The Gut Microbiota and Epigenetics
DOI:
https://doi.org/10.6000/1929-5634.2016.05.02.4Keywords:
Gut microbiota, nutrition, disease, epigeneticsAbstract
The human gut microbiota presents a strong influence on health and disease development. Metagenomic analysis has revealed the importance of the interaction between the genomes of food, gut microbiota and the host. Also, the establishment of humanized mouse gut microbiota in appropriate animal models has further contributed to the understanding of its function. The composition of the gut microbiota presents a significant impact on the risk of disease development supported by findings of substantial individual variations. Many low molecular weight bacterial substances have been indicated to affect chromatin remodeling, regulation of apoptosis, cellular differentiation and inflammation. The gut microbiota has also been linked to the etiology of cancer because of how it can alter dietary exposures. Furthermore, microbial metabolites have been associated with epigenetic modifications, reversible heritable changes in gene expression without alterations in the primary DNA sequence, which may influence the risk of various cancers and other diseases. As many microbial metabolites are absorbed into systemic circulation, gene expression might also be affected in distal regions of the gut. Therefore, the interaction of dietary intake, gut microbiota and epigenetic modifications plays an important role in disease risk, development and prevention.
References
Paul B, Barnes S, Demark-Wahnefried W, et al. Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clin Epigenetics 2015; 7: 112. http://dx.doi.org/10.1186/s13148-015-0144-7
Takahashi K. Influence of bacteria on epigenetic gene control. Cell Mol Life Sci 2014; 71: 1045-54. http://dx.doi.org/10.1007/s00018-013-1487-x
Kussman M, Van Bladeren PJ. The extended nutrigenomics – understanding the interplay between the genomes of food, gut microbes, and human host. Front Genet 2011; 2: 21. http://dx.doi.org/10.3389/fgene.2011.00021
Noble D. Conrad Waddington and the origin of epigenetics. J Exp Biol 2015; 218: 816-8. http://dx.doi.org/10.1242/jeb.120071
Su LJ, Mahabir S, Ellison GL, et al. Epigenetic contributions to the relationship between cancer and dietary intake of nutrients, bioactive food components and environmental toxicants. Front Genet 2012; 2: 1-11. http://dx.doi.org/10.3389/fgene.2011.00091
Fang M, Chen D, Yang CS. Dietary polyphenols may affect DNA methylation. J Nutr 2007; 137: 223S-228S.
Boehm TL, Drahovsky D. Alteration of enzymatic methylation of DNA cytosines by chemical carcinogens; a mechanism involved in the initiation of carcinogenesis. J Natl Cancer Inst 1983; 71: 429-33.
Costello JF, Plass C. Methylation matters. J Med Genet 2001; 38: 285-303. http://dx.doi.org/10.1136/jmg.38.5.285
Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128: 683-92. http://dx.doi.org/10.1016/j.cell.2007.01.029
Cheishvili D, Boureau L, Szyf M. DNA demethylation and invasive cancer: implications for therapeutics. Br J Pharmacol 2015; 172: 2705-15. http://dx.doi.org/10.1111/bph.12885
Bollati V, Baccarelli A. Environmental epigenetics. Heredity 2010; 105: 105-12. http://dx.doi.org/10.1038/hdy.2010.2
Yang PH, Zhang L, Zhang YJ, et al. HDAC6: physiological function and its selective inhibitors for cancer treatment. Drug Discov Ther 2013; 7: 233-42. http://dx.doi.org/10.5582/ddt.2013.v7.6.233
Duenas-Gonzalez A, Coronel J, Cetina L, et al. Hydralazine-valproate: a repositioned drug combination for the epigenetic therapy of cancer. Expert Opin Drug Metab Toxicol 2014; 10: 1433-44. http://dx.doi.org/10.1517/17425255.2014.947263
Lundstrom K. MicroRNA in disease and gene therapy. Curr Drug Discov Technol 2011; 8: 76-86. http://dx.doi.org/10.2174/157016311795563857
www.mirbase.org/cgi-bin/mirna-summary.pl?org=hsa (accessed February 25, 2016).
Shah PP, Hutchinson LE, Kakar SS. Emerging role of microRNAs in diagnosis and treatment of various diseases including ovarian cancer. J Ovarian Res 2009; 2: 11. http://dx.doi.org/10.1186/1757-2215-2-11
Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome; a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 1: 6ra 14.
Jeffrey IB, O’Toole PW. Diet-microbiota interactions and their implications for healthy living. Nutrients 2013; 5: 234-52. http://dx.doi.org/10.3390/nu5010234
Pompei A, Cordisco L, Amaretti A, et al. Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol 2007; 73: 179-85. http://dx.doi.org/10.1128/AEM.01763-06
Davie JR. Inhibition of histone deacetylase activity by butyrate. J Nutr 2003; 133: 24855-93.
Cannani RB, Constanzo MD, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics 2012; 4: 4. http://dx.doi.org/10.1186/1868-7083-4-4
Zgouras D, Wächterhäuser A, Frings D, et al. Butyrate impairs intestinal tumor cell-induced angiogenesis by inhibiting HIF-1α nuclear translocation. Biohem Biophys Res Commun 2003; 300: 155-65. http://dx.doi.org/10.1016/S0006-291X(02)02916-9
Shenderov BA. Metabiotics: novel idea or natural development of probiotic conception. Microbiol Ecol Heealth Dis 2013; 24. http://dx.doi.org/10.3402/mehd.v24i0.20399
Peserico A, Simone C. Physical and functional HAT/HDAC interplay regulates protein acetylation balance. BioMed Res Int 2010; 2011: 371832.
Carrer A, Wellen KE. Metabolism and epigenetics: a link cancer cells exploit. Curr Opin Biotechnol 2015; 34: 23-9. http://dx.doi.org/10.1016/j.copbio.2014.11.012
Shenderov BA, Midtvedt T. Epigenomic programming: a future way to health? Microbiol. Ecol Health Dis 2014; 25. http://dx.doi.org/10.3402/mehd.v25.24145
Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 6ra14. http://dx.doi.org/10.1126/scitranslmed.3000322
Cortese R, Lu L, Yu Y, et al. Epigenome-microbiome crosstalk: a new paradigm influencing neonatal susceptibility for disease. Epigenetics 2016; 11: 205-15. http://dx.doi.org/10.1080/15592294.2016.1155011
Favier CF, Vaughan EE, Vos WMD, et al. Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 2002; 68: 219-26. http://dx.doi.org/10.1128/AEM.68.1.219-226.2002
Augeron C, Laboisse CL. Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res 1984; 44: 3961-9.
Hague A, Manning AM, Hanlon KA, et al. Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer. Int J Cancer 1993; 55: 498-505. http://dx.doi.org/10.1002/ijc.2910550329
Candido EPM, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Get Cell 1978; 14: 105-13. http://dx.doi.org/10.1016/0092-8674(78)90305-7
Kumar H, Lund R, Laiho A, et al. Gut microbiota as an epigenetic regulator: pilot study based on whole-genome methylation analysis. MBio 2014; 5: e02113-4. http://dx.doi.org/10.1128/mBio.02113-14
Hughes R, Cross AJ, Pollock JRA, et al. Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation. Carcinogenesis 2001; 22: 199-202. http://dx.doi.org/10.1093/carcin/22.1.199
Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of Icarnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013; 19: 576-85. http://dx.doi.org/10.1038/nm.3145
Herr I, Buchler MW. Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev 2010; 36: 377-83. http://dx.doi.org/10.1016/j.ctrv.2010.01.002
Navarro SL, Li F, Lampe JW. Mechanisms of action of isothiocyanates in cancer chemoprevention: an update. Food Function 2011; 2: 578-87. http://dx.doi.org/10.1039/c1fo10114e
Meeran SM, Patel SN, Tollefsbol TO. Sulforaphane causes epigenetic repression of hTERT expression in human breast cancer cell lines. PLoS One 2010; 5: e11457. http://dx.doi.org/10.1371/journal.pone.0011457
Ohigashi S, Sudo K, Kbayashi D, et al. Changes of the intestinal microbiota, short chain fatty acids, and fecal pH in patients with colorectal cancer. Dig Dis Sci 2013; 58: 1717-26. http://dx.doi.org/10.1007/s10620-012-2526-4
McGarr SE, Ridlon JM, Hylemon PB. Diet, anaerobic bacterial metabolism, and colon cancer: a review of the literature. J Clin Gastroenterol 2005; 39: 98-109.
Wollowski I, Rechkemmer G, Pool-Zobel BI. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr 2001; 73: 451s.
Hullar MA, Fu BC. Diet, the gut microbiome and epigenetics. Cancer J 2014; 20: 170. http://dx.doi.org/10.1097/PPO.0000000000000053
Stringer AM, Gibson RJ, Bowen JM, et al. Chemotherapy-induced modifications to gastrointestinal microflora: evidence and implications of change. Curr Drug Metab 2009; 10: 79-83. http://dx.doi.org/10.2174/138920009787048419
Weir TL, Manter DK, Sheflin AM, et al. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One 2013; 8: e70803. http://dx.doi.org/10.1371/journal.pone.0070803
Gao Z, Guo B, Gao R, et al. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol 2015; 6: 20. http://dx.doi.org/10.3389/fmicb.2015.00020
Bultman SJ. Interplay between diet, gut microbiota, epigenetic events, and colorectal cancer. Mol Nutr Food Res 2016. http://dx.doi.org/10.1002/mnfr.201500902
Serban DE. Microbiota in inflammatory bowels disease pathogenesis and therapy: is it all about diet? Nutr Clin Pract 2015; 30: 760-79. http://dx.doi.org/10.1177/0884533615606898
Fuhrman BJ, Feigelson HS, Flores R, et al. Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J Clin Endicrinol Metabol 2014; 99: 46320-40. http://dx.doi.org/10.1210/jc.2014-2222
Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe 2011; 10: 324-35. http://dx.doi.org/10.1016/j.chom.2011.10.003
Mageroy MH, Tieman DM, Floystad A, et al. Solarium lycopersicum catechol-O-methyltransferase involved in synthesis of the flavor molecule gualacol. Plant J 2012; 69: 1043-51. http://dx.doi.org/10.1111/j.1365-313X.2011.04854.x
Dapito DH, Mencin A, Gwak GY, et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 2012; 21: 504-16. http://dx.doi.org/10.1016/j.ccr.2012.02.007
Takahashi K, Sugi Y, Nakano K, et al. Epigenetic control of the host gene by commensal bacteria in large intestinal epithelial cells. J Biol Chem 2011; 286: 35755-62. http://dx.doi.org/10.1074/jbc.M111.271007
Savidge TC. Epigenetic regulation of enteric neurotransmission by gut microbiota. Front Cell Neurosci 2016; 9: 503. http://dx.doi.org/10.3389/fncel.2015.00503
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