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Epigenetic Programming by Microbial Pathogens and Impacts on Acute and Chronic Disease

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Epigenetics of Infectious Diseases

Part of the book series: Epigenetics and Human Health ((EHH))

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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bannister A, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baylin S, Herman J (2000) DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 16:168–174

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bierne H, Hamon M, Cossart P (2012) Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2:a010272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bigger C, Murray K, Murray N (1973) Recognition sequence of a restriction enzyme. Nature 244:7–10

    CAS  Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

    Article  CAS  PubMed  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    Article  CAS  PubMed  Google Scholar 

  • Boye E, Marinus M, Løbner-Olesen A (1992) Quantitation of Dam methyltransferase in Escherichia coli. J Bacteriol 174:1682–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Casadesús J, D’Ari R (2002) Memory in bacteria and phage. Bioessays 24:512–518

    Article  PubMed  CAS  Google Scholar 

  • Casadesús J, Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70:830–856

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Centers for Disease Control and Prevention (2012) Human papillomavirus-associated cancers-United States, 2004–2008. Morb Mortal Wkly Rep 61:258

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Davis B, Wen H, Ting J (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 29:707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson M, Kouzarides T (2012) Cancer epigenetics: from mechanism to therapy. Cell 150:12–27

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Esteller M (2008) Epigenetics in cancer. N Engl J Med 358:1148–1159

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Feinberg A, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4:143–153

    Article  CAS  PubMed  Google Scholar 

  • Fernandez A, Esteller M (2010) Viral epigenomes in human tumorigenesis. Oncogene 29:1405–1420

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galindo C, Rosenzweig J, Kirtley M, Chopra A (2011) Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human yersiniosis. J Pathog 2011:1–16

    Article  Google Scholar 

  • Garagnani P, Pirazzini C, Franceschi C (2013) Colorectal cancer microenvironment: among nutrition, gut microbiota, inflammation and epigenetics. Curr Pharm Des 19:765–778

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Gilmer L (2015) Human papillomavirus vaccine update. Prim Care Clin Off Pract 42:17–32

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimm D, Thimme R, Blum H (2011) HBV life cycle and novel drug targets. Hepatol Int 5:644–653

    Article  PubMed  PubMed Central  Google Scholar 

  • Grivennikov S, Greten F, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haggard M (2008) Otitis media: prospects for prevention. Vaccine 26:G20–G24

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammerschmidt W (2015) The epigenetic life cycle of Epstein–Barr virus. Curr Top Microbiol Immunol 390(Pt 1):103–117

    CAS  PubMed  Google Scholar 

  • Hartland E, Leong J (2013) Enteropathogenic and enterohemorrhagic E. coli: ecology, pathogenesis, and evolution. Front Cell Infect Microbiol 3:15–20

    Article  PubMed  PubMed Central  Google Scholar 

  • He L, Hannon G (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284:967–970

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herman G, Modrich P (1982) Escherichia coli dam methylase. Physical and catalytic properties of the homogeneous enzyme. J Biol Chem 257:2605–2612

    CAS  PubMed  Google Scholar 

  • Heusipp G, Fälker S, Schmidt M (2007) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 297:1–7

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Iyer R, Pluciennik A, Burdett V, Modrich P (2006) DNA mismatch repair: functions and mechanisms. Chem Rev 106:302–323

    Article  CAS  PubMed  Google Scholar 

  • Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones P (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492

    Article  CAS  PubMed  Google Scholar 

  • Jones P, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kew MC (2011) Hepatitis B virus x protein in the pathogenesis of hepatitis B virus-induced hepatocellular carcinoma. J Gastroenterol Hepatol 26:144–152

    Article  CAS  PubMed  Google Scholar 

  • Khor B, Gardet A, Xavier R (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474:307–317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knights D, Lassen K, Xavier R (2013) Advances in inflammatory bowel disease pathogenesis: linking host genetics and the microbiome. Gut 62:1505–1510

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Korzeniewski N, Spardy N, Duensing A, Duensing S (2011) Genomic instability and cancer: lessons learned from human papillomaviruses. Cancer Lett 305:113–122

    Article  CAS  PubMed  Google Scholar 

  • Kostic A, Xavier R, Gevers D (2014) The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146:1489–1499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Li Y, Tollefsbol T (2008) Gene-environment interactions and epigenetic basis of human diseases. Curr Issues Mol Biol 10:25

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Løbner-Olesen A, Skovgaard O, Marinus M (2005) Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8:154–160

    Article  PubMed  CAS  Google Scholar 

  • López-Garrido J, Casadesús J (2010) Regulation of Salmonella enterica pathogenicity island 1 by DNA adenine methylation. Genetics 184:637–649

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Low D, Casadesús J (2008) Clocks and switches: bacterial gene regulation by DNA adenine methylation. Curr Opin Microbiol 11:106–112

    Article  CAS  PubMed  Google Scholar 

  • Low D, Weyand N, Mahan M (2001) Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69:7197–7204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu M, Campbell J, Boye E, Kleckner N (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77:413–426

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mahan MJ, Kubicek-Sutherland JZ, Heithoff DM (2013) Rise of the microbes. Virulence 4:213–222

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marczynski G, Shapiro L (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56:625–656

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marinus M, Morris N (1974) Biological function for 6-methyladenine residues in the DNA of Escherichia coli K12. J Mol Biol 85:309–322

    Article  CAS  PubMed  Google Scholar 

  • McAdams H, Shapiro L (2003) A bacterial cell-cycle regulatory network operating in time and space. Science 301:1874–1877

    Article  CAS  PubMed  Google Scholar 

  • Meselson M, Yuan R, Heywood J (1972) Restriction and modification of DNA. Annu Rev Biochem 41:447–466

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer B, Marinus M (1994) The dam and dcm strains of Escherichia coli—a review. Gene 143:1–12

    Article  CAS  PubMed  Google Scholar 

  • Parsonnet J (1999) Microbes and malignancy: infection as a cause of human cancers. Oxford University Press, USA

    Google Scholar 

  • Paschos K, Allday M (2010) Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol 18:439–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Polk D, Peek R (2010) Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 10:403–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Portela A, Esteller M (2010) Epigenetic modifications and human disease. Nat Biotechnol 28:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Reisenauer A, Kahng L, McCollum S, Shapiro L (1999) Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181:5135–5139

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Roberts D, Hoopes B, McClure W, Kleckner N (1985) IS10 transposition is regulated by DNA adenine methylation. Cell 43:117–130

    Article  CAS  PubMed  Google Scholar 

  • Roberts R, Macelis D (2001) REBASE—restriction enzymes and methylases. Nucleic Acids Res 29:268–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romani M, Pistillo M, Banelli B (2015) Environmental epigenetics: crossroad between public health, lifestyle, and cancer prevention. BioMed Res Int 2015:587983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saito Y, Hibino S, Saito H (2014) Alterations of epigenetics and microRNA in hepatocellular carcinoma. Hepatol Res 44:31–42

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato F, Tsuchiya S, Meltzer S, Shimizu K (2011) MicroRNAs and epigenetics. Febs J 278:1598–1609

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skarstad K, Katayama T (2013) Regulating DNA replication in bacteria. Cold Spring Harb Perspect Biol 5:a012922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith Z, Meissner A (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14:204–220

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stein R (2011) Epigenetics—the link between infectious diseases and cancer. JAMA 305:1484–1485

    Article  CAS  PubMed  Google Scholar 

  • Stilling R, Dinan T, Cryan J (2014) Microbial genes, brain & behaviour–epigenetic regulation of the gut–brain axis. Genes Brain Behav 13:69–86

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Taylor V, Titball R, Oyston P (2005) Oral immunization with a dam mutant of Yersinia pseudotuberculosis protects against plague. Microbiology 151:1919–1926

    Article  CAS  PubMed  Google Scholar 

  • Thompson P, Kurzrock R (2004) Epstein-Barr virus and cancer. Clin Can Res 10:803–821

    Article  CAS  Google Scholar 

  • Thorley-Lawson D (2015) EBV persistence—Introducing the virus. In: Münz C (ed) Epstein Barr Virus Volume 1. Springer, Switzerland, pp 151–209

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Van Vliet J, Oates N, Whitelaw E (2007) Epigenetic mechanisms in the context of complex diseases. Cell Mol Life Sci 64:1531–1538

    Article  PubMed  CAS  Google Scholar 

  • Vasu K, Nagaraja V (2013) Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 77:53–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Church G (1992) A whole genome approach to in vivo DNA-protein interactions in E. coli. Nature 360:606–610

    Article  CAS  PubMed  Google Scholar 

  • Wilson A (2008) Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 79:1514–1519

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wion D, Casadesús J (2006) N6-methyl-adenine: an epigenetic signal for DNA–protein interactions. Nat Rev Microbiol 4:183–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woellmer A, Arteaga-Salas J, Hammerschmidt W (2012) BZLF1 governs CpG-methylated chromatin of Epstein-Barr virus reversing epigenetic repression. PLoS Pathog 8:e1002902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • World Health Organization (2015) Cancer. Fact sheet No. 297. WHO Press, Geneva

    Google Scholar 

  • Wroblewski L, Peek R, Wilson K (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao S, He Z, Chen C (2015) CRISPR/Cas9-mediated genome editing of epigenetic factors for cancer therapy. Hum Gene Ther 26:463–471

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • zur Hausen H (2001) Oncogenic DNA viruses. Oncogene 20:7820–7823

    Article  PubMed  CAS  Google Scholar 

  • zur Hausen H (2009) The search for infectious causes of human cancers: where and why. Virology 392:1–10

    Article  PubMed  CAS  Google Scholar 

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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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