Abstract
Epigenetic programming of the pathogen and the host can have a marked influence on the development and progression of acute and chronic disease. Bacterial pathogenesis may be viewed as a developmental program similar to that of cell differentiation and development in eukaryotes. Bacterial epigenetic programming is imparted by DNA methylation, whereby the virulence traits expressed by a pathogen may depend on the cumulative interactions between the microbe and its environment. Such bacterial “memory” provides a means for adaptation to the varied subsequent microenvironments encountered during the infective process. DNA methylation can affect DNA–protein interactions and resultant gene expression by altering DNA thermodynamic stability and curvature and by methyl-group-mediated steric hindrance. Some of these epigenetic interactions can form heritable DNA methylation patterns in the microbial genome that control gene expression in their progeny cells. Microbes can also stimulate heritable changes in the host epigenome via infection-associated alterations to host epigenetic determinants including DNA methylation, histone modifications, chromatin-associated complexes, and noncoding RNA-mediated silencing. The resultant changes in host chromatin remodeling and gene expression may be localized and/or systemic due to direct microbe-to-host cell communication or via dissemination of microbial-host signaling. Thus, the role of epigenetics in host–microbe interactions may be the nexus of many pathological syndromes even though there may be no apparent direct link between infection and disease, providing the basis for the development of novel therapeutics and diagnostic tests for diseases with epigenomic determinants.
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References
Anayannis N, Schlecht N, Belbin T (2015) Epigenetic mechanisms of human papillomavirus-associated head and neck cancer. Arch Pathol Lab Med. doi:10.5858/arpa.2014-0554-RA
Atack J, Srikhanta Y, Fox K, Jurcisek J, Brockman K, Clark T, Boitano M, Power P, Jen F-C, McEwan A (2015) A biphasic epigenetic switch controls immunoevasion, virulence and niche adaptation in non-typeable Haemophilus influenzae. Nat Commun 6:7828. doi:10.1038./ncomms8828
Bach T, Krekling M, Skarstad K (2003) Excess SeqA prolongs sequestration of oriC and delays nucleoid segregation and cell division. EMBO J 22:315–323
Badie G, Heithoff D, Mahan M (2004) LcrV synthesis is altered by DNA adenine methylase overproduction in Yersinia pseudotuberculosis and is required to confer immunity in vaccinated hosts. Infect Immun 72:6707–6710
Badie G, Heithoff D, Sinsheimer R, Mahan M (2007) Altered levels of Salmonella DNA adenine methylase are associated with defects in gene expression, motility, flagellar synthesis, and bile resistance in the pathogenic strain 14028 but not in the laboratory strain LT2. J Bacteriol 189:1556–1564
Bannister A, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395
Baylin S, Herman J (2000) DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 16:168–174
Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, Frabetti F, Vitale L, Pelleri M, Tassani S, Piva F (2013) An estimation of the number of cells in the human body. Ann Hum Biol 40:463–471
Bierne H, Hamon M, Cossart P (2012) Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2:a010272
Bigger C, Murray K, Murray N (1973) Recognition sequence of a restriction enzyme. Nature 244:7–10
Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21
Bird A (2007) Perceptions of epigenetics. Nature 447:396–398
Boye E, Marinus M, Løbner-Olesen A (1992) Quantitation of Dam methyltransferase in Escherichia coli. J Bacteriol 174:1682–1685
Camacho E, Casadesús J (2002) Conjugal transfer of the virulence plasmid of Salmonella enterica is regulated by the leucine-responsive regulatory protein and DNA adenine methylation. Mol Microbiol 44:1589–1598
Camacho E, Casadesús J (2005) Regulation of traJ transcription in the Salmonella virulence plasmid by strand-specific DNA adenine hemimethylation. Mol Microbiol 57:1700–1718
Campellone K, Roe A, Løbner-Olesen A, Murphy K, Magoun L, Brady M, Donohue-Rolfe A, Tzipori S, Gally D, Leong J (2007) Increased adherence and actin pedestal formation by dam-deficient enterohaemorrhagic Escherichia coli O157: H7. Mol Microbiol 63:1468–1481
Casadesús J, D’Ari R (2002) Memory in bacteria and phage. Bioessays 24:512–518
Casadesús J, Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70:830–856
Centers for Disease Control and Prevention (2012) Human papillomavirus-associated cancers-United States, 2004–2008. Morb Mortal Wkly Rep 61:258
Centers for Disease Control and Prevention (2015) Humans and Brucella species. http://www.cdc.gov/brucellosis/clinicians/brucella-species.html
Coburn B, Grassl G, Finlay B (2007) Salmonella, the host and disease: a brief review. Immunol Cell Biol 85:112–118
Collier J, Murray SR, Shapiro L (2006) DnaA couples DNA replication and the expression of two cell cycle master regulators. EMBO J 25:346–356
Costenbader K, Gay S, Alarcón-Riquelme M, Iaccarino L, Doria A (2012) Genes, epigenetic regulation and environmental factors: which is the most relevant in developing autoimmune diseases? Autoimmun Rev 11:604–609
Davis B, Wen H, Ting J (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 29:707
Dawson M, Kouzarides T (2012) Cancer epigenetics: from mechanism to therapy. Cell 150:12–27
Dueger EL, House JK, Heithoff DM, Mahan MJ (2001) Salmonella DNA adenine methylase mutants elicit protective immune responses to homologous and heterologous serovars in chickens. Infect Immun 69:7950–7954
Dueger EL, House JK, Heithoff DM, Mahan MJ (2003a) Salmonella DNA adenine methylase mutants prevent colonization of newly hatched chickens by homologous and heterologous serovars. Int J Food Microbiol 80:153–159
Dueger EL, House JK, Heithoff DM, Mahan MJ (2003b) Salmonella DNA adenine methylase mutants elicit early and late onset protective immune responses in calves. Vaccine 21:3249–3258
Elinav E, Nowarski R, Thaiss C, Hu B, Jin C, Flavell R (2013) Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer 13:759–771
Esteller M (2008) Epigenetics in cancer. N Engl J Med 358:1148–1159
Fälker S, Schilling J, Schmidt M, Heusipp G (2007) Overproduction of DNA adenine methyltransferase alters motility, invasion, and the lipopolysaccharide O-antigen composition of Yersinia enterocolitica. Infect Immun 75:4990–4997
Fälker S, Schmidt M, Heusipp G (2005) DNA methylation in Yersinia enterocolitica: role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors. Microbiology 151:2291–2299
Fälker S, Schmidt M, Heusipp G (2006) Altered Ca2+ regulation of Yop secretion in Yersinia enterocolitica after DNA adenine methyltransferase overproduction is mediated by Clp-dependent degradation of LcrG. J Bacteriol 188:7072
Fang G, Munera D, Friedman D, Mandlik A, Chao M, Banerjee O, Feng Z, Losic B, Mahajan M, Jabado O (2012) Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat Biotechnol 30:1232–1239
Feinberg A, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4:143–153
Fernandez A, Esteller M (2010) Viral epigenomes in human tumorigenesis. Oncogene 29:1405–1420
Fernandez A, Rosales C, Lopez-Nieva P, Graña O, Ballestar E, Ropero S, Espada J, Melo S, Lujambio A, Fraga M (2009) The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res 19:438–451
Furuta Y, Namba-Fukuyo H, Shibata T, Nishiyama T, Shigenobu S, Suzuki Y, Sugano S, Hasebe M, Kobayashi I (2014) Methylome diversification through changes in DNA methyltransferase sequence specificity. PLoS Genet 10:e1004272
Galindo C, Rosenzweig J, Kirtley M, Chopra A (2011) Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human yersiniosis. J Pathog 2011:1–16
Garagnani P, Pirazzini C, Franceschi C (2013) Colorectal cancer microenvironment: among nutrition, gut microbiota, inflammation and epigenetics. Curr Pharm Des 19:765–778
Garcia-Del Portillo F, Pucciarelli MG, Casadesus J (1999) DNA adenine methylase mutants of Salmonella typhimurium show defects in protein secretion, cell invasion, and M cell cytotoxicity. Proc Natl Acad Sci U S A 96:11578–11583
Gilliss D, Cronquist A, Cartter M, Tobin-D’Angelo M, Blythe D, Smith K, Lathrop S, Birkhead G, Cieslak P (2011) Vital signs: incidence and trends of infection with pathogens transmitted commonly through food—foodborne diseases active surveillance Network, 10 U.S. Sites, 1996–2010. Morb Mortal Wkly Rep 60:749–755
Gilmer L (2015) Human papillomavirus vaccine update. Prim Care Clin Off Pract 42:17–32
Gómez-Díaz E, Jordà M, Peinado M, Rivero A (2012) Epigenetics of host–pathogen interactions: the road ahead and the road behind. PLoS Pathog 8:e1003007
Gonzalez D, Kozdon J, McAdams H, Shapiro L, Collier J (2014) The functions of DNA methylation by CcrM in Caulobacter crescentus: a global approach. Nucleic Acids Res 42:3720–3735
Grewal P, Aziz P, Uchiyama S, Rubio G, Lardone R, Le D, Varki N, Nizet V, Marth J (2013) Inducing host protection in pneumococcal sepsis by preactivation of the Ashwell-Morell receptor. Proc Natl Acad Sci U S A 110:20218–20223
Grimm D, Thimme R, Blum H (2011) HBV life cycle and novel drug targets. Hepatol Int 5:644–653
Grivennikov S, Greten F, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883–899
Haggard M (2008) Otitis media: prospects for prevention. Vaccine 26:G20–G24
Hale W, Van der Woude M, Low D (1994) Analysis of nonmethylated GATC sites in the Escherichia coli chromosome and identification of sites that are differentially methylated in response to environmental stimuli. J Bacteriol 176:3438–3441
Hammerschmidt W (2015) The epigenetic life cycle of Epstein–Barr virus. Curr Top Microbiol Immunol 390(Pt 1):103–117
Hartland E, Leong J (2013) Enteropathogenic and enterohemorrhagic E. coli: ecology, pathogenesis, and evolution. Front Cell Infect Microbiol 3:15–20
He L, Hannon G (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531
Heithoff D, Badie G, Julio S, Enioutina E, Daynes R, Sinsheimer R, Mahan M (2007) In vivo-selected mutations in methyl-directed mismatch repair suppress the virulence attenuation of Salmonella dam mutant strains following intraperitoneal, but not oral, infection of naïve mice. J Bacteriol 189:4708–4717
Heithoff DM, Enioutina EY, Bareyan D, Daynes RA, Mahan MJ (2008) Conditions that diminish myeloid-derived suppressor cell activities stimulate cross-protective immunity. Infect Immun 76:5191–5199
Heithoff DM, Enioutina EY, Daynes RA, Sinsheimer RL, Low DA, Mahan MJ (2001) Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect Immun 69:6725–6730
Heithoff D, House J, Thomson P, Mahan M (2015) Development of a Salmonella cross-protective vaccine for food animal production systems. Vaccine 33:100–107
Heithoff DM, Shimp WR, House JK, Xie Y, Weimer BC, Sinsheimer RL, Mahan MJ (2012) Intraspecies variation in the emergence of hyperinfectious bacterial strains in nature. PLoS Pathog 8:e1002647
Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284:967–970
Helgesen E, Fossum-Raunehaug S, Sætre F, Schink K, Skarstad K (2015) Dynamic Escherichia coli SeqA complexes organize the newly replicated DNA at a considerable distance from the replisome. Nucleic Acids Res 43:2730–2743
Herceg Z, Lambert M-P, van Veldhoven K, Demetriou C, Vineis P, Smith M, Straif K, Wild C (2013) Towards incorporating epigenetic mechanisms into carcinogen identification and evaluation. Carcinogenesis 34:1955–1967
Herman G, Modrich P (1982) Escherichia coli dam methylase. Physical and catalytic properties of the homogeneous enzyme. J Biol Chem 257:2605–2612
Heusipp G, Fälker S, Schmidt M (2007) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 297:1–7
Huang J, Wang Y, Guo Y, Sun S (2010) Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus–related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 52:60–70
Iyer R, Pluciennik A, Burdett V, Modrich P (2006) DNA mismatch repair: functions and mechanisms. Chem Rev 106:302–323
Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254
Jakomin M, Chessa D, Bäumler A, Casadesús J (2008) Regulation of the Salmonella enterica std fimbrial operon by DNA adenine methylation, SeqA, and HdfR. J Bacteriol 190:7406–7413
Jones P (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492
Jones P, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070
Joshi M, Magnan D, Montminy T, Lies M, Stepankiw N, Bates D (2013) Regulation of sister chromosome cohesion by the replication fork tracking protein SeqA. PLoS Genet 9:e1003673
Julio S, Heithoff D, Provenzano D, Klose K, Sinsheimer R, Low D, Mahan M (2001) DNA Adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69:7610–7615
Julio S, Heithoff D, Sinsheimer R, Low D, Mahan M (2002) DNA adenine methylase overproduction in Yersinia pseudotuberculosis alters YopE expression and secretion and host immune responses to infection. Infect Immun 70:1006–1009
Jung J, Arora P, Pagano J, Jang K (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
Kahramanoglou C, Prieto A, Khedkar S, Haase B, Gupta A, Benes V, Fraser G, Luscombe N, Seshasayee A (2012) Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription. Nat Comm 3:886
Kaise M, Yamasaki T, Yonezawa J, Miwa J, Ohta Y, Tajiri H (2008) CpG island hypermethylation of tumor-tuppressor genes in H. pylori-infected non-Neoplastic gastric mucosa is linked with gastric cancer risk. Helicobacter 13:35–41
Kajitani N, Satsuka A, Kawate A, Sakai H (2012) Productive lifecycle of human papillomaviruses that depends upon squamous epithelial differentiation. Front Microbiol 3:1–12
Kang S, Lee H, Han J, Hwang D (1999) Interaction of SeqA and Dam methylase on the hemimethylated origin of Escherichia coli chromosomal DNA replication. J Biol Chem 274:11463–11468
Kew MC (2011) Hepatitis B virus x protein in the pathogenesis of hepatitis B virus-induced hepatocellular carcinoma. J Gastroenterol Hepatol 26:144–152
Khor B, Gardet A, Xavier R (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474:307–317
Knights D, Lassen K, Xavier R (2013) Advances in inflammatory bowel disease pathogenesis: linking host genetics and the microbiome. Gut 62:1505–1510
Kobayashi I, Nobusato A, Kobayashi-Takahashi N, Uchiyama I (1999) Shaping the genome–restriction–modification systems as mobile genetic elements. Curr Opin Genet Dev 9:649–656
Korzeniewski N, Spardy N, Duensing A, Duensing S (2011) Genomic instability and cancer: lessons learned from human papillomaviruses. Cancer Lett 305:113–122
Kostic A, Xavier R, Gevers D (2014) The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146:1489–1499
Kubicek-Sutherland J, Heithoff D, Ersoy S, Shimp W, Mahan M (2014) Immunization with a DNA adenine methylase over-producing Yersinia pseudotuberculosis vaccine confers robust cross-protection against heterologous pathogenic serotypes. Vaccine 32:1451–1459
Kumar R, Mukhopadhyay A, Ghosh P, Rao D (2012) Comparative transcriptomics of H. pylori strains AM5, SS1 and their hpyAVIBM deletion mutants: possible roles of cytosine methylation. PLoS One 7(8):e42303
Laurson J, Khan S, Chung R, Cross K, Raj K (2010) Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein. Carcinogenesis 31:918–926
Liu L, Li Y, Tollefsbol T (2008) Gene-environment interactions and epigenetic basis of human diseases. Curr Issues Mol Biol 10:25
Løbner-Olesen A, Marinus M, Hansen F (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci U S A 100:4672–4677
Løbner-Olesen A, Skovgaard O, Marinus M (2005) Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8:154–160
López-Garrido J, Casadesús J (2010) Regulation of Salmonella enterica pathogenicity island 1 by DNA adenine methylation. Genetics 184:637–649
López-Garrido J, Casadesús J (2012) Crosstalk between virulence loci: regulation of Salmonella enterica pathogenicity island 1 (SPI-1) by products of the std fimbrial operon. PLoS One 7:e30499
Low D, Casadesús J (2008) Clocks and switches: bacterial gene regulation by DNA adenine methylation. Curr Opin Microbiol 11:106–112
Low D, Weyand N, Mahan M (2001) Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69:7197–7204
Lu M, Campbell J, Boye E, Kleckner N (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77:413–426
Luo G-Z, Blanco M, Greer E, He C, Shi Y (2015) DNA N6-methyladenine: a new epigenetic mark in eukaryotes? Nat Rev Mol Cell Biol 16:705–710
Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, Arii K, Kaneda A, Tsukamoto T, Tatematsu M (2006) High levels of aberrant DNA methylation in Helicobacter pylori–infected gastric mucosae and its possible association with gastric cancer risk. Clin Can Res 12:989–995
Mahan MJ, Kubicek-Sutherland JZ, Heithoff DM (2013) Rise of the microbes. Virulence 4:213–222
Mahan M, Sinsheimer R, Shimp W, Heithoff D (2010) Covert operations: the adaptable plan of attack deployed by pathogenic bacteria. In: Maloy S, Hughes K, Casadesús J (eds) The lure of bacterial genetics: a tribute to John Roth. American Society for Microbiology Press, Washington, DC, pp 185–200
Marazzi I, Ho J, Kim J, Manicassamy B, Dewell S, Albrecht R, Seibert C, Schaefer U, Jeffrey K, Prinjha R (2012) Suppression of the antiviral response by an influenza histone mimic. Nature 483:428–433
Marczynski G, Shapiro L (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56:625–656
Marinus M, Casadesús J (2009) Roles of DNA adenine methylation in host–pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol Rev 33:488–503
Marinus M, Morris N (1974) Biological function for 6-methyladenine residues in the DNA of Escherichia coli K12. J Mol Biol 85:309–322
McAdams H, Shapiro L (2003) A bacterial cell-cycle regulatory network operating in time and space. Science 301:1874–1877
Meselson M, Yuan R, Heywood J (1972) Restriction and modification of DNA. Annu Rev Biochem 41:447–466
Mohler V, Heithoff D, Mahan M, Hornitzky M, Thomson P, House J (2012) Development of a novel in-water vaccination protocol for DNA adenine methylase deficient Salmonella enterica serovar Typhimurium vaccine in adult sheep. Vaccine 30:1481–1491
Mohler VL, Heithoff DM, Mahan MJ, Walker KH, Hornitzky MA, Gabor L, Thomson PC, Thompson A, House JK (2011) Protective immunity conferred by a DNA adenine methylase deficient Salmonella enterica serovar Typhimurium vaccine when delivered in-water to sheep challenged with Salmonella enterica serovar Typhimurium. Vaccine 29:3571–3582
Mohler V, Heithoff D, Mahan M, Walker K, Hornitzky M, McConnell C, Shum L, House J (2006) Cross-protective immunity in calves conferred by a DNA adenine methylase deficient Salmonella enterica serovar Typhimurium vaccine. Vaccine 24:1339
Mohler V, Heithoff D, Mahan M, Walker K, Hornitzky M, Shum L, Makin K, House J (2008) Cross-protective immunity conferred by a DNA adenine methylase deficient Salmonella enterica serovar Typhimurium vaccine in calves challenged with Salmonella serovar Newport. Vaccine 26:1751–1758
Moore P, Chang Y (2010) Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer 10:878–889
Münger K, Baldwin A, Edwards K, Hayakawa H, Nguyen C, Owens M, Grace M, Huh K (2004) Mechanisms of human papillomavirus-induced oncogenesis. J Virol 78:11451–11460
Murphy K, Ritchie J, Waldor M, Løbner-Olesen A, Marinus M (2008) Dam methyltransferase is required for stable lysogeny of the Shiga toxin (Stx2)-encoding bacteriophage 933W of enterohemorrhagic Escherichia coli O157: H7. J Bacteriol 190:438–441
Nakajima T, Maekita T, Oda I, Gotoda T, Yamamoto S, Umemura S, Ichinose M, Sugimura T, Ushijima T, Saito D (2006) Higher methylation levels in gastric mucosae significantly correlate with higher risk of gastric cancers. Cancer Epidemiol Biomarkers Prev 15:2317–2321
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 70:1430–1440
Noyer-Weidner M, Trautner T (1992) Methylation of DNA in prokaryotes. In: Jost JP, Saluz H (eds) DNA methylation: molecular biology and biological significance. Birkhauser Basel, Switzerland, pp 39–108
Odumade O, Hogquist K, Balfour H (2011) Progress and problems in understanding and managing primary Epstein-Barr virus infections. Clin Microbiol Rev 24:193–209
Palmer B, Marinus M (1994) The dam and dcm strains of Escherichia coli—a review. Gene 143:1–12
Parsonnet J (1999) Microbes and malignancy: infection as a cause of human cancers. Oxford University Press, USA
Paschos K, Allday M (2010) Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol 18:439–447
Pennini M, Pai R, Schultz D, Boom W, Harding C (2006) Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-γ-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 176:4323–4330
Polk D, Peek R (2010) Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 10:403–414
Pollicino T, Belloni L, Raffa G, Pediconi N, Squadrito G, Raimondo G, Levrero M (2006) Hepatitis B virus replication is regulated by the acetylation status of hepatitis B virus cccDNA-bound H3 and H4 histones. Gastroenterology 130:823–837
Portela A, Esteller M (2010) Epigenetic modifications and human disease. Nat Biotechnol 28:1057–1068
Protzer U (2015) Hepatitis: epigenetic control of HBV by HBx protein-releasing the break? Nat Rev Gastroenterol Hepatol 12. doi:10.1016/j.jhep.2015.1006.1023
Pucciarelli M, Prieto A, Casadesús J, Garcıa-del Portillo F (2002) Envelope instability in DNA adenine methylase mutants of Salmonella enterica. Microbiology 148:1171–1182
Pukkila P, Peterson J, Herman G, Modrich P, Meselson M (1983) Effects of high levels of DNA adenine methylation on methyl-directed mismatch repair in Escherichia coli. Genetics 104:571–582
Quasdorff M, Hösel M, Odenthal M, Zedler U, Bohne F, Gripon P, Dienes HP, Drebber U, Stippel D, Goeser T (2008) A concerted action of HNF4α and HNF1α links hepatitis B virus replication to hepatocyte differentiation. Cell Microbiol 10:1478–1490
Reisenauer A, Kahng L, McCollum S, Shapiro L (1999) Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181:5135–5139
Rickinson A, Long H, Palendira U, Münz C, Hislop A (2014) Cellular immune controls over Epstein–Barr virus infection: new lessons from the clinic and the laboratory. Trends Immunol 35:159–169
Ringquist S, Smith C (1992) The Escherichia coli chromosome contains specific, unmethylated dam and dcm sites. Proc Natl Acad Sci U S A 89:4539–4543
Rivière L, Gerossier L, Ducroux A, Dion S, Deng Q, Michel M-L, Buendia M-A, Hantz O, Neuveut C (2015) HBx relieves chromatin-mediated transcriptional repression of hepatitis B viral cccDNA involving SETDB1 histone methyltransferase. J Hepatol 63:1093–1102
Roberts D, Hoopes B, McClure W, Kleckner N (1985) IS10 transposition is regulated by DNA adenine methylation. Cell 43:117–130
Roberts R, Macelis D (2001) REBASE—restriction enzymes and methylases. Nucleic Acids Res 29:268–269
Robertson G, Reisenauer A, Wright R, Jensen R, Jensen A, Shapiro L, Roop R (2000) The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182:3482–3489
Romani M, Pistillo M, Banelli B (2015) Environmental epigenetics: crossroad between public health, lifestyle, and cancer prevention. BioMed Res Int 2015:587983
Saito Y, Hibino S, Saito H (2014) Alterations of epigenetics and microRNA in hepatocellular carcinoma. Hepatol Res 44:31–42
Sánchez-Romero M, Cota I, Casadesús J (2015) DNA methylation in bacteria: from the methyl group to the methylome. Curr Opin Microbiol 25:9–16
Sarnacki S, Marolda C, Llana M, Giacomodonato M, Valvano M, Cerquetti M (2009) Dam methylation controls O-antigen chain length in Salmonella enterica serovar enteritidis by regulating the expression of Wzz protein. J Bacteriol 191:6694–6700
Sato F, Tsuchiya S, Meltzer S, Shimizu K (2011) MicroRNAs and epigenetics. Febs J 278:1598–1609
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17:7–15
Schett G, Elewaut D, McInnes I, Dayer J-M, Neurath M (2013) How cytokine networks fuel inflammation: toward a cytokine-based disease taxonomy. Nat Med 19:822–824
Schleithoff C, Völter-Mahlknecht S, Dahmke I, Mahlknecht U (2012) On the epigenetics of vascular regulation and disease. Clin Epigenetics 4. http://www.clinicalepigeneticsjournal.com/content/4/1/7
Schmeinck A (2011) Acquisition and loss of chromatin modifications during an Epstein-Barr Virus infection. Dissertaion, Ludwig Maximilians-University, Munich
Schweitzer A, Horn J, Mikolajczyk R, Krause G, Ott JJ (2015) Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 246:1546–1555
Shell S, Prestwich E, Baek S-H, Shah R, Sassetti C, Dedon P, Fortune S (2013) DNA methylation impacts gene expression and ensures hypoxic survival of Mycobacterium tuberculosis. PLoS Pathog 9:e1003419
Shenderov B (2012) Gut indigenous microbiota and epigenetics. Microb Ecol Health Dis 23. doi:10.3402/mehd.v23i0.17195
Shtrichman R, Heithoff D, Mahan M, Samuel C (2002) Tissue selectivity of interferon-stimulated gene expression in mice infected with Dam+ versus Dam− Salmonella enterica serovar Typhimurium strains. Infect Immun 70:5579–5588
Simon R, Heithoff D, Mahan M, Samuel C (2007) Comparison of tissue-selective proinflammatory gene induction in mice infected with wild-type, DNA adenine methylase-deficient, and flagellin-deficient Salmonella enterica. Infect immun 75:5627–5639
Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5:a012922
Smith Z, Meissner A (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14:204–220
Srikhanta Y, Fox K, Jennings M (2010) The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat Rev Microbiol 8:196–206
Steenbergen R, Snijders P, Heideman D, Meijer C (2014) Clinical implications of (epi) genetic changes in HPV-induced cervical precancerous lesions. Nat Rev Cancer 14:395–405
Stein R (2011) Epigenetics—the link between infectious diseases and cancer. JAMA 305:1484–1485
Stilling R, Dinan T, Cryan J (2014) Microbial genes, brain & behaviour–epigenetic regulation of the gut–brain axis. Genes Brain Behav 13:69–86
Sun C, Reimers L, Burk R (2011) Methylation of HPV16 genome CpG sites is associated with cervix precancer and cancer. Gynecol Oncol 121:59–63
Tauxe R (2015) Epidemiology of yersiniosis. In: Calderwood SB, section editor, Bloom A, deputy editor (eds) http://www.uptodate.com/contents/epidemiology-of-yersiniosis. Accessed 14 Aug 2015
Tavazoie S, Church G (1998) Quantitative whole-genome analysis of DNA-protein interactions by in vivo methylase protection in E. coli. Nat Biotechnol 16:566–571
Taylor V, Titball R, Oyston P (2005) Oral immunization with a dam mutant of Yersinia pseudotuberculosis protects against plague. Microbiology 151:1919–1926
Thompson P, Kurzrock R (2004) Epstein-Barr virus and cancer. Clin Can Res 10:803–821
Thorley-Lawson D (2015) EBV persistence—Introducing the virus. In: Münz C (ed) Epstein Barr Virus Volume 1. Springer, Switzerland, pp 151–209
Tian Y, Yang W, Song J, Wu Y, Ni B (2013) Hepatitis B virus X protein-induced aberrant epigenetic modifications contributing to human hepatocellular carcinoma pathogenesis. Mol Cell Biol 33:2810–2816
Tsai C-L, Li H-P, Lu Y-J, Hsueh C, Liang Y, Chen C-L, Tsao S, Tse K-P, Yu J-S, Chang Y-S (2006) Activation of DNA methyltransferase 1 by EBV LMP1 involves c-Jun NH2-terminal kinase signaling. Cancer Res 66:11668–11676
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 Can Res 18:923–929
Van Vliet J, Oates N, Whitelaw E (2007) Epigenetic mechanisms in the context of complex diseases. Cell Mol Life Sci 64:1531–1538
Vasu K, Nagaraja V (2013) Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 77:53–72
Ventham N, Kennedy N, Nimmo E, Satsangi J (2013) Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology 145:293–308
Wang M, Church G (1992) A whole genome approach to in vivo DNA-protein interactions in E. coli. Nature 360:606–610
Wilson A (2008) Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 79:1514–1519
Wilson G, Lechner M, Köferle A, Caren H, Butcher L, Feber A, Fenton T, Jay A, Boshoff C, Beck S (2013) Integrated virus-host methylome analysis in head and neck squamous cell carcinoma. Epigenetics 8:953–961
Wion D, Casadesús J (2006) N6-methyl-adenine: an epigenetic signal for DNA–protein interactions. Nat Rev Microbiol 4:183–192
Woellmer A, Arteaga-Salas J, Hammerschmidt W (2012) BZLF1 governs CpG-methylated chromatin of Epstein-Barr virus reversing epigenetic repression. PLoS Pathog 8:e1002902
World Health Organization (2006) http://www.who.int/csr/resources/publications/Brucellosis.pdf. In: Corbel MJ, Elberg SS, Cosivi O (eds) Geneva, pp 1–102
World Health Organization (2014a) Global tuberculosis report 2014. http://apps.who.int/iris/bitstream/10665/137094/1/9789241564809_eng.pdf?ua=1. WHO Press, Geneva, pp 1–171
World Health Organization (2014b) World cancer report, 2014. In: Stewart B, Wild C (eds) WHO Report. WHO Press, Geneva
World Health Organization (2015) Cancer. Fact sheet No. 297. WHO Press, Geneva
Wroblewski L, Peek R, Wilson K (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739
Yang W, Aziz P, Heithoff D, Mahan M, Smith J, Marth J (2015) An intrinsic mechanism of secreted protein aging and turnover. Proc Natl Acad Sci U S A 112:13657–13662
Yao S, He Z, Chen C (2015) CRISPR/Cas9-mediated genome editing of epigenetic factors for cancer therapy. Hum Gene Ther 26:463–471
Yoshida T, Kato J, Maekita T, Yamashita S, Enomoto S, Ando T, Niwa T, Deguchi H, Ueda K, Inoue I (2013) Altered mucosal DNA methylation in parallel with highly active Helicobacter pylori-related gastritis. Gastric Cancer 16:488–497
Youngblood B, Davis C, Ahmed R (2010) Making memories that last a lifetime: heritable functions of self-renewing memory CD8 T cells. Int Immunol. doi:10.1093/intimm/dxq437
zur Hausen H (2001) Oncogenic DNA viruses. Oncogene 20:7820–7823
zur Hausen H (2009) The search for infectious causes of human cancers: where and why. Virology 392:1–10
Acknowledgments
The scope of this chapter and its space limitations have unfortunately resulted in the inability to separately cite many of the original publications that have contributed substantially to the field. We sincerely apologize to the authors of these publications. This work was supported by G. Harold & Leila Y. Mathers Foundation and Santa Barbara Cottage Hospital Research Program (to M.J.M).
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Mahan, M.J., Heithoff, D.M., Barnes V, L., Sinsheimer, R.L. (2017). Epigenetic Programming by Microbial Pathogens and Impacts on Acute and Chronic Disease. 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_5
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