Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases
Open accessAbstract
Epigenetic modulation of gene activity occurs in response to non-genetic factors such as body weight status, physical activity, dietary factors, and environmental toxins. In addition, each of these factors is thought to affect and be affected by the gut microbiome. A primary mechanism that links these various factors together in mediating control of gene expression is the production of metabolites that serve as critical cofactors and allosteric regulators of epigenetic processes. Here, we review the involvement of the gut microbiota and its interactions with dietary factors, many of which have known cellular bioactivity, focusing on particular epigenetic processes affected and the influence they have on human health and disease, particularly cancer and response to treatment. Advances in DNA sequencing have expanded the capacity for studying the microbiome. Combining this with rapidly improving techniques to measure the metabolome provides opportunities to understand complex relationships that may underlie the development and progression of cancer as well as treatment-related sequelae. Given broad reaching and fundamental biology, both at the cellular and organismal levels, we propose that interactive research programs, which utilize a wide range of mutually informative experimental model systems-each one optimally suited for answering particular questions-provide the best path forward for breaking ground on new knowledge and ultimately understanding the epigenetic significance of the gut microbiome and its response to dietary factors in cancer prevention and therapy.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The gut microbiome induces host epigenetic changes that might contribute to the development of cancer.
“The gut microbiome has been shown to induce host epigenetic changes that might contribute to the development of cancer193,194”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [193]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Obesity alters gut microbial ecology
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504978102 · Cited by 6,176 · see citing works
Long non-coding RNAs: insights into functions
Mercer, T. R., Dinger, M. E., & Mattick, J. S. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2521 · Cited by 5,654 · see citing works
Non-coding RNAs in human disease
Esteller, M. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3074 · Cited by 4,825 · see citing works
Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis
Koeth, R. A., Wang, Z., Levison, B. S., Buffa, J. A., Org, E., Sheehy, B. T., Britt, E. B., Fu, X., Wu, Y., Li, L., et al. (2013) · Nature Medicine · doi:10.1038/nm.3145 · Cited by 4,386 · see citing works
Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43
Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H. C., Rolph, M. S., Mackay, F., Artis, D., et al. (2009) · Nature · doi:10.1038/nature08530 · Cited by 3,241 · see citing works
The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice
Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., & Gordon, J. I. (2009) · Science Translational Medicine · doi:10.1126/scitranslmed.3000322 · Cited by 3,058 · cited 1× · see citing works
“It has been shown that maternal and neonatal nutrition have a major impact on the epigenome of the offspring in that the food consumed modulates the composition of the gut microbiota and also the metabolites that they produce [89].”
BackgroundFactors influencing the composition of the intestinal microbiota in early infancy
Penders, J., Thijs, C., Vink, C., Stelma, F. F., Snijders, B., Kummeling, I., van den Brandt, P. A., & Stobberingh, E. E. (2006) · PEDIATRICS · doi:10.1542/peds.2005-2824 · Cited by 2,232 · see citing works
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179 · see citing works
<i>Fusobacterium nucleatum</i> infection is prevalent in human colorectal carcinoma
Castellarin, M., Warren, R. L., Freeman, J. D., Dreolini, L., Krzywinski, M., Strauss, J., Barnes, R., Watson, P., Allen-Vercoe, E., Moore, R. A., et al. (2012) · Genome Research · doi:10.1101/gr.126516.111 · Cited by 2,043 · see citing works
The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon
Donohoe, D. R., Garge, N., Zhang, X., Sun, W., O'Connell, T. M., Bunger, M. K., & Bultman, S. J. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.02.018 · Cited by 2,003 · cited 1× · see citing works
“SCFAs such as butyrate, acetate, and propionate, which are fermentation products from dietary fibers by colonic gut microbiota, can regulate neutrophil function and migration and exhibit anti-inflammatory activity [15].”
BackgroundInflammation-induced cancer: Crosstalk between tumours, immune cells and microorganisms
Elinav, E., Nowarski, R., Thaiss, C. A., Hu, B., Jin, C., & Flavell, R. A. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3611 · Cited by 2,000 · see citing works
Dent, S., Denu, J. M., & Allis, C. D. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.81 · Cited by 1,844 · see citing works
H OW H OST -M ICROBIAL I NTERACTIONS S HAPE THE N UTRIENT E NVIRONMENT OF THE M AMMALIAN I NTESTINE
Hooper, L. V., Midtvedt, T., & Gordon, J. I. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.011602.092259 · Cited by 1,623 · see citing works
Inhibition of Histone Deacetylase Activity by Butyrate
Davie, J. R. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.7.2485s · Cited by 1,515 · see citing works
Promotion of Hepatocellular Carcinoma by the Intestinal Microbiota and TLR4
Dapito, D. H., Mencin, A., Gwak, G.-Y., Pradere, J.-P., Jang, M.-K., Mederacke, I., Caviglia, J. M., Khiabanian, H., Adeyemi, A., Bataller, R., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.007 · Cited by 1,346 · see citing works
Rajilić–Stojanović, M., Biagi, E., Heilig, H. G. H. J., Kajander, K., Kekkonen, R. A., Tims, S., & de Vos, W. M. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.043 · Cited by 1,041 · see citing works
Sodium butyrate inhibits histone deacetylation in cultured cells
Candido, E. (1978) · Cell · doi:10.1016/0092-8674(78)90305-7 · Cited by 1,036 · see citing works
TETonic shift: biological roles of TET proteins in DNA demethylation and transcription
Pastor, W. A., Aravind, L., & Rao, A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3589 · Cited by 897 · cited 1× · see citing works
“They use a metabolite intermediate, α-ketoglutarate (α-KG), and molecular oxygen as enzyme cofactors for this reaction [65].”
BackgroundMolecular Monitoring of Succession of Bacterial Communities in Human Neonates
Favier, C. F., Vaughan, E. E., de Vos, W. M., & Akkermans, A. D. L. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.1.219-226.2002 · Cited by 859 · see citing works
Walker, A. W., Duncan, S. H., McWilliam Leitch, E. C., Child, M. W., & Flint, H. J. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.7.3692-3700.2005 · Cited by 796 · see citing works
Parracho, H. M., Bingham, M. O., Gibson, G. R., & McCartney, A. L. (2005) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46101-0 · Cited by 784 · see citing works
Plottel, C. S., & Blaser, M. J. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.003 · Cited by 743 · see citing works
Cai, L., Sutter, B. M., Li, B., & Tu, B. P. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.05.004 · Cited by 701 · see citing works
Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults
Weir, T. L., Manter, D. K., Sheflin, A. M., Barnett, B. A., Heuberger, A. L., & Ryan, E. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070803 · Cited by 642 · see citing works
Rowland, I. R., Wiseman, H., Sanders, T. A. B., Adlercreutz, H., & Bowey, E. A. (2000) · Nutrition and Cancer · doi:10.1207/s15327914nc3601_5 · Cited by 583 · see citing works
Protective role of probiotics and prebiotics in colon cancer
Wollowski, I., Rechkemmer, G., & Pool-Zobel, B. L. (2001) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.451s · Cited by 560 · see citing works
Augeron, C., & LABOISSE, C. L. (1984) · PubMed · Cited by 539 · see citing works
Microbiota disbiosis is associated with colorectal cancer
Gao, Z., Guo, B., Gao, R., Zhu, Q., & Qin, H. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00020 · Cited by 537 · see citing works
Hague, A., Manning, A. M., Hanlon, K. A., Hart, D. A., Paraskeva, C., & Huschtscha, L. I. (1993) · International Journal of Cancer · doi:10.1002/ijc.2910550329 · Cited by 531 · see citing works
Micros for microbes: non-coding regulatory RNAs in bacteria
Gottesman, S. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.05.008 · Cited by 500 · see citing works
The epigenetic effects of butyrate: potential therapeutic implications for clinical practice
Berni Canani, R., Di Costanzo, M., & Leone, L. (2012) · Clinical Epigenetics · doi:10.1186/1868-7083-4-4 · Cited by 431 · see citing works
Fecal microbiota in early rheumatoid arthritis.
Vaahtovuo, J., Munukka, E., Korkeamäki, M., Luukkainen, R., & Toivanen, P. (2008) · PubMed · Cited by 426 · see citing works
Cheon, D., & Oršulić, S. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.3.121806.154244 · Cited by 397 · see citing works
Sulforaphane Causes Epigenetic Repression of hTERT Expression in Human Breast Cancer Cell Lines
Meeran, S. M., Patel, S. N., & Tollefsbol, T. O. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011457 · Cited by 372 · see citing works
Self-citationPhysical and Functional HAT/HDAC Interplay Regulates Protein Acetylation Balance
Peserico, A., & Simone, C. (2010) · BioMed Research International · doi:10.1155/2011/371832 · Cited by 362 · see citing works
Folate Production by Bifidobacteria as a Potential Probiotic Property
Pompei, A., Cordisco, L., Amaretti, A., Zanoni, S., Matteuzzi, D., & Rossi, M. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01763-06 · Cited by 356 · see citing works
Fuhrman, B. J., Feigelson, H. S., Flores, R., Gail, M. H., Xu, X., Ravel, J., & Goedert, J. J. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2222 · Cited by 339 · see citing works
Herr, I., & Büchler, M. W. (2010) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2010.01.002 · Cited by 335 · see citing works
Samsel, A., & Seneff, S. (2013) · Entropy · doi:10.3390/e15041416 · Cited by 293 · see citing works
Martínez-Medina, M., Aldeguer, X., Gónzalez‐Huix, F., Acero, D., & Garcia-Gil, L. J. (2006) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000235828.09305.0c · Cited by 263 · see citing works
Diet, anaerobic bacterial metabolism, and colon cancer: a review of the literature.
McGarr, S. E., Ridlon, J. M., & Hylemon, P. B. (2005) · PubMed · Cited by 259 · see citing works
A Role for Gut Microbiota and the Metabolite‐Sensing Receptor GPR43 in a Murine Model of Gout
Vieira, A. T., Macia, L., Galvão, I., Martins, F. S., Canesso, M. C. C., Amaral, F. A., Garcia, C. C., Maslowski, K. M., Leon, E. D., Shim, D., et al. (2015) · Arthritis & Rheumatology · doi:10.1002/art.39107 · Cited by 252 · see citing works
Gut Microbiota as an Epigenetic Regulator: Pilot Study Based on Whole-Genome Methylation Analysis
Kumar, H., Lund, R., Laiho, A., Lundelin, K., Ley, R. E., Isolauri, E., & Salminen, S. (2014) · mBio · doi:10.1128/mbio.02113-14 · Cited by 236 · see citing works
Dose-dependent effect of dietary meat on endogenous colonic N-nitrosation
Hughes, R. (2001) · Carcinogenesis · doi:10.1093/carcin/22.1.199 · Cited by 234 · see citing works
Hu, S., Dong, T. S., Dalal, S. R., Wu, F., Bissonnette, M., Kwon, J. H., & Chang, E. B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016221 · Cited by 231 · see citing works
Epigenetic Cross-Talk between DNA Methylation and Histone Modifications in Human Cancers
Kondo, Y. (2009) · Yonsei Medical Journal · doi:10.3349/ymj.2009.50.4.455 · Cited by 223 · see citing works
Bolte, E. R. (1998) · Medical Hypotheses · doi:10.1016/s0306-9877(98)90107-4 · Cited by 213 · see citing works
Metabiotics: novel idea or natural development of probiotic conception
Ba, S. (2013) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v24i0.20399 · Cited by 212 · see citing works
Diet, the Gut Microbiome, and Epigenetics
Hullar, M. A. J., & Fu, B. C. (2014) · The Cancer Journal · doi:10.1097/ppo.0000000000000053 · Cited by 205 · see citing works
Current concepts on the role of inflammation in COPD and lung cancer
Yao, H., & Rahman, I. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.06.009 · Cited by 200 · see citing works
Release of Luminal Exosomes Contributes to TLR4-Mediated Epithelial Antimicrobial Defense
Hu, G., Gong, A.-Y., Roth, A. L., Huang, B. Q., Ward, H., Zhu, G., LaRusso, N. F., Hanson, N. D., & Chen, X. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003261 · Cited by 199 · see citing works
Diet-microbiota interactions and their implications for healthy living
Jeffery, I., & O'Toole, P. (2013) · Nutrients · doi:10.3390/nu5010234 · Cited by 199 · see citing works
Diet, microbiota and autoimmune diseases
Vieira, S., Pagovich, O., & Kriegel, M. A. (2014) · Lupus · doi:10.1177/0961203313501401 · Cited by 193 · see citing works
Erdman, S. E., Rao, V. P., Poutahidis, T., Rogers, A. B., Taylor, C. L., Jackson, E. A., Ge, Z., Lee, C. W., Schauer, D. B., Wogan, G. N., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812347106 · Cited by 183 · see citing works
Ohigashi, S., Sudo, K., Kobayashi, D., Takahashi, O., Takahashi, T., Asahara, T., Nomoto, K., & Onodera, H. (2013) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2526-4 · Cited by 182 · see citing works
Epigenetic Control of the Host Gene by Commensal Bacteria in Large Intestinal Epithelial Cells
Takahashi, K., Sugi, Y., Nakano, K., Tsuda, M., Kurihara, K., Hosono, A., & Kaminogawa, S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.271007 · Cited by 180 · see citing works
Taberlay, P. C., & Jones, P. A. (2010) · Springer eBooks · doi:10.1007/978-3-7643-8989-5_1 · Cited by 172 · see citing works
Ding, S., Goldberg, J. B., & Hatakeyama, M. (2010) · Future Oncology · doi:10.2217/fon.10.37 · Cited by 169 · see citing works
Barnes, S., PRASAIN, J. K., D'Alessandro, T. L., Arabshahi, A., Botting, N. P., Lila, M. A., Jackson, G. S., Janle, E. M., & Weaver, C. M. (2011) · Food & Function · doi:10.1039/c1fo10025d · Cited by 166 · see citing works
Self-citationJu, Y. H., Fultz, J., Allred, K. F., Doerge, D. R., & Helferich, W. G. (2006) · Carcinogenesis · doi:10.1093/carcin/bgi320 · Cited by 157 · see citing works
Induction of apoptosis in tumor cells by naturally occurring sulfur-containing compounds
WU, X., Kassie, F., & Mersch‐Sundermann, V. (2005) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2004.11.001 · Cited by 148 · see citing works
Hayashi, Y., Tsujii, M., Wang, J., et al. (2012) · Gut · doi:10.1136/gutjnl-2011-301625 · Cited by 144 · see citing works
Rodríguez, A. R. L. A. G. (2000) · Scandinavian Journal of Gastroenterology · doi:10.1080/003655200750024191 · Cited by 133 · see citing works
Saldanha, S. N., Kala, R., & Tollefsbol, T. O. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.01.024 · Cited by 132 · see citing works
Self-citationMechanisms of action of isothiocyanates in cancer chemoprevention: an update
Navarro, S. L., Li, F., & Lampe, J. W. (2011) · Food & Function · doi:10.1039/c1fo10114e · Cited by 129 · see citing works
Quantitative Dynamics of the Link between Cellular Metabolism and Histone Acetylation
Evertts, A. G., Zee, B. M., DiMaggio, P. A., Gonzales-Cope, M., Coller, H. A., & Garcia, B. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.428318 · Cited by 119 · see citing works
Albaugh, B. N., Arnold, K. M., & Denu, J. M. (2010) · ChemBioChem · doi:10.1002/cbic.201000438 · Cited by 117 · see citing works
Metabolic tinkering by the gut microbiome
Selkrig, J., Wong, P., Zhang, X., & Pettersson, S. (2014) · Gut Microbes · doi:10.4161/gmic.28681 · Cited by 116 · see citing works
Ding, S., Fischer, W. H., Kaparakis‐Liaskos, M., Liechti, G. W., Merrell, D. S., Grant, P. A., Ferrero, R. L., Crowe, S. E., Haas, R., Hatakeyama, M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009875 · Cited by 115 · see citing works
Stringer, A. M., Gibson, R. J., Bowen, J. M., & Keefe, D. M. K. (2009) · Current Drug Metabolism · doi:10.2174/138920009787048419 · Cited by 110 · see citing works
Metabolism and epigenetics: a link cancer cells exploit
Carrer, A., & Wellen, K. E. (2014) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.11.012 · Cited by 109 · see citing works
Heuck, C. J., Mehta, J., Bhagat, T. D., Gundabolu, K., Yu, Y., Khan, S. N., Chrysofakis, G., Schinke, C., Tariman, J. D., Vickrey, E., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202493 · Cited by 106 · see citing works
Magerøy, M. H., Tieman, D. M., Floystad, A., et al. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04854.x · Cited by 104 · see citing works
Chronic fatigue syndrome: lactic acid bacteria may be of therapeutic value.
Logan, A., Rao, A., & Irani, D. (2003) · Medical Hypotheses · doi:10.1016/s0306-9877(03)00096-3 · Cited by 99 · see citing works
Kuitunen, M., Saukkonen, T. T., Ilonen, J., Åkerblom, H. K., & Savilahti, E. (2002) · Autoimmunity · doi:10.1080/0891693021000008526 · Cited by 98 · see citing works
MicroRNAs: an emerging science in cancer epigenetics
Kala, R., Peek, G. W., Hardy, T. M., & Tollefsbol, T. (2013) · Journal of Clinical Bioinformatics · doi:10.1186/2043-9113-3-6 · Cited by 90 · see citing works
Self-citationZgouras, D., Wächtershäuser, A., Frings, D., & Stein, J. M. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02916-9 · Cited by 84 · see citing works
Phenotypic and functional characterization of intestinal epithelial exosomes
Mallegol, J., van Niel, G., & Heyman, M. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.04.001 · Cited by 83 · see citing works
Normalization of reproductive function in germfree mice following bacterial contamination
SHIMIZU, K., MURANAKA, Y., FUJIMURA, R., ISHIDA, H., TAZUME, S., & SHIMAMURA, T. (1998) · Experimental Animals · doi:10.1538/expanim.47.151 · Cited by 77 · see citing works
5‐Hydroxymethylcytosine: a new kid on the epigenetic block?
Matarese, F., Pau, E. C. D. S., & Stunnenberg, H. G. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.95 · Cited by 74 · see citing works
Gut indigenous microbiota and epigenetics
Shenderov, B. A. (2012) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v23i0.17195 · Cited by 73 · see citing works
The human microbiome: eliminating the biomedical/environmental dichotomy in microbial ecology
Ley, R. E., Knight, R., & Gordon, J. I. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01222_3.x · Cited by 71 · see citing works
Influence of bacteria on epigenetic gene control
Takahashi, K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1487-x · Cited by 69 · see citing works
Fehri, L. F., Rechner, C., Janßen, S., Mak, T. N., Holland, C., Bartfeld, S., Brüggemann, H., & Meyer, T. F. (2009) · Epigenetics · doi:10.4161/epi.4.8.10217 · Cited by 63 · see citing works
Epigenomic programing: a future way to health?
Ba, S., & Midtvedt, T. (2014) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v25.24145 · Cited by 58 · see citing works
Tsuji, S., Kawai, N., Tsujii, M., Kawano, S., & Hori, M. (2003) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.18.s1.22.x · Cited by 57 · see citing works
Lipid Metabolism by Gut Microbes and Atherosclerosis
Loscalzo, J. (2011) · Circulation Research · doi:10.1161/res.0b013e3182290620 · Cited by 54 · see citing works
Nör, C., Sassi, F. A., de Farias, C. B., Schwartsmann, G., Abujamra, A. L., Lenz, G., Brunetto, A. L., & Roesler, R. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8441-7 · Cited by 52 · see citing works
Legette, L. L., PRASAIN, J. K., King, J. L., Arabshahi, A., Barnes, S., & Weaver, C. M. (2014) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf400097m · Cited by 48 · see citing works
Self-citationLi, G., Su, H., Zhou, Z., & Yao, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097342 · Cited by 48 · see citing works
Epigenetics, development, and cancer: Zebrafish make their mark
Mudbhary, R., & Sadler, K. C. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20207 · Cited by 48 · see citing works
An Update on Helicobacter pylori as the Cause of Gastric Cancer
Zhang, W., Lü, H., & Graham, D. Y. (2014) · Gastrointestinal Tumors · doi:10.1159/000365310 · Cited by 39 · see citing works
Smythies, L. E., & Smythies, J. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00104 · Cited by 35 · see citing works
Hýžďalová, M., Hofmanová, J., Pachernı́k, J., Vaculová, A. H., & Kozubı́k, A. (2008) · Cytokine · doi:10.1016/j.cyto.2008.06.003 · Cited by 35 · see citing works
Metabostemness: Metaboloepigenetic reprogramming of cancer stem-cell functions
Menéndez, J. A., Corominas-Faja, B., Cuyàs, E., & Alarcón, T. (2014) · Oncoscience · doi:10.18632/oncoscience.113 · Cited by 32 · see citing works
Clinical significance of the interaction between non-coding RNAs and the epigenetics machinery
Maia, B. M., Rocha, R. M., & Călin, G. A. (2013) · Epigenetics · doi:10.4161/epi.26488 · Cited by 31 · see citing works
Living long and ageing well: is epigenomics the missing link between nature and nurture?
The ACUME2 Project, Rea, I. M., Dellett, M., & Mills, K. (2015) · Biogerontology · doi:10.1007/s10522-015-9589-5 · Cited by 29 · see citing works
Mechanistic links between COPD and lung cancer: a role of microRNA let-7?
Shin, J. I., & Brusselle, G. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3477-c1 · Cited by 23 · see citing works
Gut microbiota and obesity-related gastrointestinal cancer: a focus on epigenetics
Hesson, L. B. (2013) · Translational gastrointestinal cancer · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease
Yang, T., Richards, E. M., Pepine, C. J., & Raizada, M. K. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0018-2 · Cited by 753 · see citing works
Microbiome, inflammation, epigenetic alterations, and mental diseases
Alam, R., Abdolmaleky, H. M., & Zhou, J. (2017) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32567 · Cited by 240 · see citing works
Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health
Schagdarsurengin, U., & Steger, K. (2016) · Nature Reviews Urology · doi:10.1038/nrurol.2016.157 · Cited by 222 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
Epigenetic Regulation at the Interplay Between Gut Microbiota and Host Metabolism
Miro-Blanch, J., & Yanes, O. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00638 · Cited by 195 · see citing works
The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
Malan-Muller, S., Valles-Colomer, M., Raes, J., Lowry, C. A., Seedat, S., & Hemmings, S. M. J. (2018) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2017.0077 · Cited by 161 · see citing works
Williams, C. J., Gurd, B. J., Bonafiglia, J. T., Voisin, S., Li, Z., Harvey, N., Croci, I., Taylor, J. L., Gajanand, T., Ramos, J. S., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00019 · Cited by 117 · see citing works
Epigenetics in eating disorders: a systematic review
Hübel, C., Marzi, S. J., Breen, G., & Bulik, C. M. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0254-7 · Cited by 116 · see citing works
Inserra, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00330 · Cited by 91 · see citing works
Gut Microbiota Composition Is Associated with the Global DNA Methylation Pattern in Obesity
Ramos-Molina, B., Sánchez-Alcoholado, L., Cabrera-Mulero, A., Lopez-Dominguez, R., Carmona-Saez, P., Garcia-Fuentes, E., Moreno-Indias, I., & Tinahones, F. J. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00613 · Cited by 64 · see citing works
De Sales-Millán, A., Aguirre-Garrido, J. F., González-Cervantes, R. M., & Velázquez-Aragón, J. A. (2023) · doi:10.20944/preprints202305.1223.v1 · Cited by 44 · see citing works
Peng, Y., Tao, H., Wang, S., Xiao, J., Wang, Y., & Su, H. (2021) · Journal of Functional Foods · doi:10.1016/j.jff.2021.104463 · Cited by 31 · see citing works
The holobiont mind: A bridge between 4E-cognition and the microbiome
Palacios-Garcia, I., & Parada, F. J. (2021) · doi:10.31234/osf.io/thuvc · Cited by 21 · see citing works
- Authors
- Paul, B., Barnes, S., Demark-Wahnefried, W., Morrow, C., Salvador, C., Skibola, C., & Tollefsbol, T. O.
- Affiliations
- University of Alabama at Birmingham (US)
- Corresponding author
- Tollefsbol, Trygve O.
- Venue
- Clinical Epigenetics
- Published
- 2015-10-16
- Volume
- 7
- Issue
- 1
- Pages
- 112-112
- ISSN
- 1868-7075 (ISSN-L)
- 1868-7083
- PMC
- PMC4609101
- OpenAlex
- W2115908082
- Cited by
- 306
- References
- 100
- Citations by year
- 2026: 15 · 2025: 19 · 2024: 23 · 2023: 26 · 2022: 26 · 2021: 33 · 2020: 48 · 2019: 39 · 2018: 28 · 2017: 27 · 2016: 19 · 2015: 1
- FWCI
- 2.42
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Clinical Epigenetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (R01 CA178441)
- American Institute for Cancer Research (316184)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Nutrition, Genetics, and Disease
- Keywords
- gut microbiota, diet, epigenetic modulation, cancer, microbiota metabolites, DNA methylation, histone modifications, tumor response, cancer prevention, metabolomics, gene expression regulation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
