Abstract
Cellular information is inherited by daughter cells through epigenetic routes in addition to genetic routes. Epigenetics, which is primarily mediated by inheritable DNA methylation and histone post-translational modifications, involves changes in the chromatin structure important for regulating gene expression. It is widely known that epigenetic control of gene expression plays an essential role in cell differentiation processes in vertebrates. Furthermore, because epigenetic changes can occur reversibly depending on environmental factors in differentiated cells, they have recently attracted considerable attention as targets for disease prevention and treatment. These environmental factors include diet, exposure to bacteria or viruses, and air pollution, of which this review focuses on the influence of bacteria on epigenetic gene control in a host. Host-bacterial interactions not only occur upon pathogenic bacterial infection but also continuously exist between commensal bacteria and the host. These bacterial stimuli play an essential role in various biological responses involving external stimuli and in maintaining physiological homeostasis by altering epigenetic markers and machinery.
Similar content being viewed by others
References
Robertson KD, Wolffe AP (2000) DNA methylation in health and disease. Nat Rev Genet 1:11–19
Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349:2042–2054
Unoki M, Masuda A, Dohmae N, Arita K, Yoshimatsu M, Iwai Y, Fukui Y, Ueda K, Hamamoto R, Shirakawa M, Sasaki H, Nakamura Y (2013) Lysyl 5-hydroxylation, a novel histone modification, by Jumonji domain containing 6 (JMJD6). J Biol Chem 288:6053–6062
Anderson OS, Sant KE, Dolinoy DC (2012) Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 23:853–859
Ghoshal K, Li X, Datta J, Bai S, Pogribny I, Pogribny M, Huang Y, Young D, Jacob ST (2006) A folate- and methyl-deficient diet alters the expression of DNA methyltransferases and methyl CpG binding proteins involved in epigenetic gene silencing in livers of F344 rats. J Nutr 136:1522–1527
Stefanska B, Salamé P, Bednarek A, Fabianowska-Majewska K (2012) Comparative effects of retinoic acid, vitamin D and resveratrol alone and in combination with adenosine analogues on methylation and expression of phosphatase and tensin homologue tumour suppressor gene in breast cancer cells. Br J Nutr 107:781–790
Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF (1997) Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277:1996–2000
Bigey P, Ramchandani S, Theberge J, Araujo FD, Szyf M (2000) Transcriptional regulation of the human DNA methyltransferase (dnmt1) gene. Gene 242:407–418
Yang CS, Fang M, Lambert JD, Yan P, Huang TH (2008) Reversal of hypermethylation and reactivation of genes by dietary polyphenolic compounds. Nutr Rev 66(Suppl 1):S18–S20
Dashwood RH, Ho E (2007) Dietary histone deacetylase inhibitors: from cells to mice to man. Semin Cancer Biol 17:363–369
Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT (2009) Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 4:e7845
Waterland RA, Jirtle RL (2004) Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20:63–68
Kovacheva VP, Mellott TJ, Davison JM, Wagner N, Lopez-Coviella I, Schnitzler AC, Blusztajn JK (2007) Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J Biol Chem 282:31777–31788
Waterland RA, Lin JR, Smith CA, Jirtle RL (2006) Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet 15:705–716
Ollikainen M, Smith KR, Joo EJ, Ng HK, Andronikos R, Novakovic B, Abdul Aziz NK, Carlin JB, Morley R, Saffery R, Craig JM (2010) DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet 19:4176–4188
Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J (2010) A longitudinal study of epigenetic variation in twins. Epigenetics 5:516–526
Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73
Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 104:19351–19356
Hollingsworth JW, Maruoka S, Boon K, Garantziotis S, Li Z, Tomfohr J, Bailey N, Potts EN, Whitehead G, Brass DM, Schwartz DA (2008) In utero supplementation with methyl donors enhances allergic airway disease in mice. J Clin Invest 118:3462–3469
Schaub B, Liu J, Höppler S, Schleich I, Huehn J, Olek S, Wieczorek G, Illi S, von Mutius E (2009) Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J Allergy Clin Immunol 123:774–782
Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz J (2009) Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 179:572–578
Perera F, Tang WY, Herbstman J, Tang D, Levin L, Miller R, Ho SM (2009) Relation of DNA methylation of 5′-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS One 4:e4488
Singh NP, Singh UP, Singh B, Price RL, Nagarkatti M, Nagarkatti PS (2011) Activation of aryl hydrocarbon receptor (AhR) leads to reciprocal epigenetic regulation of FoxP3 and IL-17 expression and amelioration of experimental colitis. PLoS One 6:e23522
Takamura T, Harama D, Matsuoka S, Shimokawa N, Nakamura Y, Okumura K, Ogawa H, Kitamura M, Nakao A (2010) Activation of the aryl hydrocarbon receptor pathway may ameliorate dextran sodium sulfate-induced colitis in mice. Immunol Cell Biol 88:685–689
Lebreton A, Lakisic G, Job V, Fritsch L, Tham TN, Camejo A, Matteï PJ, Regnault B, Nahori MA, Cabanes D, Gautreau A, Ait-Si-Ali S, Dessen A, Cossart P, Bierne H (2011) A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response. Science 331:1319–1321
Pennini ME, Perrinet S, Dautry-Varsat A, Subtil A (2010) Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog 6:e1000995
Rolando M, Sanulli S, Rusniok C, Gomez-Valero L, Bertholet C, Sahr T, Margueron R, Buchrieser C (2013) Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 13:395–405
Park J, Kim KJ, Choi KS, Grab DJ, Dumler JS (2004) Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol 6:743–751
Zhu B, Nethery KA, Kuriakose JA, Wakeel A, Zhang X, McBride JW (2009) Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infect Immun 77:4243–4455
Bierne H, Cossart P (2012) When bacteria target the nucleus: the emerging family of nucleomodulins. Cell Microbiol 14:622–633
Yamamoto Y, Verma UN, Prajapati S, Kwak YT, Gaynor RB (2003) Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423:655–659
Baek SH (2011) When signaling kinases meet histones and histone modifiers in the nucleus. Mol Cell 42:274–284
Schmeck B, Beermann W, van Laak V, Zahlten J, Opitz B, Witzenrath M, Hocke AC, Chakraborty T, Kracht M, Rosseau S, Suttorp N, Hippenstiel S (2005) Intracellular bacteria differentially regulated endothelial cytokine release by MAPK-dependent histone modification. J Immunol 175:2843–2850
Opitz B, Püschel A, Beermann W, Hocke AC, Förster S, Schmeck B, van Laak V, Chakraborty T, Suttorp N, Hippenstiel S (2006) Listeria monocytogenes activated p38 MAPK and induced IL-8 secretion in a nucleotide-binding oligomerization domain 1-dependent manner in endothelial cells. J Immunol 176:484–490
Hamon MA, Cossart P (2011) K+ efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins. Infect Immun 79:2839–2846
Saccani S, Pantano S, Natoli G (2002) p38-Dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat Immunol 3:69–75
Schmeck B, Lorenz J, N’guessan PD, Opitz B, van Laak V, Zahlten J, Slevogt H, Witzenrath M, Flieger A, Suttorp N, Hippenstiel S (2008) Histone acetylation and flagellin are essential for Legionella pneumophila-induced cytokine expression. J Immunol 181:940–947
Ding SZ, Goldberg JB, Hatakeyama M (2010) Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future Oncol 6:851–862
Ushijima T, Hattori N (2012) Molecular pathways: involvement of Helicobacter pylori-triggered inflammation in the formation of an epigenetic field defect, and its usefulness as cancer risk and exposure markers. Clin Cancer Res 18:923–929
Nakajima T, Enomoto S, Yamashita S, Ando T, Nakanishi Y, Nakazawa K, Oda I, Gotoda T, Ushijima T (2010) Persistence of a component of DNA methylation in gastric mucosae after Helicobacter pylori eradication. J Gastroenterol 45:37–44
Tolg C, Sabha N, Cortese R, Panchal T, Ahsan A, Soliman A, Aitken KJ, Petronis A, Bägli DJ (2011) Uropathogenic E. coli infection provokes epigenetic downregulation of CDKN2A (p16INK4A) in uroepithelial cells. Lab Invest 91:825–836
Haller D, Holt L, Kim SC, Schwabe RF, Sartor RB, Jobin C (2003) Transforming growth factor-beta 1 inhibits non-pathogenic Gram negative bacteria-induced NF-kappa B recruitment to the interleukin-6 gene promoter in intestinal epithelial cells through modulation of histone acetylation. J Biol Chem 278:23851–23860
Slevogt H, Schmeck B, Jonatat C, Zahlten J, Beermann W, van Laak V, Opitz B, Dietel S, N’Guessan PD, Hippenstiel S, Suttorp N, Seybold J (2006) Moraxella catarrhalis induces inflammatory response of bronchial epithelial cells via MAPK and NF-kappaB activation and histone deacetylase activity reduction. Am J Physiol Lung Cell Mol Physiol 290:L818–L826
Negri I, Franchini A, Gonella E, Daffonchio D, Mazzoglio PJ, Mandrioli M, Alma A (2009) Unravelling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting. Proc Biol Sci 276:2485–2491
Ghadimi D, Helwig U, Schrezenmeir J, Heller KJ, de Vrese M (2012) Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. J Leukoc Biol 92:895–911
Acharya MR, Sparreboom A, Venitz J, Figg WD (2005) Rational development of histone deacetylase inhibitors as anticancer agents: a review. Mol Pharmacol 68:917–932
Marks PA, Richon VM, Miller T, Kelly WK (2004) Histone deacetylase inhibitors. Adv Cancer Res 91:137–168
Davie JR (2003) Inhibition of histone deacetylase activity by butyrate. J Nutr 133:2485S–2493S
Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15:1183–1189
Gill RK, Kumar A, Malhotra P, Maher D, Singh V, Dudeja PK, Alrefai W, Saksena S (2013) Regulation of intestinal serotonin transporter expression via epigenetic mechanisms: role of HDAC2. Am J Physiol Cell Physiol 304:C334–C341
Perona M, Rodríguez C, Carpano M, Thomasz L, Nievas S, Olivera M, Thorp S, Curotto P, Pozzi E, Kahl S, Pisarev M, Juvenal G, Dagrosa A (2013) Improvement of the boron neutron capture therapy (BNCT) by the previous administration of the histone deacetylase inhibitor sodium butyrate for the treatment of thyroid carcinoma. Radiat Environ Biophys 52:363–373
St Laurent R, O’Brien LM, Ahmad ST (2013) Sodium butyrate improves locomotor impairment and early mortality in a rotenone-induced Drosophila model of Parkinson’s disease. Neuroscience 246:382–390
Imai K, Yamada K, Tamura M, Ochiai K, Okamoto T (2012) Reactivation of latent HIV-1 by a wide variety of butyric acid-producing bacteria. Cell Mol Life Sci 69:2583–2592
Imai K, Ochiai K, Okamoto T (2009) Reactivation of latent HIV-1 infection by the periodontopathic bacterium Porphyromonas gingivalis involves histone modification. J Immunol 182:3688–3695
Takahashi K, Sugi Y, Hosono A, Kaminogawa S (2009) Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J Immunol 183:6522–6529
Takahashi K, Sugi Y, Nakano K, Tsuda M, Kurihara K, Hosono A, Kaminogawa S (2011) Epigenetic control of the host gene by commensal bacteria in large intestinal epithelial cells. J Biol Chem 286:35755–35762
Kellermayer R, Dowd SE, Harris RA, Balasa A, Schaible TD, Wolcott RD, Tatevian N, Szigeti R, Li Z, Versalovic J, Smith CW (2011) Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice. FASEB J 25:1449–1460
Choi KC, Jung MG, Lee YH, Yoon JC, Kwon SH, Kang HB, Kim MJ, Cha JH, Kim YJ, Jun WJ, Lee JM, Yoon HG (2009) Epigallocatechin-3-gallate, a histone acetyltransferase inhibitor, inhibits EBV-induced B lymphocyte transformation via suppression of RelA acetylation. Cancer Res 69:583–592
Ding SZ, Fischer W, Kaparakis-Liaskos M, Liechti G, Merrell DS, Grant PA, Ferrero RL, Crowe SE, Haas R, Hatakeyama M, Goldberg JB (2010) Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One 5:e9875
Fehri LF, Rechner C, Janssen S, Mak TN, Holland C, Bartfeld S, Brüggemann H, Meyer TF (2009) Helicobacter pylori-induced modification of the histone H3 phosphorylation status in gastric epithelial cells reflects its impact on cell cycle regulation. Epigenetics 4:577–586
Li N, Tang B, Zhu ED, Li BS, Zhuang Y, Yu S, Lu DS, Zou QM, Xiao B, Mao XH (2012) Increased miR-222 in H. pylori-associated gastric cancer correlated with tumor progression by promoting cancer cell proliferation and targeting RECK. FEBS Lett 586:722–728
Zhu Y, Jiang Q, Lou X, Ji X, Wen Z, Wu J, Tao H, Jiang T, He W, Wang C, Du Q, Zheng S, Mao J, Huang J (2012) MicroRNAs up-regulated by CagA of Helicobacter pylori induce intestinal metaplasia of gastric epithelial cells. PLoS One 7:e35147
Belair C, Baud J, Chabas S, Sharma CM, Vogel J, Staedel C, Darfeuille F (2011) Helicobacter pylori interferes with an embryonic stem cell micro RNA cluster to block cell cycle progression. Silence 2:7
Marazzi I, Ho JS, Kim J, Manicassamy B, Dewell S, Albrecht RA, Seibert CW, Schaefer U, Jeffrey KL, Prinjha RK, Lee K, García-Sastre A, Roeder RG, Tarakhovsky A (2012) Suppression of the antiviral response by an influenza histone mimic. Nature 483:428–433
Tsai CN, Tsai CL, Tse KP, Chang HY, Chang YS (2002) The Epstein–Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc Natl Acad Sci USA 99:10084–10089
Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL, Tsao SW, Tse KP, Yu JS, Chang YS (2006) Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer Res 66:11668–11676
McCabe MT, Low JA, Imperiale MJ, Day ML (2006) Human polyomavirus BKV transcriptionally activates DNA methyltransferase 1 through the pRb/E2F pathway. Oncogene 25:2727–2735
Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F (2007) Viral oncoproteins target the DNA methyltransferases. Oncogene 26:1650–1655
Jung JK, Arora P, Pagano JS, Jang KL (2007) Expression of DNA methyltransferase 1 is activated by hepatitis B virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway. Cancer Res 67:5771–5778
Wang WH, Hullinger RL, Andrisani OM (2008) Hepatitis B virus X protein via the p38MAPK pathway induces E2F1 release and ATR kinase activation mediating p53 apoptosis. J Biol Chem 283:25455–25467
Mikovits JA, Young HA, Vertino P, Issa JP, Pitha PM, Turcoski-Corrales S, Taub DD, Petrow CL, Baylin SB, Ruscetti FW (1998) Infection with human immunodeficiency virus type 1 upregulates DNA methyltransferase, resulting in de novo methylation of the gamma interferon (IFN-gamma) promoter and subsequent downregulation of IFN-gamma production. Mol Cell Biol 18:5166–5177
Fang JY, Mikovits JA, Bagni R, Petrow-Sadowski CL, Ruscetti FW (2001) Infection of lymphoid cells by integration-defective human immunodeficiency virus type 1 increases de novo methylation. J Viol 75:9753–9761
Acknowledgments
I thank Dr. Shuichi Kaminogawa for helpful discussion and kind encouragement and Dr. Yutaka Sugi for figure preparation. This work was supported in part by JSPS KAKENHI Grant Number 23580186.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Takahashi, K. Influence of bacteria on epigenetic gene control. Cell. Mol. Life Sci. 71, 1045–1054 (2014). https://doi.org/10.1007/s00018-013-1487-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-013-1487-x