Abstract
Multidisciplinary approaches combining microbiology, cell biology, and genetics have improved our understanding of bacterial diseases by elucidating mechanisms employed by bacteria to manipulate eukaryotic cellular processes. In parallel, research on epigenetics has increased our knowledge about eukaryotic gene expression by providing a mechanistic basis for the amazing plasticity of the genome in response to developmental and environmental cues. These two fields of research have now converged, providing information about the ways in which bacteria shape the epigenome and the mechanisms by which the epigenetic machinery allows the host to respond to colonization by pathogenic or commensal bacteria. The study of this cross talk has revealed remarkable diversity in the mechanisms of action of bacteria on chromatin and has identified epigenetic regulators involved in host responsiveness to bacteria. One powerful strategy used by intracellular pathogens (e.g., Anaplasma, Chlamydia, Ehrlichia, Legionella, Listeria, Mycobacteria, Mycoplasma, Shigella) is the secretion of nucleomodulins that manipulate chromatin structure in the host nucleus. The effects of this dialog are often limited in time, causing transient gene expression changes. However, increasing evidence suggests that certain epigenetic changes triggered by bacterial molecules are long-lasting, leading to the priming of transcriptional responses and the reprogramming of genes involved in inflammation or tolerance, with consequences for reinfection and polymicrobial infections. In addition, the effects of bacteria on the host epigenome may ultimately modify the identity of the cell by breaking epigenetic barriers, leading to cell differentiation, dedifferentiation, or trans-differentiation, thereby potentially contributing to tissue remodeling and emergence of complex diseases.
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References
Agarwal S, Agarwal S, Jin H, Pancholi P, Pancholi V (2012) Serine/threonine phosphatase (SP-STP), secreted from Streptococcus pyogenes, is a pro-apoptotic protein. J Biol Chem 287(12):9147–9167. doi:10.1074/jbc.M111.316554
Aguilera C, Nakagawa K, Sancho R, Chakraborty A, Hendrich B, Behrens A (2011) c-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complex. Nature 469 (7329):231–235. doi:10.1038/nature09607
Alenghat T, Artis D (2014) Epigenomic regulation of host-microbiota interactions. Trends in immunology 35(11):518–525. doi:10.1016/j.it.2014.09.007
Alenghat T, Osborne LC, Saenz SA, Kobuley D, Ziegler CG, Mullican SE, Choi I, Grunberg S, Sinha R, Wynosky-Dolfi M, Snyder A, Giacomin PR, Joyce KL, Hoang TB, Bewtra M, Brodsky IE, Sonnenberg GF, Bushman FD, Won KJ, Lazar MA, Artis D (2013) Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 504(7478):153–157. doi:10.1038/nature12687
Allemand E, Batsche E, Muchardt C (2008) Splicing, transcription, and chromatin: a menage a trois. Curr Opin Genet Dev 18(2):145–151. doi:10.1016/j.gde.2008.01.006
Alvarez-Errico D, Vento-Tormo R, Sieweke M, Ballestar E (2015) Epigenetic control of myeloid cell differentiation, identity and function. Nat Rev Immunol 15(1):7–17. doi:10.1038/nri3777
Ando T, Yoshida T, Enomoto S, Asada K, Tatematsu M, Ichinose M, Sugiyama T, Ushijima T (2009) DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect. Int J Cancer 124(10):2367–2374. doi:10.1002/ijc.24219
Arbibe L, Kim DW, Batsche E, Pedron T, Mateescu B, Muchardt C, Parsot C, Sansonetti PJ (2007) An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat Immunol 8(1):47–56. doi:10.1038/ni1423
Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504(7480):451–455. doi:10.1038/nature12726
Arts RJ, Blok BA, van Crevel R, Joosten LA, Aaby P, Benn CS, Netea MG (2015) Vitamin A induces inhibitory histone methylation modifications and down-regulates trained immunity in human monocytes. J Leukoc Biol 98(1):129–136. doi:10.1189/jlb.6AB0914-416R
Arzate-Mejia RG, Valle-Garcia D, Recillas-Targa F (2011) Signaling epigenetics: novel insights on cell signaling and epigenetic regulation. IUBMB Life 63(10):881–895. doi:10.1002/iub.557
Baek SH (2011) When signaling kinases meet histones and histone modifiers in the nucleus. Mol Cell 42(3):274–284. doi:10.1016/j.molcel.2011.03.022
Bandyopadhaya A, Tsurumi A, Maura D, Jeffrey KL, Rahme LG (2016) A quorum-sensing signal promotes host tolerance training through HDAC1-mediated epigenetic reprogramming. Nat Microbiol 1:16174. doi:10.1371/journal.ppat.1003024
Bardwell AJ, Abdollahi M, Bardwell L (2004) Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem J 378(Pt 2):569–577. doi:10.1042/BJ20031382
Bayarsaihan D (2011) Epigenetic mechanisms in inflammation. J Dent Res 90(1):9–17. doi:10.1177/0022034510378683
Benabdillah R, Ls JM, Lützelschwab S, Demoinet E, Cornelis GR (2004) Identification of a nuclear targeting signal in YopM from Yersinia spp. Microbial pathogenesis 36(5):247–261. doi:10.1016/j.micpath.2003.12.006
Berneking L, Schnapp M, Rumm A, Trasak C, Ruckdeschel K, Alawi M, Grundhoff A, Kikhney AG, Koch-Nolte F, Buck F, Perbandt M, Betzel C, Svergun DI, Hentschke M, Aepfelbacher M (2016) Immunosuppressive Yersinia effector YopM binds DEAD box helicase DDX3 to control ribosomal S6 kinase in the nucleus of host cells. PLoS Pathog 12(6):e1005660. doi:10.1371/journal.ppat.1005660
Bessede E, Staedel C, Acuna Amador LA, Nguyen PH, Chambonnier L, Hatakeyama M, Belleannee G, Megraud F, Varon C (2014) Helicobacter pylori generates cells with cancer stem cell properties via epithelial-mesenchymal transition-like changes. Oncogene 33(32):4123–4131. doi:10.1038/onc.2013.380
Bhavsar AP, Guttman JA, Finlay BB (2007) Manipulation of host-cell pathways by bacterial pathogens. Nature 449(7164):827–834. doi:10.1038/nature06247
Bhutani N, Burns DM, Blau HM (2011) DNA demethylation dynamics. Cell 146(6):866–872. doi:10.1016/j.cell.2011.08.042
Bierne H (2013) Nuclear microbiology—bacterial assault on the nucleolus. EMBO Rep 14(8):663–664. doi:10.1038/embor.2013.105
Bierne H, Cossart P (2012) When bacteria target the nucleus: the emerging family of nucleomodulins. Cell Microbiol. doi:10.1111/j.1462-5822.2012.01758.x
Bierne H, Hamon M, Cossart P (2012) Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2(12):a010272. doi:10.1101/cshperspect.a010272
Bierne H, Tham TN, Batsche E, Dumay A, Leguillou M, Kerneis-Golsteyn S, Regnault B, Seeler JS, Muchardt C, Feunteun J, Cossart P (2009) Human BAHD1 promotes heterochromatic gene silencing. Proc Natl Acad Sci U S A 106(33):13826–13831. doi:10.1073/pnas.0901259106
Bird A (2007) Perceptions of epigenetics. Nature 447(7143):396–398. doi:10.1038/nature05913
Bobetsis YA, Barros SP, Lin DM, Weidman JR, Dolinoy DC, Jirtle RL, Boggess KA, Beck JD, Offenbacher S (2007) Bacterial infection promotes DNA hypermethylation. J Dent Res 86(2):169–174. doi:10.1177/154405910708600212
Borjesson DL, Kobayashi SD, Whitney AR, Voyich JM, Argue CM, Deleo FR (2005) Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J Immunol 174(10):6364–6372
Brennan DF, Barford D (2009) Eliminylation: a post-translational modification catalyzed by phosphothreonine lyases. Trends Biochem Sci 34(3):108–114. doi:10.1016/j.tibs.2008.11.005
Brestoff JR, Artis D (2013) Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14(7):676–684. doi:10.1038/ni.2640
Buck-Koehntop BA, Defossez PA (2013) On how mammalian transcription factors recognize methylated DNA. Epigenetics 8(2):131–137. doi:10.4161/epi.23632
Bussiere FI, Michel V, Memet S, Ave P, Vivas JR, Huerre M, Touati E (2010) H. pylori-induced promoter hypermethylation downregulates USF1 and USF2 transcription factor gene expression. Cell Microbiol 12(8):1124–1133. doi:10.1111/j.1462-5822.2010.01457.x
Cai Y, Geutjes EJ, de Lint K, Roepman P, Bruurs L, Yu LR, Wang W, van Blijswijk J, Mohammad H, de Rink I, Bernards R, Baylin SB (2014) The NuRD complex cooperates with DNMTs to maintain silencing of key colorectal tumor suppressor genes. Oncogene 33(17):2157–2168. doi:10.1038/Onc.2013.178
Canonne J, Rivas S (2012) Bacterial effectors target the plant cell nucleus to subvert host transcription. Plant Signal Behav 7(2):217–221. doi:10.4161/psb.18885
Cao J (2014) The functional role of long non-coding RNAs and epigenetics. Biol Proced Online 16:11. doi:10.1186/1480-9222-16-11
Carson WF, Cavassani KA, Dou Y, Kunkel SL (2011) Epigenetic regulation of immune cell functions during post-septic immunosuppression. Epigenetics 6(3):273–283
Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nature Rev Genetics 10(5):295–304. doi:10.1038/nrg2540
Chan AO, Lam SK, Wong BC, Wong WM, Yuen MF, Yeung YH, Hui WM, Rashid A, Kwong YL (2003) Promoter methylation of E-cadherin gene in gastric mucosa associated with Helicobacter pylori infection and in gastric cancer. Gut 52(4):502–506
Chandran A, Antony C, Jose L, Mundayoor S, Natarajan K, Kumar RA (2015) Mycobacterium tuberculosis infection induces HDAC1-mediated suppression of IL-12B gene expression in macrophages. Front Cell Infect Microbiol 5:90. doi:10.3389/fcimb.2015.00090
Chang PV, Hao L, Offermanns S, Medzhitov R (2014) The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A 111(6):2247–2252. doi:10.1073/pnas.1322269111
Chen ZX, Riggs AD (2011) DNA methylation and demethylation in mammals. J Biol Chem 286(21):18347–18353. doi:10.1074/jbc.R110.205286
Chen X, Yoza BK, El Gazzar M, Hu JY, Cousart SL, McCall CE (2009) RelB sustains IkappaBalpha expression during endotoxin tolerance. Clin Vaccine Immunol 16(1):104–110. doi:10.1128/CVI.00320-08
Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, Giamarellos-Bourboulis EJ, Martens JH, Rao NA, Aghajanirefah A, Manjeri GR, Li Y, Ifrim DC, Arts RJ, van der Veer BM, Deen PM, Logie C, O’Neill LA, Willems P, van de Veerdonk FL, van der Meer JW, Ng A, Joosten LA, Wijmenga C, Stunnenberg HG, Xavier RJ, Netea MG (2014) mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345(6204):1250684. doi:10.1126/science.1250684
Chernov AV, Reyes L, Xu Z, Gonzalez B, Golovko G, Peterson S, Perucho M, Fofanov Y, Strongin AY (2015) Mycoplasma CG- and GATC-specific DNA methyltransferases selectively and efficiently methylate the host genome and alter the epigenetic landscape in human cells. Epigenetics 10(4):303–318. doi:10.1080/15592294.2015.1020000
Cuddapah S, Barski A, Zhao K (2010) Epigenomics of T cell activation, differentiation, and memory. Curr Opin Immunol 22(3):341–347. doi:10.1016/j.coi.2010.02.007
de Camargo Pereira G, Guimaraes GN, Planello AC, Santamaria MP, de Souza AP, Line SR, Marques MR (2013) Porphyromonas gingivalis LPS stimulation downregulates DNMT1, DNMT3a, and JMJD3 gene expression levels in human HaCaT keratinocytes. Clin Oral Investig 17(4):1279–1285. doi:10.1007/s00784-012-0816-z
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(3):428–437. doi:10.1136/gutjnl-2014-306944
Diacovich L, Gorvel JP (2010) Bacterial manipulation of innate immunity to promote infection. Nat Rev Microbiol 8(2):117–128. doi:10.1038/nrmicro2295
Ding SZ, Fischer W, Kaparakis-Liaskos M, Liechti G, Merrell DS, Grant PA, Ferrero RL, Crowe SE, Haas R, Hatakeyama M, Goldberg JB (2010a) Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One 5(4):e9875. doi:10.1371/journal.pone.0009875
Ding SZ, Goldberg JB, Hatakeyama M (2010b) Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future Oncol 6(5):851–862. doi:10.2217/fon.10.37
Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, Sorek R, Rechavi G (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485(7397):201–206. doi:10.1038/nature11112
Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC, Zheng GQ, Pan T, Solomon O, Eyal E, Hershkovitz V, Han D, Dore LC, Amariglio N, Rechavi G, He C (2016) The dynamic N-1-methyladenosine methylome in eukaryotic messenger RNA. Nature 530(7591):441–446. doi:10.1038/nature16998
Du J, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16(9):519–532. doi:10.1038/nrm4043
Dumler JS, Sinclair SH, Pappas-Brown V, Shetty AC (2016) Genome-wide Anaplasma phagocytophilum AnkA-DNA interactions are enriched in intergenic regions and gene promoters and correlate with infection-induced differential gene expression. Front Cell Infect Microbiol 20(6):97. doi:10.3389/fcimb.2016.00097
Dunphy PS, Luo T, McBride JW (2014) Ehrlichia chaffeensis exploits host SUMOylation pathways to mediate effector-host interactions and promote intracellular survival. Infect Immun 82(10):4154–4168. doi:10.1128/IAI.01984-14
Dussurget O, Bierne H, Cossart P (2014) The bacterial pathogen Listeria monocytogenes and the interferon family: type I, type II and type III interferons. Front Cell Infect Microbiol 4:50. doi:10.3389/fcimb.2014.00050
El Gazzar M, Yoza BK, Chen X, Hu J, Hawkins GA, McCall CE (2008) G9a and HP1 couple histone and DNA methylation to TNFalpha transcription silencing during endotoxin tolerance. J Biol Chem 283(47):32198–32208. doi:10.1074/jbc.M803446200
Eskandarian HA, Impens F, Nahori MA, Soubigou G, Coppee JY, Cossart P, Hamon MA (2013) A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science 341(6145):1238858. doi:10.1126/science.1238858
Faghihi MA, Wahlestedt C (2009) Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 10(9):637–643. doi:10.1038/nrm2738
Farris TR, Dunphy PS, Zhu B, Kibler CE, McBride JW (2016) Ehrlichia chaffeensis TRP32 is a nucleomodulin that directly regulates expression of host genes governing differentiation and proliferation. Infect Immun 84:3182–3194. doi:10.1128/IAI.00657-16
Fehri LF, Rechner C, Janssen S, Mak TN, Holland C, Bartfeld S, Bruggemann 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(8):577–586
Fujita N, Watanabe S, Ichimura T, Tsuruzoe S, Shinkai Y, Tachibana M, Chiba T, Nakao M (2003) Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem 278(26):24132–24138. doi:10.1074/jbc.M302283200
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446–450. doi:10.1038/nature12721
Furusawa Y, Obata Y, Hase K (2015) Commensal microbiota regulates T cell fate decision in the gut. Semin Immunopathol 37(1):17–25. doi:10.1007/s00281-014-0455-3
Garcia-Dominguez M, Reyes JC (2009) SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 1789(6–8):451–459. doi:10.1016/j.bbagrm.2009.07.001
Garcia-Garcia JC, Barat NC, Trembley SJ, Dumler JS (2009a) Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog 5(6):e1000488. doi:10.1371/journal.ppat.1000488
Garcia-Garcia JC, Rennoll-Bankert KE, Pelly S, Milstone AM, Dumler JS (2009b) Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen Anaplasma phagocytophilum. Infect Immun 77(6):2385–2391. doi:10.1128/IAI.00023-09
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(4):895–911. doi:10.1189/jlb.0611286
Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453(7197):948–951. doi:10.1038/nature06947
Ha SD, Han CY, Reid C, Kim SO (2014) HDAC8-mediated epigenetic reprogramming plays a key role in resistance to anthrax lethal toxin-induced pyroptosis in macrophages. J Immunol 193(3):1333–1343. doi:10.4049/jimmunol.1400420
Ha SD, Reid C, Meshkibaf S, Kim SO (2016) Inhibition of interleukin 1beta (IL-1beta) expression by anthrax Lethal Toxin (LeTx) is reversed by Histone Deacetylase 8 (HDAC8) inhibition in murine macrophages. J Biol Chem 291(16):8745–8755. doi:10.1074/jbc.M115.695809
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(26):23851–23860. doi:10.1074/jbc.M300075200
Hamon MA, Batsche E, Regnault B, Tham TN, Seveau S, Muchardt C, Cossart P (2007) Histone modifications induced by a family of bacterial toxins. Proc Natl Acad Sci U S A 104 (33):13467–13472. doi:10.1073/pnas.0702729104
Hamon M, Bierne H, Cossart P (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4(6):423–434. doi:10.1038/nrmicro1413
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(7):2839–2846. doi:10.1128/IAI.01243-10
Haraga A, Miller SI (2003) A Salmonella enterica serovar typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect Immun 71(7):4052–4058
Harouz H, Rachez C, Meijer BM, Marteyn B, Donnadieu F, Cammas F, Muchardt C, Sansonetti P, Arbibe L (2014) Shigella flexneri targets the HP1gamma subcode through the phosphothreonine lyase OspF. EMBO J 33 (22):2606–2622. doi:10.15252/embj.201489244
Hattori N, Ushijima T (2016) Epigenetic impact of infection on carcinogenesis: mechanisms and applications. Genome Med 8(1):10. doi:10.1186/s13073-016-0267-2
Hicks SW, Galan JE (2010) Hijacking the host ubiquitin pathway: structural strategies of bacterial E3 ubiquitin ligases. Curr Opin Microbiol 13(1):41–46. doi:10.1016/j.mib.2009.11.008
Hiragami-Hamada K, Shinmyozu K, Hamada D, Tatsu Y, Uegaki K, Fujiwara S, Nakayama J (2011) N-terminal phosphorylation of HP1{alpha} promotes its chromatin binding. Mol Cell Biol 31(6):1186–1200. doi:10.1128/MCB.01012-10
Hnilicova J, Stanek D (2011) Where splicing joins chromatin. Nucleus 2(3):182–188. doi:10.4161/nucl.2.3.15876
Holeski LM, Jander G, Agrawal AA (2012) Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol Evol 27(11):618–626. doi:10.1016/j.tree.2012.07.011
Hur K, Niwa T, Toyoda T, Tsukamoto T, Tatematsu M, Yang HK, Ushijima T (2011) Insufficient role of cell proliferation in aberrant DNA methylation induction and involvement of specific types of inflammation. Carcinogenesis 32(1):35–41. doi:10.1093/carcin/bgq219
Ichimura T, Watanabe S, Sakamoto Y, Aoto T, Fujita N, Nakao M (2005) Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins. J Biol Chem 280(14):13928–13935. doi:10.1074/jbc.M413654200
Ifrim DC, Quintin J, Joosten LA, Jacobs C, Jansen T, Jacobs L, Gow NA, Williams DL, van der Meer JW, Netea MG (2014) Trained immunity or tolerance: opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors. Clin Vaccine Immunol 21(4):534–545. doi:10.1128/CVI.00688-13
Imai K, Inoue H, Tamura M, Cueno ME, Inoue H, Takeichi O, Kusama K, Saito I, Ochiai K (2012) The periodontal pathogen Porphyromonas gingivalis induces the Epstein-Barr virus lytic switch transactivator ZEBRA by histone modification. Biochimie 94(3):839–846. doi:10.1016/j.biochi.2011.12.001
Imai K, Inoue H, Tamura M, Cueno ME, Takeichi O, Kusama K, Saito I, Ochiai K (2011) The periodontal pathogen Porphyromonas gingivalis induces the Epstein-Barr virus lytic switch transactivator ZEBRA by histone modification. Biochimie. doi:10.1016/j.biochi.2011.12.001
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(6):3688–3695. doi:10.4049/jimmunol.0802906
Jenner RG, Young RA (2005) Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3(4):281–294. doi:10.1038/nrmicro1126
Jimenez A, Chen D, Alto NM (2016) How bacteria subvert animal cell structure and function. Annu Rev Cell Dev Biol. doi:10.1146/annurev-cellbio-100814-125227
Jose L, Ramachandran R, Bhagavat R, Gomez RL, Chandran A, Raghunandanan S, Omkumar RV, Chandra N, Mundayoor S, Kumar RA (2016) Hypothetical protein Rv3423.1 of Mycobacterium tuberculosis is a histone acetyltransferase. FEBS J 283(2):265–281. doi:10.1111/febs.13566
Kaikkonen MU, Lam MT, Glass CK (2011) Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res 90(3):430–440. doi:10.1093/cvr/cvr097
Kleinnijenhuis J, Quintin J, Preijers F, Joosten LA, Ifrim DC, Saeed S, Jacobs C, van Loenhout J, de Jong D, Stunnenberg HG, Xavier RJ, van der Meer JW, van Crevel R, Netea MG (2012) Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci U S A 109(43):17537–17542. doi:10.1073/pnas.1202870109
Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31 (2):89–97. doi:1016/j.tibs.2005.12.008
Kohwi-Shigematsu T, Kohwi Y, Takahashi K, Richards HW, Ayers SD, Han HJ, Cai S (2012) SATB1-mediated functional packaging of chromatin into loops. Methods 58(3):243–254. doi:10.1016/j.ymeth.2012.06.019
Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693–705. doi:10.1016/j.cell.2007.02.005
Lai AY, Wade PA (2011) Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer 11(8):588–596. doi:10.1038/nrc3091
Lakisic G, Lebreton A, Pourpre R, Wendling O, Libertini E, Radford EJ, Le Guillou M, Champy MF, Wattenhofer-Donze M, Soubigou G, Ait-Si-Ali S, Feunteun J, Sorg T, Coppee JY, Ferguson-Smith AC, Cossart P, Bierne H (2016) Role of the BAHD1 chromatin-repressive complex in placental development and regulation of steroid metabolism. PLoS Genet 12(3):e1005898. doi:10.1371/journal.pgen.1005898
Langst G, Manelyte L (2015) Chromatin remodelers: from function to dysfunction. Genes (Basel) 6(2):299–324. doi:10.3390/genes6020299
Latham JA, Dent SY (2007) Cross-regulation of histone modifications. Nat Struct Mol Biol 14(11):1017–1024. doi:10.1038/nsmb1307
Latham T, Mackay L, Sproul D, Karim M, Culley J, Harrison DJ, Hayward L, Langridge-Smith P, Gilbert N, Ramsahoye BH (2012) Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Res 40(11):4794–4803. doi:10.1093/nar/gks066
Lebreton A, Cossart P, Bierne H (2012) Bacteria tune interferon responses by playing with chromatin. Virulence 3(1):87–91
Lebreton A, Job V, Ragon M, Le Monnier A, Dessen A, Cossart P, Bierne H (2014) Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA. MBio 5(1):e00775–e00713. doi:10.1128/mBio.00775-13
Lebreton A, Lakisic G, Job V, Fritsch L, Tham TN, Camejo A, Mattei P-J, Regnault B, Nahori M-A, 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(6022):1319–1321
Lee HC, Kioi M, Han J, Puri RK, Goodman JL (2008) Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics 92(3):144–151. doi:10.1016/j.ygeno.2008.05.005
Lee JS, Smith E, Shilatifard A (2010) The language of histone crosstalk. Cell 142(5):682–685. doi:10.1016/j.cell.2010.08.011
Li T, Lu Q, Wang G, Xu H, Huang H, Cai T, Kan B, Ge J, Shao F (2013) SET-domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription. EMBO Rep 14(8):733–740. doi:10.1038/embor.2013.86
Li H, Rauch T, Chen ZX, Szabo PE, Riggs AD, Pfeifer GP (2006) The histone methyltransferase SETDB1 and the DNA methyltransferase DNMT3A interact directly and localize to promoters silenced in cancer cells. J Biol Chem 281(28):19489–19500. doi:10.1074/jbc.M513249200
Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou J-M, Shao F (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315(5814):1000–1003. doi:10.1126/science.1138960
Libertini E, Lebreton A, Lakisic G, Dillies MA, Beck S, Coppee JY, Cossart P, Bierne H (2015) Overexpression of the heterochromatinization factor BAHD1 in HEK293 cells differentially reshapes the DNA methylome on autosomes and X chromosome. Front Genet 6:339. doi:10.3389/fgene.2015.00339
Licciardi PV, Wong SS, Tang ML, Karagiannis TC (2010) Epigenome targeting by probiotic metabolites. Gut Pathog 2(1):24. doi:10.1186/1757-4749-2-24
Liu Y, Zhang X, Blumenthal RM, Cheng X (2013) A common mode of recognition for methylated CpG. Trends Biochem Sci 38(4):177–183. doi:10.1016/j.tibs.2012.12.005
Luo T, Kuriakose JA, Zhu B, Wakeel A, McBride JW (2011) Ehrlichia chaffeensis TRP120 interacts with a diverse array of eukaryotic proteins involved in transcription, signaling, and cytoskeleton organization. Infect Immun 79(11):4382–4391. doi:10.1128/IAI.05608-11
Luo T, McBride JW (2012) Ehrlichia chaffeensis TRP32 interacts with host cell targets that influence intracellular survival. Infect Immun 80(7):2297–2306. doi:10.1128/IAI.00154-12
Ma KW, Flores C, Ma W (2011) Chromatin configuration as a battlefield in plant-bacteria interactions. Plant Physiol. doi:10.1104/pp.111.182295
Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, Arii K, Kaneda A, Tsukamoto T, Tatematsu M, Tamura G, Saito D, Sugimura T, Ichinose M, Ushijima T (2006) High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 12(3 Pt 1):989–995. doi:10.1158/1078-0432.CCR-05-2096
Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469(7330):343–349. doi:10.1038/nature09784
Masaki T, McGlinchey A, Cholewa-Waclaw J, Qu J, Tomlinson SR, Rambukkana A (2014) Innate immune response precedes Mycobacterium leprae-induced reprogramming of adult Schwann cells. Cell Reprogram 16(1):9–17. doi:10.1089/cell.2013.0064
Masaki T, Qu J, Cholewa-Waclaw J, Burr K, Raaum R, Rambukkana A (2013) Reprogramming adult Schwann cells to stem cell-like cells by leprosy bacilli promotes dissemination of infection. Cell 152(1–2):51–67. doi:10.1016/j.cell.2012.12.014
Mattick JS, Makunin IV (2005) Small regulatory RNAs in mammals. Hum Mol Genet 14(1):R121–R132. doi:10.1093/hmg/ddi101
Mattout A, Cabianca DS, Gasser SM (2015) Chromatin states and nuclear organization in development—a view from the nuclear lamina. Genome Biol 16:174. doi:10.1186/s13059-015-0747-5
McCall CE, Yoza B, Liu T, El Gazzar M (2010) Gene-specific epigenetic regulation in serious infections with systemic inflammation. J Innate Immun 2(5):395–405. doi:10.1159/000314077
McCoy MW, Marre ML, Lesser CF, Mecsas J (2010) The C-terminal tail of Yersinia pseudotuberculosis YopM is critical for interacting with RSK1 and for virulence. Infect Immun 78(6):2584–2598. doi:10.1128/IAI.00141-10
McDonald C, Vacratsis PO, Bliska JB, Dixon JE (2003) The yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J Biol Chem 278(20):18514–18523. doi:10.1074/jbc.M301226200
Medvedeva YA, Lennartsson A, Ehsani R, Kulakovskiy IV, Vorontsov IE, Panahandeh P, Khimulya G, Kasukawa T, Consortium F, Drablos F (2015) EpiFactors: a comprehensive database of human epigenetic factors and complexes. Database (Oxford) 2015:bav067. doi:10.1093/database/bav067
Medzhitov R, Horng T (2009) Transcriptional control of the inflammatory response. Nature Rev Immunol 9(10):692–703. doi:10.1038/nri2634
Meyer KD, Jaffrey SR (2014) The dynamic epitranscriptome: N6-methyladenosine and gene expression control. Nat Rev Mol Cell Biol 15(5):313–326. doi:10.1038/nrm3785
Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448(7153):553–560. doi:10.1038/nature06008
Minarovits J (2009) Microbe-induced epigenetic alterations in host cells: the coming era of patho-epigenetics of microbial infections. A review. Acta Microbiol Immunol Hung 56(1):1–19. doi:10.1556/AMicr.56.2009.1.1
Mohammad HP, Baylin SB (2010) Linking cell signaling and the epigenetic machinery. Nat Biotechnol 28(10):1033–1038. doi:10.1038/nbt1010-1033
Mojica SA, Hovis KM, Frieman MB, Tran B, Hsia RC, Ravel J, Jenkins-Houk C, Wilson KL, Bavoil PM (2015) SINC, a type III secreted protein of Chlamydia psittaci, targets the inner nuclear membrane of infected cells and uninfected neighbors. Mol Biol Cell 26(10):1918–1934. doi:10.1091/mbc.E14-11-1530
Morris TL, Arnold RR, Webster-Cyriaque J (2007) Signaling cascades triggered by bacterial metabolic end products during reactivation of Kaposi's sarcoma-associated herpesvirus. J Virol 81(11):6032–6042. doi:10.1128/JVI.02504-06
Mujtaba S, Winer BY, Jaganathan A, Patel J, Sgobba M, Schuch R, Gupta YK, Haider S, Wang R, Fischetti VA (2013) Anthrax SET protein: a potential virulence determinant that epigenetically represses NF-kappaB activation in infected macrophages. J Biol Chem 288(32):23458–23472. doi:10.1074/jbc.M113.467696
Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O’Neill LA, Xavier RJ (2016) Trained immunity: a program of innate immune memory in health and disease. Science 352(6284):aaf1098. doi:10.1126/science.aaf1098
Nigro G, Rossi R, Commere PH, Jay P, Sansonetti PJ (2014) The cytosolic bacterial peptidoglycan sensor Nod2 affords stem cell protection and links microbes to gut epithelial regeneration. Cell Host Microbe 15(6):792–798. doi:10.1016/j.chom.2014.05.003
Niwa T, Tsukamoto T, Toyoda T, Mori A, Tanaka H, Maekita T, Ichinose M, Tatematsu M, Ushijima T (2010) Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res 70(4):1430–1440. doi:10.1158/0008-5472.CAN-09-2755
Noordermeer D, Duboule D (2013) Chromatin looping and organization at developmentally regulated gene loci. Wiley Interdiscip Rev Dev Biol 2(5):615–630. doi:10.1002/wdev.103
Ohta K, Kawano R, Ito N (2012) Lactic acid bacteria convert human fibroblasts to multipotent cells. PloS one 7(12):e51866. doi:10.1371/journal.pone.0051866
Okuda J, Toyotome T, Kataoka N, Ohno M, Abe H, Shimura Y, Seyedarabi A, Pickersgill R, Sasakawa C (2005) Shigella effector IpaH9.8 binds to a splicing factor U2AF35 to modulate host immune responses. Biochem Biophys Res Commun 333 (2):531–539. doi:10.1016/j.bbrc.2005.05.145
Opitz B, Puschel A, Beermann W, Hocke AC, Forster 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(1):484–490. doi:10.4049/jimmunol.176.1.484
Ostuni R, Piccolo V, Barozzi I, Polletti S, Termanini A, Bonifacio S, Curina A, Prosperini E, Ghisletti S, Natoli G (2013) Latent enhancers activated by stimulation in differentiated cells. Cell 152 (1–2):157–171. doi:10.1016/j.cell.2012.12.018
Pacis A, Tailleux L, Morin AM, Lambourne J, MacIsaac JL, Yotova V, Dumaine A, Danckaert A, Luca F, Grenier JC, Hansen KD, Gicquel B, Yu M, Pai A, He C, Tung J, Pastinen T, Kobor MS, Pique-Regi R, Gilad Y, Barreiro LB (2015) Bacterial infection remodels the DNA methylation landscape of human dendritic cells. Genome Res 25(12):1801–1811. doi:10.1101/gr.192005.115
Padeken J, Heun P (2014) Nucleolus and nuclear periphery: velcro for heterochromatin. Curr Opin Cell Biol 28:54–60. doi:10.1016/j.ceb.2014.03.001
Pamer EG (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4(10):812–823. doi:10.1038/nri1461
Park J, Kim KJ, K-S C, Grab DJ, Dumler JS (2004) Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol 6(8):743–751. doi:10.1111/j.1462-5822.2004.00400.x
Pathak SK, Basu S, Bhattacharyya A, Pathak S, Banerjee A, Basu J, Kundu M (2006) TLR4-dependent NF-kappaB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J Immunol 177(11):7950–7958. doi:10.4049/jimmunol.177.11.7950
Pennini ME, Liu Y, Yang J, Croniger CM, Boom WH, Harding CV (2007) CCAAT/enhancer-binding protein beta and delta binding to CIITA promoters is associated with the inhibition of CIITA expression in response to Mycobacterium tuberculosis 19-kDa lipoprotein. J Immunol 179 (10):6910–6918. doi:179/10/6910 [pii]
Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV (2006) Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 176(7):4323–4330. doi:10.4049/jimmunol.176.7.4323
Pennini M, 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(7):e1000995. doi:10.1371/journal.ppat.1000995
Perdiguero EG, Geissmann F (2016) The development and maintenance of resident macrophages. Nat Immunol 17(1):2–8. doi:10.1038/ni.3341
Quintin J, Saeed S, Martens JH, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, Jacobs L, Jansen T, Kullberg BJ, Wijmenga C, Joosten LA, Xavier RJ, van der Meer JW, Stunnenberg HG, Netea MG (2012) Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12(2):223–232. doi:10.1016/j.chom.2012.06.006
Rais Y, Zviran A, Geula S, Gafni O, Chomsky E, Viukov S, Mansour AA, Caspi I, Krupalnik V, Zerbib M, Maza I, Mor N, Baran D, Weinberger L, Jaitin DA, Lara-Astiaso D, Blecher-Gonen R, Shipony Z, Mukamel Z, Hagai T, Gilad S, Amann-Zalcenstein D, Tanay A, Amit I, Novershtern N, Hanna JH (2013) Deterministic direct reprogramming of somatic cells to pluripotency. Nature 502(7469):65–70. doi:10.1038/nature12587
Ram O, Goren A, Amit I, Shoresh N, Yosef N, Ernst J, Kellis M, Gymrek M, Issner R, Coyne M, Durham T, Zhang X, Donaghey J, Epstein CB, Regev A, Bernstein BE (2011) Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 147(7):1628–1639. doi:10.1016/j.cell.2011.09.057
Raymond B, Batsche E, Boutillon F, Wu YZ, Leduc D, Balloy V, Raoust E, Muchardt C, Goossens PL, Touqui L (2009) Anthrax lethal toxin impairs IL-8 expression in epithelial cells through inhibition of histone H3 modification. PLoS Pathog 5(4):e1000359. doi:10.1371/journal.ppat.1000359
Rennoll-Bankert KE, Dumler JS (2012) Lessons from Anaplasma phagocytophilum: chromatin remodeling by bacterial effectors. Infect Disord Drug Targets 12(5):380–387
Rennoll-Bankert KE, Garcia-Garcia JC, Sinclair SH, Dumler JS (2015) Chromatin-bound bacterial effector ankyrin A recruits histone deacetylase 1 and modifies host gene expression. Cell Microbiol 17(11):1640–1652. doi:10.1111/cmi.12461
Riggs AD, Martienssen RA, Russo VEA (1996) Introduction. In Russo, VEA et al (ed) Epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, New York, p 1
Riggs MG, Whittaker RG, Neumann JR, Ingram VM (1977) n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature 268(5619):462–464
Roadmap Epigenomics C, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, Heravi-Moussavi A, Kheradpour P, Zhang Z, Wang J, Ziller MJ, Amin V, Whitaker JW, Schultz MD, Ward LD, Sarkar A, Quon G, Sandstrom RS, Eaton ML, Wu YC, Pfenning AR, Wang X, Claussnitzer M, Liu Y, Coarfa C, Harris RA, Shoresh N, Epstein CB, Gjoneska E, Leung D, Xie W, Hawkins RD, Lister R, Hong C, Gascard P, Mungall AJ, Moore R, Chuah E, Tam A, Canfield TK, Hansen RS, Kaul R, Sabo PJ, Bansal MS, Carles A, Dixon JR, Farh KH, Feizi S, Karlic R, Kim AR, Kulkarni A, Li D, Lowdon R, Elliott G, Mercer TR, Neph SJ, Onuchic V, Polak P, Rajagopal N, Ray P, Sallari RC, Siebenthall KT, Sinnott-Armstrong NA, Stevens M, Thurman RE, Wu J, Zhang B, Zhou X, Beaudet AE, Boyer LA, De Jager PL, Farnham PJ, Fisher SJ, Haussler D, Jones SJ, Li W, Marra MA, McManus MT, Sunyaev S, Thomson JA, Tlsty TD, Tsai LH, Wang W, Waterland RA, Zhang MQ, Chadwick LH, Bernstein BE, Costello JF, Ecker JR, Hirst M, Meissner A, Milosavljevic A, Ren B, Stamatoyannopoulos JA, Wang T, Kellis M (2015) Integrative analysis of 111 reference human epigenomes. Nature 518(7539):317–330. doi:10.1038/nature14248
Rohde JR, Breitkreutz A, Chenal A, Sansonetti PJ, Parsot C (2007) Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1(1):77–83. doi:10.1016/j.chom.2007.02.002
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(4):395–405. doi:10.1016/j.chom.2013.03.004
Romanoski CE, Glass CK, Stunnenberg HG, Wilson L, Almouzni G (2015) Epigenomics: roadmap for regulation. Nature 518(7539):314–316. doi:10.1038/518314a
Rye M, Sandve GK, Daub CO, Kawaji H, Carninci P, Forrest AR, Drablos F, Fantom Consortium (2014) Chromatin states reveal functional associations for globally defined transcription start sites in four human cell lines. BMC Genomics 15:120. doi:10.1186/1471-2164-15-120
Saccani S, Pantano S, Natoli G (2002) p38-Dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat Immunol 3(1):69–75. doi:10.1038/ni748
Sadakierska-Chudy A, Filip M (2015) A comprehensive view of the epigenetic landscape. Part II: Histone post-translational modification, nucleosome level, and chromatin regulation by ncRNAs. Neurotox Res 27(2):172–197. doi:10.1007/s12640-014-9508-6
Salles, II, Tucker AE, Voth DE, Ballard JD (2003) Toxin-induced resistance in Bacillus anthracis lethal toxin-treated macrophages. Proc Natl Acad Sci U S A 100 (21):12426–12431. doi:10.1073/pnas.2134042100
Samba-Louaka A, Pereira JM, Nahori MA, Villiers V, Deriano L, Hamon MA, Cossart P (2014) Listeria monocytogenes dampens the DNA damage response. PLoS Pathog 10(10):e1004470. doi:10.1371/journal.ppat.1004470
Sasai N, Defossez PA (2009) Many paths to one goal? The proteins that recognize methylated DNA in eukaryotes. Int J Dev Biol 53(2–3):323–334. doi:10.1387/ijdb.082652ns
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(2):940–947. doi:10.4049/jimmunol.181.2.940
Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24(20):2264–2269. doi:10.1101/gad.590910
Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottiere HM, Galmiche JP (2000) Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut 47(3):397–403
Seyedarabi A, Sullivan JA, Sasakawa C, Pickersgill RW (2011) A disulfide driven domain swap switches off the activity of Shigella IpaH9.8 E3 ligase. FEBS Lett 584(19):4163–4168. doi:10.1016/j.febslet.2010.09.006
Shames SR, Bhavsar AP, Croxen MA, Law RJ, Mak SH, Deng W, Li Y, Bidshari R, de Hoog CL, Foster LJ, Finlay BB (2011) The pathogenic Escherichia coli type III secreted protease NleC degrades the host acetyltransferase p300. Cell Microbiol 13(10):1542–1557. doi:10.1111/j.1462-5822.2011.01640.x
Sharma G, Sowpati DT, Singh P, Khan MZ, Ganji R, Upadhyay S, Banerjee S, Nandicoori VK, Khosla S (2016) Genome-wide non-CpG methylation of the host genome during M. tuberculosis infection. Sci Rep 6:25006. doi:10.1038/srep25006
Sharma G, Upadhyay S, Srilalitha M, Nandicoori VK, Khosla S (2015) The interaction of mycobacterial protein Rv2966c with host chromatin is mediated through non-CpG methylation and histone H3/H4 binding. Nucleic Acids Res 43(8):3922–3937. doi:10.1093/nar/gkv261
Sinclair SH, Garcia-Garcia JC, Dumler JS (2015a) Bioinformatic and mass spectrometry identification of Anaplasma phagocytophilum proteins translocated into host cell nuclei. Front Microbiol 6:55. doi:10.3389/fmicb.2015.00055
Sinclair SH, Rennoll-Bankert KE, Dumler JS (2014) Effector bottleneck: microbial reprogramming of parasitized host cell transcription by epigenetic remodeling of chromatin structure. Front Genet 5:274. doi:10.3389/fgene.2014.00274
Sinclair SH, Yegnasubramanian S, Dumler JS (2015b) Global DNA methylation changes and differential gene expression in Anaplasma phagocytophilum-infected human neutrophils. Clin Epigenetics 7(1):77. doi:10.1186/s13148-015-0105-1
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(5):L818–L826. doi:10.1152/ajplung.00428.2005
Sommer F, Backhed F (2013) The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11(4):227–238. doi:10.1038/nrmicro2974
Soundararajan V, Patel N, Subramanian V, Sasisekharan V, Sasisekharan R (2011) The many faces of the YopM effector from plague causative bacterium Yersinia pestis and its implications for host immune modulation. Innate Immun 17(6):548–557. doi:10.1177/1753425910377099
Suganuma T, Workman JL (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80:473–499. doi:10.1146/annurev-biochem-061809-175347
Sun J (2010) Enteric bacteria and cancer stem cells. Cancers 3(1):285–297. doi:10.3390/cancers3010285
Tahoun A, Mahajan S, Paxton E, Malterer G, Donaldson DS, Wang D, Tan A, Gillespie TL, O'Shea M, Roe AJ, Shaw DJ, Gally DL, Lengeling A, Mabbott NA, Haas J, Mahajan A (2012) Salmonella transforms follicle-associated epithelial cells into M cells to promote intestinal invasion. Cell Host Microbe 12(5):645–656. doi:10.1016/j.chom.2012.10.009
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(41):35755–35762. doi:10.1074/jbc.M111.271007
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676. doi:10.1016/j.cell.2006.07.024
Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14(11):1025–1040. doi:10.1038/nsmb1338
Ting K, Aitken KJ, Penna F, Samiei AN, Sidler M, Jiang JX, Ibrahim F, Tolg C, Delgado-Olguin P, Rosenblum N, Bagli DJ (2016) Uropathogenic E.coli (UPEC) infection induces proliferation through Enhancer of Zeste Homologue 2 (EZH2). PLoS One 11(3):e0149118. doi:10.1371/journal.pone.0149118
Tisseur M, Kwapisz M, Morillon A (2011) Pervasive transcription – Lessons from yeast. Biochimie 93(11):1889–1896. doi:10.1016/j.biochi.2011.07.001
Tiwari VK, Stadler MB, Wirbelauer C, Paro R, Schubeler D, Beisel C (2011) A chromatin-modifying function of JNK during stem cell differentiation. Nat Genet 44(1):94–100. doi:10.1038/ng.1036
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
Toyotome T (2001) Shigella protein IpaH9.8 Is secreted from bacteria within mammalian cells and transported to the nucleus. J Biol Chem 276(34):32071–32079. doi:10.1074/jbc.M101882200
Turgeon N, Blais M, Gagne JM, Tardif V, Boudreau F, Perreault N, Asselin C (2013) HDAC1 and HDAC2 restrain the intestinal inflammatory response by regulating intestinal epithelial cell differentiation. PLoS One 8(9):e73785. doi:10.1371/journal.pone.0073785
Turner AM, Morris KV (2010) Controlling transcription with noncoding RNAs in mammalian cells. Biotechniques 48(6):ix–xvi. doi:10.2144/000113442
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. doi:10.1158/1078-0432.CCR-11-2011
Valenzuela MA, Canales J, Corvalan AH, Quest AF (2015) Helicobacter pylori-induced inflammation and epigenetic changes during gastric carcinogenesis. World J Gastroenterol 21(45):12742–12756. doi:10.3748/wjg.v21.i45.12742
Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439(7078):871–874. doi:10.1038/nature04431
Wakeel A, Zhu B, Yu XJ, McBride JW (2010) New insights into molecular Ehrlichia chaffeensis-host interactions. Microbes Infect 12(5):337–345. doi:10.1016/j.micinf.2010.01.009
Wang Y, Curry HM, Zwilling BS, Lafuse WP (2005) Mycobacteria inhibition of IFN-gamma induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J Immunol 174(9):5687–5694. doi:10.4049/jimmunol.174.9.5687
Wang TY, Han ZM, Chai YR, Zhang JH (2010) A mini review of MAR-binding proteins. Mol Biol Rep 37 (7):3553–3560. doi:10.1007/s11033-010-0003-8
Wani AH, Boettiger AN, Schorderet P, Ergun A, Munger C, Sadreyev RI, Zhuang X, Kingston RE, Francis NJ (2016) Chromatin topology is coupled to Polycomb group protein subnuclear organization. Nat Commun 7:10291. doi:10.1038/ncomms10291
Weber MM, Faris R, McLachlan J, Tellez A, Wright WU, Galvan G, Luo ZQ, Samuel JE (2016) Modulation of the host transcriptome by Coxiella burnetii nuclear effector Cbu1314. Microbes Infect 18(5):336–345. doi:10.1016/j.micinf.2016.01.003
Wu H, Zhang Y (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25(23):2436–2452. doi:10.1101/gad.179184.111
Xia G, Schneider-Stock R, Diestel A, Habold C, Krueger S, Roessner A, Naumann M, Lendeckel U (2008) Helicobacter pylori regulates p21(WAF1) by histone H4 acetylation. Biochem Biophys Res Commun 369 (2):526–531. doi:1016/j.bbrc.2008.02.073
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(6940):655–659. doi:10.1038/nature01576
Yan J, Zhang M, Zhang J, Chen X, Zhang X (2011) Helicobacter pylori infection promotes methylation of WWOX gene in human gastric cancer. Biochem Biophys Res Commun 408(1):99–102. doi:10.1016/j.bbrc.2011.03.127
Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD, Dorrestein PC, Rosenfeld MG (2011) ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147(4):773–788. doi:10.1016/j.cell.2011.08.054
Yao Y, Tao H, Park DI, Sepulveda JL, Sepulveda AR (2006) Demonstration and characterization of mutations induced by Helicobacter pylori organisms in gastric epithelial cells. Helicobacter 11(4):272–286. doi:10.1111/j.1523-5378.2006.00408.x
Yaseen I, Kaur P, Nandicoori VK, Khosla S (2015) Mycobacteria modulate host epigenetic machinery by Rv1988 methylation of a non-tail arginine of histone H3. Nat Commun 6:8922. doi:10.1038/ncomms9922
Ye F, Karn J (2015) Bacterial short chain fatty acids push all the buttons needed to reactivate latent viruses. Stem Cell Epigenetics 2(1). doi:10.14800/sce.532
Yin L, Chung WO (2011) Epigenetic regulation of human beta-defensin 2 and CC chemokine ligand 20 expression in gingival epithelial cells in response to oral bacteria. Mucosal Immunol 4(4):409–419. doi:10.1038/mi.2010.83
Yuan X, Feng W, Imhof A, Grummt I, Zhou Y (2007) Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol Cell 27(4):585–595. doi:10.1016/j.molcel.2007.06.021
Zhang S, Barros SP, Niculescu MD, Moretti AJ, Preisser JS, Offenbacher S (2010) Alteration of PTGS2 promoter methylation in chronic periodontitis. J Dent Res 89(2):133–137. doi:10.1177/0022034509356512
Zhou Y, Kim J, Yuan X, Braun T (2011) Epigenetic modifications of stem cells: a paradigm for the control of cardiac progenitor cells. Circ Res 109(9):1067–1081. doi:10.1161/CIRCRESAHA.111.243709
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(10):4243–4255. doi:10.1128/IAI.00376-09
Zurawski DV, Mumy KL, Faherty CS, Mccormick BA, Maurelli AT (2009) Shigella flexneritype III secretion system effectors OspB and OspF target the nucleus to downregulate the host inflammatory response via interactions with retinoblastoma protein. Mol Microbiol 71(2):350–368. doi:10.1111/j.1365-2958.2008.06524.x
Acknowledgements
I apologize to colleagues whose work was not cited here. I acknowledge support from INRA, French Ligue Nationale Contre le Cancer (LNCC RS10/75-76 Bierne), French National Research Agency (ANR, grant EPILIS), and the iXcore Research Foundation.
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Bierne, H. (2017). Cross Talk Between Bacteria and the Host Epigenetic Machinery. In: Doerfler, W., Casadesús, J. (eds) Epigenetics of Infectious Diseases. Epigenetics and Human Health. Springer, Cham. https://doi.org/10.1007/978-3-319-55021-3_6
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