubMedCrossRef
149.
Pot GK, Geelen A, van Heijningen EM, Siezen CL, van Kranen HJ, Kampman E. Opposing associations of serum n-3 and n-6 polyunsaturated fatty acids with colorectal adenoma risk: an endoscopy-based case-control study. Int J Cancer.. 2008;123:1974–1977.PubMedCrossRef
150.
Goncalves P, Martel F. Butyrate and colorectal cancer: the role of butyrate transport. Curr Drug Metab.. 2013;14:994–1008.PubMedCrossRef
151.
Sengupta S, Tjandra JJ, Gibson PR. Dietary fiber and colorectal neoplasia. Dis Colon Rectum. 2001;44:1016–1033.PubMedCrossRef
152.
McIntyre A, Gibson PR, Young GP. Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut. 1993;34:386–391.PubMedPubMedCentralCrossRef
153.
Asano T, McLeod RS. Dietary fibre for the prevention of colorectal adenomas and carcinomas. Cochrane Database Syst Rev. 2002;003430.
Metadata
Title
Diet and Gut Microbes Act Coordinately to Enhance Programmed Cell Death and Reduce Colorectal Cancer Risk
Authors
Robert S. Chapkin
Sandi L. Navarro
Meredith A. J. Hullar
Johanna W. Lampe
Publication date
01-03-2020
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 3/2020
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-020-06106-8

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