Advertisement

Diet-Induced Epigenetic Modifications and Implications for Intestinal Diseases

  • Elodie Gimier
  • Nicolas Barnich
  • Jérémy DenizotEmail author
Reference work entry

Abstract

Epigenetic modifications, such as post-translational modifications of histones, DNA methylation, and microRNA expression, are involved in gene transcription changes in the cells in response to environmental signals. It is now clear that particular phenotypes are the consequences of environmental effects on epigenetic marks. In this chapter, we describe the interactions existing between environment and epigenetic marks. Among the environmental factors, we’ll specially focus on diet, through different examples such as the effect of diet on bee cast formation, on microbiota composition and short-chain fatty acid concentration in the gut, and the consequences on epigenetic marks. Finally, we describe the link that exists between diet and epigenetic modifications in the context of inflammatory bowel disease (IBD). So far, epigenetic marks have been poorly investigated in the context of IBD, but it has recently become an expanding field of research since new data raise crucial role for epigenetic modifications in the etiology of IBD.

Keywords

DNA methylation DNMT3A Microbiota Inflammatory bowel disease Folate Short-chain fatty acids Butyrate Dysbiosis Crohn’s disease Nutrition GPR43 

List of Abbreviations

BPA

Bisphenol A

CD

Crohn’s Disease

DNMT

DNA-Methyltransferase

DSS

Dextran Sodium Sulfate

EWAS

Epigenome Wide Association Study

GPR43

G-protein Coupled Receptors 43

HC

Healthy Controls

HDAC

Histone Deacetylase

HFD

High-Fat Diet

HPTM

Histone Post-Translational Modification

IAP

Intracisternal A Particle

IBD

Inflammatory Bowel Disease

IEC

Intestinal Epithelial Cells

KAT2B

Lysine Acetyltransferase 2B

SCFA

Short-Chain Fatty Acid

SNP

Single-Nucleotide Polymorphism

UC

Ulcerative Colitis

References

  1. Agus A, Denizot J, Thévenot J, Martinez-Medina M, Massier S, Sauvanet P, Bernalier-Donadille A, Denis S, Hofman P, Bonnet R et al (2016) Western diet induces a shift in microbiota composition enhancing susceptibility to adherent-invasive E. coli infection and intestinal inflammation. Sci Rep 6:19032CrossRefGoogle Scholar
  2. Bai AHC, Wu WKK, Xu L, Wong SH, Go MY, Chan AWH, Harbord M, Zhang S, Chen M, Wu JCY et al (2016) Dysregulated lysine acetyltransferase 2B promotes inflammatory bowel disease pathogenesis through transcriptional repression of interleukin-10. J Crohns Colitis 10:726–734CrossRefGoogle Scholar
  3. Bernstein CN, Shanahan F (2008) Disorders of a modern lifestyle: reconciling the epidemiology of inflammatory bowel diseases. Gut 57:1185–1191CrossRefGoogle Scholar
  4. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, Gewirtz AT (2016) Corrigendum: dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 536:238CrossRefGoogle Scholar
  5. Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, Feng G, Peng H, Zhang X, Zhang Y et al (2016) Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351:397–400CrossRefGoogle Scholar
  6. Cooke J, Zhang H, Greger L, Silva A-L, Massey D, Dawson C, Metz A, Ibrahim A, Parkes M (2012) Mucosal genome-wide methylation changes in inflammatory bowel disease. Inflamm Bowel Dis 18:2128–2137CrossRefGoogle Scholar
  7. Cooney CA, Dave AA, Wolff GL (2002) Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 132:2393S–2400SCrossRefGoogle Scholar
  8. Denizot J, Desrichard A, Agus A, Uhrhammer N, Dreux N, Vouret-Craviari V, Hofman P, Darfeuille-Michaud A, Barnich N (2015) Diet-induced hypoxia responsive element demethylation increases CEACAM6 expression, favouring Crohn’s disease-associated Escherichia coli colonisation. Gut 64:428–437Google Scholar
  9. Dolinoy DC (2008) The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr Rev 66(Suppl 1):S7–S11CrossRefGoogle Scholar
  10. Dolinoy DC, Huang D, Jirtle RL (2007) Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A 104:13056–13061CrossRefGoogle Scholar
  11. Franke A, McGovern DPB, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Lees CW, Balschun T, Lee J, Roberts R et al (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn’s disease susceptibility loci. Nat Genet 42:1118–1125CrossRefGoogle Scholar
  12. Glauben R, Batra A, Fedke I, Zeitz M, Lehr HA, Leoni F, Mascagni P, Fantuzzi G, Dinarello CA, Siegmund B (2006) Histone hyperacetylation is associated with amelioration of experimental colitis in mice. J Immunol 176:5015–5022CrossRefGoogle Scholar
  13. Harris RA, Shah R, Hollister EB, Tronstad RR, Hovdenak N, Szigeti R, Versalovic J, Kellermayer R (2016) Colonic mucosal epigenome and microbiome development in children and adolescents. J Immunol Res 2016:9170162CrossRefGoogle Scholar
  14. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132:1012–1017CrossRefGoogle Scholar
  15. Keyes MK, Jang H, Mason JB, Liu Z, Crott JW, Smith DE, Friso S, Choi S-W (2007) Older age and dietary folate are determinants of genomic and p16-specific DNA methylation in mouse colon. J Nutr 137:1713–1717CrossRefGoogle Scholar
  16. Krautkramer KA, Kreznar JH, Romano KA, Vivas EI, Barrett-Wilt GA, Rabaglia ME, Keller MP, Attie AD, Rey FE, Denu JM (2016) Diet-microbiota interactions mediate global epigenetic programming in multiple host tissues. Mol Cell 64:982–992CrossRefGoogle Scholar
  17. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–1830CrossRefGoogle Scholar
  18. Lee H-S (2015) Impact of maternal diet on the epigenome during in utero life and the developmental programming of diseases in childhood and adulthood. Nutrients 7:9492–9507CrossRefGoogle Scholar
  19. Li C-J, Li RW, Baldwin RL, Blomberg LA, Wu S, Li W (2016) Transcriptomic sequencing reveals a set of unique genes activated by butyrate-induced histone modification. Gene Regul Syst Biol 10:1–8Google Scholar
  20. Lin Z, Hegarty JP, Cappel JA, Yu W, Chen X, Faber P, Wang Y, Kelly AA, Poritz LS, Peterson BZ et al (2011) Identification of disease-associated DNA methylation in intestinal tissues from patients with inflammatory bowel disease. Clin Genet 80:59–67CrossRefGoogle Scholar
  21. Lin Z, Hegarty JP, Yu W, Cappel JA, Chen X, Faber PW, Wang Y, Poritz LS, Fan J-B, Koltun WA (2012) Identification of disease-associated DNA methylation in B cells from Crohn’s disease and ulcerative colitis patients. Dig Dis Sci 57:3145–3153CrossRefGoogle Scholar
  22. Louis P, Young P, Holtrop G, Flint HJ (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: acetate CoA-transferase gene. Environ Microbiol 12:304–314CrossRefGoogle Scholar
  23. Macfarlane S, Macfarlane GT (2003) Regulation of short-chain fatty acid production. Proc Nutr Soc 62:67–72CrossRefGoogle Scholar
  24. Mao W, Schuler MA, Berenbaum MR (2015) A dietary phytochemical alters caste-associated gene expression in honey bees. Sci Adv 1:e1500795CrossRefGoogle Scholar
  25. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D et al (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461:1282–1286CrossRefGoogle Scholar
  26. Nimmo ER, Prendergast JG, Aldhous MC, Kennedy NA, Henderson P, Drummond HE, Ramsahoye BH, Wilson DC, Semple CA, Satsangi J (2012) Genome-wide methylation profiling in Crohn’s disease identifies altered epigenetic regulation of key host defense mechanisms including the Th17 pathway. Inflamm Bowel Dis 18:889–899CrossRefGoogle Scholar
  27. Pinsk V, Lemberg DA, Grewal K, Barker CC, Schreiber RA, Jacobson K (2007) Inflammatory bowel disease in the South Asian pediatric population of British Columbia. Am J Gastroenterol 102:1077–1083CrossRefGoogle Scholar
  28. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65CrossRefGoogle Scholar
  29. Quévrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermúdez-Humarán LG, Pigneur B et al (2016) Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut 65:415–425CrossRefGoogle Scholar
  30. Reynolds CM, Gray C, Li M, Segovia SA, Vickers MH (2015) Early life nutrition and energy balance disorders in offspring in later life. Nutrients 7:8090–8111CrossRefGoogle Scholar
  31. Rogler G, Zeitz J, Biedermann L (2016) The search for causative environmental factors in inflammatory bowel disease. Dig Dis Basel Switz 34(Suppl 1):48–55CrossRefGoogle Scholar
  32. Rossi O, van Berkel LA, Chain F, Tanweer Khan M, Taverne N, Sokol H, Duncan SH, Flint HJ, Harmsen HJM, Langella P et al (2016) Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep 6:18507CrossRefGoogle Scholar
  33. Saito S, Kato J, Hiraoka S, Horii J, Suzuki H, Higashi R, Kaji E, Kondo Y, Yamamoto K (2011) DNA methylation of colon mucosa in ulcerative colitis patients: correlation with inflammatory status. Inflamm Bowel Dis 17:1955–1965CrossRefGoogle Scholar
  34. Schaible TD, Harris RA, Dowd SE, Smith CW, Kellermayer R (2011) Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 20:1687–1696CrossRefGoogle Scholar
  35. Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533CrossRefGoogle Scholar
  36. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F et al (2016) Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351:391–396CrossRefGoogle Scholar
  37. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, Blugeon S, Bridonneau C, Furet J-P, Corthier G et al (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 105:16731–16736CrossRefGoogle Scholar
  38. Sun M, Wu W, Liu Z, Cong Y (2017) Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J Gastroenterol 52:1–8CrossRefGoogle Scholar
  39. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249CrossRefGoogle Scholar
  40. Tsaprouni LG, Ito K, Powell JJ, Adcock IM, Punchard N (2011) Differential patterns of histone acetylation in inflammatory bowel diseases. J Inflamm Lond Engl 8:1CrossRefGoogle Scholar
  41. Tschurtschenthaler M, Kachroo P, Heinsen F-A, Adolph TE, Rühlemann MC, Klughammer J, Offner FA, Ammerpohl O, Krueger F, Smallwood S et al (2016) Paternal chronic colitis causes epigenetic inheritance of susceptibility to colitis. Sci Rep 6:31640CrossRefGoogle Scholar
  42. Waldecker M, Kautenburger T, Daumann H, Busch C, Schrenk D (2008) Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 19:587–593CrossRefGoogle Scholar
  43. Zhu K, Liu M, Fu Z, Zhou Z, Kong Y, Liang H, Lin Z, Luo J, Zheng H, Wan P et al (2017) Plant microRNAs in larval food regulate honeybee caste development. PLoS Genet 13:e1006946CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Elodie Gimier
    • 1
  • Nicolas Barnich
    • 1
  • Jérémy Denizot
    • 1
    Email author
  1. 1.M2iSHUniversité Clermont Auvergne, Inserm U1071, USC-INRA 2018Clermont-FerrandFrance

Personalised recommendations