Bacterial DNA methyltransferase: A key to the epigenetic world with lessons learned from proteobacteria

Epigenetics modulates expression levels of various important genes in both prokaryotes and eukaryotes. These epigenetic traits are heritable without any change in genetic DNA sequences. DNA methylation is a universal mechanism of epigenetic regulation in all kingdoms of life. In bacteria, DNA methylation is the main form of epigenetic regulation and plays important roles in affecting clinically relevant phenotypes, such as virulence, host colonization, sporulation, biofilm formation et al. In this review, we survey bacterial epigenomic studies and focus on the recent developments in the structure, function, and mechanism of several highly conserved bacterial DNA methylases. These methyltransferases are relatively common in bacteria and participate in the regulation of gene expression and chromosomal DNA replication and repair control. Recent advances in sequencing techniques capable of detecting methylation signals have enabled the characterization of genome-wide epigenetic regulation. With their involvement in critical cellular processes, these highly conserved DNA methyltransferases may emerge as promising targets for developing novel epigenetic inhibitors for biomedical applications.

[1]  Yizhou Zhang,et al.  DNA Methyltransferase Regulates Nitric Oxide Homeostasis and Virulence in a Chronically Adapted Pseudomonas aeruginosa Strain , 2022, mSystems.

[2]  Chun-Xiao Song,et al.  Whole-genome long-read TAPS deciphers DNA methylation patterns at base resolution using PacBio SMRT sequencing technology , 2022, Nucleic acids research.

[3]  Tianhua Zhou,et al.  Fusobacterium nucleatum reduces METTL3-mediated m6A modification and contributes to colorectal cancer metastasis , 2022, Nature Communications.

[4]  R. Roberts,et al.  Beyond Restriction Modification: Epigenomic Roles of DNA Methylation in Prokaryotes. , 2021, Annual review of microbiology.

[5]  Xue-Song Zhang,et al.  Discovering multiple types of DNA methylation from bacteria and microbiome using nanopore sequencing , 2021, Nature Methods.

[6]  K. Militello,et al.  DNA cytosine methyltransferase enhances viability during prolonged stationary phase in Escherichia coli. , 2020, FEMS microbiology letters.

[7]  V. de Crécy-Lagard,et al.  Detection of preQ0 deazaguanine modifications in bacteriophage CAjan DNA using Nanopore sequencing reveals same hypermodification at two distinct DNA motifs , 2020, Nucleic acids research.

[8]  K. Seib,et al.  Epigenetic Regulation of Virulence and Immunoevasion by Phase-Variable Restriction-Modification Systems in Bacterial Pathogens. , 2020, Annual review of microbiology.

[9]  R. Blumenthal,et al.  Beta class amino methyltransferases from bacteria to humans: evolution and structural consequences , 2020, Nucleic acids research.

[10]  D. Rao,et al.  Tetramerization at low pH licenses DNA methylation activity of M.HpyAXI in the presence of acid stress. , 2020, Journal of molecular biology.

[11]  De-Ming Kong,et al.  Terminal deoxynucleotidyl transferase-activated nicking enzyme amplification reaction for specific and sensitive detection of DNA methyltransferase and polynucleotide kinase. , 2019, Biosensors & bioelectronics.

[12]  J. Casadesús,et al.  The bacterial epigenome , 2019, Nature Reviews Microbiology.

[13]  A. Kasarskis,et al.  Epigenomic characterization of Clostridioides difficile finds a conserved DNA methyltransferase that mediates sporulation and pathogenesis , 2019, Nature Microbiology.

[14]  Xiaodong Cheng,et al.  The cell cycle-regulated DNA adenine methyltransferase CcrM opens a bubble at its DNA recognition site , 2019, Nature Communications.

[15]  Lei Ge,et al.  Label-free and immobilization-free photoelectrochemical biosensing strategy using methylene blue in homogeneous solution as signal probe for facile DNA methyltransferase activity assay. , 2019, Biosensors & bioelectronics.

[16]  J. Casadesús,et al.  Regulation of bistability in the std fimbrial operon of Salmonella enterica by DNA adenine methylation and transcription factors HdfR, StdE and StdF , 2019, Nucleic acids research.

[17]  A. Adewoye,et al.  Potentiation of Phase Variation in Multiple Outer-Membrane Proteins During Spread of the Hyperinvasive Neisseria meningitidis Serogroup W ST-11 Lineage , 2019, The Journal of infectious diseases.

[18]  J. Gowrishankar,et al.  A new role for Escherichia coli Dam DNA methylase in prevention of aberrant chromosomal replication , 2019, Nucleic acids research.

[19]  T. Arndt.  Crystal , 2019, Springer Reference Medizin.

[20]  Jing-Ren Zhang,et al.  Phase Variation of Streptococcus pneumoniae. , 2019, Microbiology spectrum.

[21]  D. Lehmann,et al.  Moraxella catarrhalis Restriction–Modification Systems Are Associated with Phylogenetic Lineage and Disease , 2018, Genome biology and evolution.

[22]  N. Reich,et al.  The highly specific, cell cycle–regulated methyltransferase from Caulobacter crescentus relies on a novel DNA recognition mechanism , 2018, The Journal of Biological Chemistry.

[23]  Justine Collier,et al.  The impact of DNA methylation in Alphaproteobacteria , 2018, Molecular microbiology.

[24]  J. Casadesús,et al.  Formation of phenotypic lineages in Salmonella enterica by a pleiotropic fimbrial switch , 2018, PLoS genetics.

[25]  C. Josenhans,et al.  The core genome m5C methyltransferase JHP1050 (M.Hpy99III) plays an important role in orchestrating gene expression in Helicobacter pylori , 2018, bioRxiv.

[26]  A. Kiss,et al.  Circularly permuted variants of two CG-specific prokaryotic DNA methyltransferases , 2018, PloS one.

[27]  R. Morgan,et al.  N4-cytosine DNA methylation regulates transcription and pathogenesis in Helicobacter pylori , 2018, Nucleic acids research.

[28]  K. Seib,et al.  Phasevarions of Bacterial Pathogens: Methylomics Sheds New Light on Old Enemies. , 2018, Trends in microbiology.

[29]  Yuanjian Zhang,et al.  Highly Sensitive and Quality Self-Testable Electrochemiluminescence Assay of DNA Methyltransferase Activity Using Multifunctional Sandwich-Assembled Carbon Nitride Nanosheets. , 2018, ACS applied materials & interfaces.

[30]  R. Roberts,et al.  The non-specific adenine DNA methyltransferase M.EcoGII , 2017, Nucleic acids research.

[31]  F. Lyko.  The DNA methyltransferase family: a versatile toolkit for epigenetic regulation , 2017, Nature Reviews Genetics.

[32]  Tyson A. Clark,et al.  Methylomic and phenotypic analysis of the ModH5 phasevarion of Helicobacter pylori , 2017, Scientific Reports.

[33]  P. Gao,et al.  Structural basis underlying complex assembly and conformational transition of the type I R-M system , 2017, Proceedings of the National Academy of Sciences.

[34]  S. Bentley,et al.  Phase-variable methylation and epigenetic regulation by type I restriction-modification systems. , 2017, FEMS microbiology reviews.

[35]  N. Reich,et al.  Caulobacter crescentus Cell Cycle-Regulated DNA Methyltransferase Uses a Novel Mechanism for Substrate Recognition. , 2017, Biochemistry.

[36]  Albert Jeltsch,et al.  Design of synthetic epigenetic circuits featuring memory effects and reversible switching based on DNA methylation , 2017, Nature Communications.

[37]  K. Seib,et al.  The Capricious Nature of Bacterial Pathogens: Phasevarions and Vaccine Development , 2016, Front. Immunol..

[38]  Xiaodong Cheng,et al.  DNA Base Flipping: A General Mechanism for Writing, Reading, and Erasing DNA Modifications. , 2016, Advances in experimental medicine and biology.

[39]  Patrick D Curtis,et al.  DNA methyltransferases and epigenetic regulation in bacteria. , 2016, FEMS microbiology reviews.

[40]  Naomi Attar.  Bacterial genetics: SMRT-seq reveals an epigenetic switch , 2016, Nature Reviews Microbiology.

[41]  Hongquan Zhang,et al.  Biochemical and structural characterization of a DNA N6-adenine methyltransferase from Helicobacter pylori , 2016, Oncotarget.

[42]  P. Cossart,et al.  A Lasting Impression: Epigenetic Memory of Bacterial Infections? , 2016, Cell host & microbe.

[43]  A. Fisher,et al.  Structures of human ADAR2 bound to dsRNA reveal base-flipping mechanism and basis for site selectivity , 2016, Nature Structural &Molecular Biology.

[44]  R. Roberts,et al.  Structure of Type IIL Restriction-Modification Enzyme MmeI in Complex with DNA Has Implications for Engineering New Specificities , 2016, PLoS biology.

[45]  M. Szczelkun,et al.  Structural insights into DNA sequence recognition by Type ISP restriction-modification enzymes , 2016, Nucleic acids research.

[46]  A. Goesmann,et al.  DistAMo: A Web-Based Tool to Characterize DNA-Motif Distribution on Bacterial Chromosomes , 2016, Front. Microbiol..

[47]  Christian A. Ross,et al.  A role for the bacterial GATC methylome in antibiotic stress survival , 2016, Nature Genetics.

[48]  Dongwan D. Kang,et al.  The Epigenomic Landscape of Prokaryotes , 2016, PLoS genetics.

[49]  I. Connerton,et al.  Phase variation of a Type IIG restriction-modification enzyme alters site-specific methylation patterns and gene expression in Campylobacter jejuni strain NCTC11168 , 2016, Nucleic acids research.

[50]  J. Casadesús.  Bacterial DNA Methylation and Methylomes. , 2016, Advances in experimental medicine and biology.

[51]  J. Minárovits,et al.  Patho-epigenetics of Infectious Diseases Caused by Intracellular Bacteria. , 2016, Advances in experimental medicine and biology.

[52]  A. Piekarowicz,et al.  Type III Methyltransferase M.NgoAX from Neisseria gonorrhoeae FA1090 Regulates Biofilm Formation and Interactions with Human Cells , 2015, Front. Microbiol..

[53]  J. Casadesús,et al.  Epigenetic Control of Salmonella enterica O-Antigen Chain Length: A Tradeoff between Virulence and Bacteriophage Resistance , 2015, PLoS genetics.

[54]  A. Karyagina,et al.  Role of restriction-modification systems in prokaryotic evolution and ecology , 2015, Biochemistry (Moscow).

[55]  Tyson A. Clark,et al.  A biphasic epigenetic switch controls immunoevasion, virulence and niche adaptation in non-typeable Haemophilus influenzae , 2015, Nature Communications.

[56]  Shuang-yong Xu,et al.  Structural basis of asymmetric DNA methylation and ATP-triggered long-range diffusion by EcoP15I , 2015, Nature Communications.

[57]  J. Casadesús,et al.  DNA methylation in bacteria: from the methyl group to the methylome. , 2015, Current opinion in microbiology.

[58]  R. Blumenthal,et al.  Structures of Escherichia coli DNA adenine methyltransferase (Dam) in complex with a non-GATC sequence: potential implications for methylation-independent transcriptional repression , 2015, Nucleic acids research.

[59]  Yuriy Fofanov,et al.  Mycoplasma CG- and GATC-specific DNA methyltransferases selectively and efficiently methylate the host genome and alter the epigenetic landscape in human cells , 2015, Epigenetics.

[60]  J. Lees,et al.  R–M systems go on the offensive , 2015, Nature Reviews Microbiology.

[61]  Richard J. Roberts,et al.  REBASE—a database for DNA restriction and modification: enzymes, genes and genomes , 2009, Nucleic Acids Res..

[62]  D. M. Heithoff,et al.  Development of a Salmonella cross-protective vaccine for food animal production systems. , 2015, Vaccine.

[63]  Alexander N Gorban,et al.  A random six-phase switch regulates pneumococcal virulence via global epigenetic changes , 2014, Nature Communications.

[64]  B. Marshall,et al.  Phase-variable restriction/modification systems are required for Helicobacter pylori colonization , 2014, Gut Pathogens.

[65]  Tyson A. Clark,et al.  ModM DNA methyltransferase methylome analysis reveals a potential role for Moraxella catarrhalis phasevarions in otitis media , 2014, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[66]  E. Biondi,et al.  DNA methylation in Caulobacter and other Alphaproteobacteria during cell cycle progression. , 2014, Trends in microbiology.

[67]  M. Touchon,et al.  The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts , 2014, Nucleic acids research.

[68]  Y. Brun,et al.  Identification of essential alphaproteobacterial genes reveals operational variability in conserved developmental and cell cycle systems , 2014, Molecular microbiology.

[69]  B. Weimer,et al.  Exploring bacterial epigenomics in the next-generation sequencing era: a new approach for an emerging frontier. , 2014, Trends in microbiology.

[70]  V. Barbe,et al.  Fuse or die: how to survive the loss of Dam in Vibrio cholerae , 2014, Molecular microbiology.

[71]  Bing Sun,et al.  A new strategy for methylated DNA detection based on photoelectrochemical immunosensor using Bi2S3 nanorods, methyl bonding domain protein and anti-his tag antibody. , 2014, Biosensors & bioelectronics.

[72]  H. McAdams,et al.  The functions of DNA methylation by CcrM in Caulobacter crescentus: a global approach , 2014, Nucleic acids research.

[73]  David T. F. Dryden,et al.  Type I restriction enzymes and their relatives , 2013, Nucleic acids research.

[74]  R. Simon,et al.  Cytosine DNA methylation influences drug resistance in Escherichia coli through increased sugE expression. , 2014, FEMS microbiology letters.

[75]  Tyson A. Clark,et al.  Global methylation state at base-pair resolution of the Caulobacter genome throughout the cell cycle , 2013, Proceedings of the National Academy of Sciences.

[76]  D. van Sinderen,et al.  Bacteriophage Orphan DNA Methyltransferases: Insights from Their Bacterial Origin, Function, and Occurrence , 2013, Applied and Environmental Microbiology.

[77]  V. Villeret,et al.  DNA Binding of the Cell Cycle Transcriptional Regulator GcrA Depends on N6-Adenosine Methylation in Caulobacter crescentus and Other Alphaproteobacteria , 2013, PLoS genetics.

[78]  J. Casadesús,et al.  Programmed Heterogeneity: Epigenetic Mechanisms in Bacteria , 2013, The Journal of Biological Chemistry.

[79]  Justine Collier,et al.  DNA methylation by CcrM activates the transcription of two genes required for the division of Caulobacter crescentus , 2013, Molecular microbiology.

[80]  V. Nagaraja,et al.  Diverse Functions of Restriction-Modification Systems in Addition to Cellular Defense , 2013, Microbiology and Molecular Reviews.

[81]  Tyson A. Clark,et al.  Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing , 2012, Nature Biotechnology.

[82]  Jeong-Sun Kim,et al.  Structural characterization of a modification subunit of a putative type I restriction enzyme from Vibrio vulnificus YJ016. , 2012, Acta crystallographica. Section D, Biological crystallography.

[83]  G. Verdine,et al.  Structural Origins of DNA Target Selection and Nucleobase Extrusion by a DNA Cytosine Methyltransferase* , 2012, The Journal of Biological Chemistry.

[84]  J. Casadesús,et al.  STM2209-STM2208 (opvAB): A Phase Variation Locus of Salmonella enterica Involved in Control of O-Antigen Chain Length , 2012, PloS one.

[85]  S. Krishna,et al.  Context-dependent conservation of DNA methyltransferases in bacteria , 2012, Nucleic acids research.

[86]  G. Kneale,et al.  Structural and Functional Analysis of the Symmetrical Type I Restriction Endonuclease R.EcoR124INT , 2012, PloS one.

[87]  Vladimir Benes,et al.  Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription , 2012, Nature Communications.

[88]  A. Jeltsch,et al.  The Caulobacter crescentus DNA-(adenine-N6)-methyltransferase CcrM methylates DNA in a distributive manner , 2011, Nucleic acids research.

[89]  John H. White,et al.  Structure and operation of the DNA-translocating type I DNA restriction enzymes. , 2012, Genes & development.

[90]  A. Piekarowicz,et al.  Deletion of One Nucleotide within the Homonucleotide Tract Present in the hsdS Gene Alters the DNA Sequence Specificity of Type I Restriction-Modification System NgoAV , 2011, Journal of bacteriology.

[91]  R. Rappuoli,et al.  A novel epigenetic regulator associated with the hypervirulent Neisseria meningitidis clonal complex 41/44 , 2011, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[92]  S. Biswas,et al.  Effects of DNA Methylation on Expression of Virulence Genes in Streptococcus mutans , 2011, Applied and Environmental Microbiology.

[93]  M. Gavioli,et al.  An Epigenetic Switch Involving Overlapping Fur and DNA Methylation Optimizes Expression of a Type VI Secretion Gene Cluster , 2011, PLoS genetics.

[94]  B. Shen,et al.  Characterization and crystal structure of the type IIG restriction endonuclease RM.BpuSI , 2011, Nucleic acids research.

[95]  M. Maiden,et al.  Influence of the combination and phase variation status of the haemoglobin receptors HmbR and HpuAB on meningococcal virulence , 2011, Microbiology.

[96]  X. Coumoul,et al.  BRCA1 affects global DNA methylation through regulation of DNMT1 , 2010, Cell Research.

[97]  M. Davies,et al.  Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism , 2010, Molecular microbiology.

[98]  Tyson A. Clark,et al.  Direct detection of DNA methylation during single-molecule, real-time sequencing , 2010, Nature Methods.

[99]  R. Miyahara,et al.  Restriction–modification systems may be associated with Helicobacter pylori virulence , 2010, Journal of gastroenterology and hepatology.

[100]  M. Jennings,et al.  The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes , 2010, Nature Reviews Microbiology.

[101]  Javier López-Garrido,et al.  Regulation of Salmonella enterica Pathogenicity Island 1 by DNA Adenine Methylation , 2010, Genetics.

[102]  I. Kobayashi,et al.  Genome comparison and context analysis reveals putative mobile forms of restriction–modification systems and related rearrangements , 2010, Nucleic acids research.

[103]  Matteo Brilli,et al.  The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis , 2010, BMC Systems Biology.

[104]  H. J. Beaumont,et al.  Experimental evolution of bet hedging , 2009, Nature.

[105]  M. N. Giacomodonato,et al.  Dam and its role in pathogenicity of Salmonella enterica. , 2009, Journal of infection in developing countries.

[106]  D. Armant,et al.  Epigenetics: Definition, Mechanisms and Clinical Perspective , 2009, Seminars in reproductive medicine.

[107]  M. Marinus,et al.  Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. , 2009, FEMS microbiology reviews.

[108]  K. Skarstad,et al.  The Escherichia coli SeqA protein. , 2009, Plasmid.

[109]  H. Bayley,et al.  Continuous base identification for single-molecule nanopore DNA sequencing. , 2009, Nature nanotechnology.

[110]  S. Grimmond,et al.  Phasevarions Mediate Random Switching of Gene Expression in Pathogenic Neisseria , 2009, PLoS pathogens.

[111]  John H. White,et al.  The structure of M.EcoKI Type I DNA methyltransferase with a DNA mimic antirestriction protein , 2008, Nucleic acids research.

[112]  R. Masui,et al.  Crystal structure of a putative DNA methylase TTHA0409 from Thermus thermophilus HB8 , 2008, Proteins.

[113]  I. Henderson,et al.  Regulation and function of Ag43 (flu). , 2008, Annual review of microbiology.

[114]  M. Waldor,et al.  Dam Methyltransferase Is Required for Stable Lysogeny of the Shiga Toxin (Stx2)-Encoding Bacteriophage 933W of Enterohemorrhagic Escherichia coli O157:H7 , 2007, Journal of bacteriology.

[115]  H. Mori,et al.  The applications of systematic in-frame, single-gene knockout mutant collection of Escherichia coli K-12. , 2008, Methods in molecular biology.

[116]  Guo-Min Li,et al.  Mechanisms and functions of DNA mismatch repair , 2008, Cell Research.

[117]  M. Schmidt,et al.  Overproduction of DNA Adenine Methyltransferase Alters Motility, Invasion, and the Lipopolysaccharide O-Antigen Composition of Yersinia enterocolitica , 2007, Infection and Immunity.

[118]  Xiaodong Cheng,et al.  Two Alternative Conformations of S-Adenosyl-L-homocysteine Bound to Escherichia coli DNA Adenine Methyltransferase and the Implication of Conformational Changes in Regulating the Catalytic Cycle* , 2007, Journal of Biological Chemistry.

[119]  A. Erwin,et al.  Haemophilus influenzae phasevarions have evolved from type III DNA restriction systems into epigenetic regulators of gene expression , 2007, Nucleic acids research.

[120]  A. Seshasayee.  An Assessment of the Role of DNA Adenine Methyltransferase on Gene Expression Regulation in E coli , 2007, PloS one.

[121]  S. Tzipori,et al.  Increased adherence and actin pedestal formation by dam‐deficient enterohaemorrhagic Escherichia coli O157:H7 , 2007, Molecular microbiology.

[122]  Shivakumara Bheemanaik,et al.  Structure, function and mechanism of exocyclic DNA methyltransferases. , 2006, The Biochemical journal.

[123]  J. Casadesús,et al.  Epigenetic Gene Regulation in the Bacterial World , 2006, Microbiology and Molecular Biology Reviews.

[124]  N. Reich,et al.  Selective Inhibitors of Bacterial DNA Adenine Methyltransferases , 2006, Journal of biomolecular screening.

[125]  Xiaodong Cheng,et al.  Structure and substrate recognition of the Escherichia coli DNA adenine methyltransferase. , 2006, Journal of molecular biology.

[126]  D. Wion,et al.  N6-methyl-adenine: an epigenetic signal for DNA–protein interactions , 2006, Nature Reviews Microbiology.

[127]  V. Robinson,et al.  A dam mutant of Yersinia pestis is attenuated and induces protection against plague. , 2005, FEMS microbiology letters.

[128]  R. Titball,et al.  Oral immunization with a dam mutant of Yersinia pseudotuberculosis protects against plague. , 2005, Microbiology.

[129]  S. Grimmond,et al.  The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[130]  Ole Skovgaard,et al.  Dam methylation: coordinating cellular processes. , 2005, Current opinion in microbiology.

[131]  D. Low,et al.  Regulation of the pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. , 2004, Molecular cell.

[132]  A. Piekarowicz,et al.  Characterization of a dam mutant of Haemophilus influenzae Rd. , 2004, Microbiology.

[133]  Michael E. Watson,et al.  Inactivation of deoxyadenosine methyltransferase (dam) attenuates Haemophilus influenzae virulence , 2004, Molecular microbiology.

[134]  Lucy Shapiro,et al.  Oscillating Global Regulators Control the Genetic Circuit Driving a Bacterial Cell Cycle , 2004, Science.

[135]  Michael T. Laub,et al.  Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus , 2004, Nature Reviews Microbiology.

[136]  Martin A Walsh,et al.  Crystal structure of MboIIA methyltransferase. , 2003, Nucleic acids research.

[137]  R. Gumport,et al.  Structures of Liganded and Unliganded RsrI N6-Adenine DNA Methyltransferase , 2003, Journal of Biological Chemistry.

[138]  M. Marinus,et al.  Role of SeqA and Dam in Escherichia coli gene expression: A global/microarray analysis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[139]  Lucy Shapiro,et al.  DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter , 2002, The EMBO journal.

[140]  C. A. White-Ziegler,et al.  The N-Acetyltransferase RimJ Responds to Environmental Stimuli To Repress pap Fimbrial Transcription in Escherichia coli , 2002, Journal of bacteriology.

[141]  H. Mori,et al.  Genome‐wide analysis of deoxyadenosine methyltransferase‐mediated control of gene expression in Escherichia coli , 2002, Molecular microbiology.

[142]  A. Jeltsch,et al.  The Escherichia coli dam DNA methyltransferase modifies DNA in a highly processive reaction. , 2002, Journal of molecular biology.

[143]  Lucy Shapiro,et al.  Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[144]  J. Casadesús,et al.  Envelope instability in DNA adenine methylase mutants of Salmonella enterica. , 2002, Microbiology.

[145]  D. Rao,et al.  Structure, Function, and Mechanism of HhaI DNA Methyltransferases , 2002, Critical reviews in biochemistry and molecular biology.

[146]  I. Kobayashi.  Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. , 2001, Nucleic acids research.

[147]  D. Dryden,et al.  Nucleoside triphosphate-dependent restriction enzymes. , 2001, Nucleic acids research.

[148]  R J Roberts,et al.  AdoMet-dependent methylation, DNA methyltransferases and base flipping. , 2001, Nucleic acids research.

[149]  L. Shapiro,et al.  The CcrM DNA Methyltransferase of Agrobacterium tumefaciens Is Essential, and Its Activity Is Cell Cycle Regulated , 2001, Journal of bacteriology.

[150]  S. Benkovic,et al.  Identification of the Active Oligomeric State of an Essential Adenine DNA Methyltransferase from Caulobacter crescentus * , 2001, The Journal of Biological Chemistry.

[151]  R J Roberts,et al.  Comparative genomics of the restriction-modification systems in Helicobacter pylori , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[152]  Marc Pignot,et al.  Structure of the N6-adenine DNA methyltransferase M•TaqI in complex with DNA and a cofactor analog , 2001, Nature Structural Biology.

[153]  I. Kobayashi,et al.  Diversity of restriction-modification gene homologues in Helicobacter pylori. , 2000, Gene.

[154]  M A Walsh,et al.  Structure of RsrI methyltransferase, a member of the N6-adenine beta class of DNA methyltransferases. , 2000, Nucleic acids research.

[155]  R. B. Jensen,et al.  The Brucella abortus CcrM DNA Methyltransferase Is Essential for Viability, and Its Overexpression Attenuates Intracellular Replication in Murine Macrophages , 2000, Journal of bacteriology.

[156]  N. Murray.  Type I Restriction Systems: Sophisticated Molecular Machines (a Legacy of Bertani and Weigle) , 2000, Microbiology and Molecular Biology Reviews.

[157]  L. Shapiro,et al.  Feedback control of a master bacterial cell-cycle regulator. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[158]  Lucy Shapiro,et al.  The CtrA Response Regulator Mediates Temporal Control of Gene Expression during the Caulobacter Cell Cycle , 1999, Journal of bacteriology.

[159]  R. Roberts,et al.  Structure of a binary complex of HhaI methyltransferase with S-adenosyl-L-methionine formed in the presence of a short non-specific DNA oligonucleotide. , 1999, Journal of molecular biology.

[160]  S. Lacks,et al.  Crystal structure of the DpnM DNA adenine methyltransferase from the DpnII restriction system of streptococcus pneumoniae bound to S-adenosylmethionine. , 1998, Structure.

[161]  A. Jeltsch,et al.  Functional Roles of Conserved Amino Acid Residues in DNA Methyltransferases Investigated by Site-directed Mutagenesis of theEcoRV Adenine-N 6-methyltransferase* , 1998, The Journal of Biological Chemistry.

[162]  J. Köhl,et al.  Phase-variable Expression of Lipopolysaccharide Contributes to the Virulence of Legionella pneumophila , 1998, The Journal of experimental medicine.

[163]  M. W. van der Woude,et al.  Thermoregulation of Escherichia coli pap transcription: H‐NS is a temperature‐dependent DNA methylation blocking factor , 1998, Molecular microbiology.

[164]  R. Roberts,et al.  Base flipping. , 1998, Annual review of biochemistry.

[165]  C. Helmstetter,et al.  DNA sequestration and transcription in the oriC region of Escherichia coli , 1997, Molecular microbiology.

[166]  R. Blumenthal,et al.  Structure of pvu II DNA-(cytosine N4) methyltransferase, an example of domain permutation and protein fold assignment. , 1997, Nucleic acids research.

[167]  I. Henderson,et al.  Phase-variable outer membrane proteins in Escherichia coli. , 1996, FEMS immunology and medical microbiology.

[168]  J. Casadesús,et al.  DNA adenine methylase mutants of Salmonella typhimurium and a novel dam-regulated locus. , 1996, Genetics.

[169]  D. Rao,et al.  Functional analysis of conserved motifs in EcoP15I DNA methyltransferase. , 1996, Journal of molecular biology.

[170]  A. Danchin,et al.  Uneven distribution of GATC motifs in the Escherichia coli chromosome, its plasmids and its phages. , 1996, Journal of molecular biology.

[171]  A. Bhagwat,et al.  Overproduction of DNA Cytosine Methyltransferases Causes Methylation and C T Mutations at Non-canonical Sites (*) , 1996, The Journal of Biological Chemistry.

[172]  L. Shapiro,et al.  A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[173]  M. W. van der Woude,et al.  Epigenetic phase variation of the pap operon in Escherichia coli. , 1996, Trends in microbiology.

[174]  L. Kaltenbach,et al.  Differential binding of Lrp to two sets of pap DNA binding sites mediated by Pap I regulates Pap phase variation in Escherichia coli. , 1995, The EMBO journal.

[175]  W. Lipscomb,et al.  The crystal structure of Haelll methyltransferase covalently complexed to DNA: An extrahelical cytosine and rearranged base pairing , 1995, Cell.

[176]  W. Saenger,et al.  A model for DNA binding and enzyme action derived from crystallographic studies of the TaqI N6-adenine-methyltransferase. , 1995, Gene.

[177]  K Kusano,et al.  Selfish behavior of restriction-modification systems , 1995, Science.

[178]  M. Schaechter,et al.  SeqA limits DnaA activity in replication from oriC in Escherichia coli , 1994, Molecular microbiology.

[179]  Nancy Kleckner,et al.  SeqA: A negative modulator of replication initiation in E. coli , 1994, Cell.

[180]  L. Shapiro,et al.  A Caulobacter DNA methyltransferase that functions only in the predivisional cell. , 1994, Journal of molecular biology.

[181]  Richard J. Roberts,et al.  Crystal structure of the Hhal DNA methyltransferase complexed with S-adenosyl-l-methionine , 1993, Cell.

[182]  T. Bickle,et al.  Biology of DNA restriction , 1993 .

[183]  M. W. Woude,et al.  Evidence for global regulatory control of pilus expression in Escherichia coli by Lrp and DNA methylation: model building based on analysis of pap , 1992, Molecular microbiology.

[184]  E. Boye,et al.  Expression of the Escherichia coli dam gene , 1992, Molecular microbiology.

[185]  A. Bergerat,et al.  Allosteric and catalytic binding of S-adenosylmethionine to Escherichia coli DNA adenine methyltransferase monitored by 3H NMR. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[186]  L. Blyn,et al.  Regulation of pap pilin phase variation by a mechanism involving differential dam methylation states. , 1990, The EMBO journal.

[187]  N. Kleckner,et al.  E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork , 1990, Cell.

[188]  Hamilton O. Smith,et al.  Finding sequence motifs in groups of functionally related proteins. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[189]  D. Berg,et al.  Transposition effect of adenine (Dam) methylation on activity of O end mutants of IS50. , 1989, Journal of molecular biology.

[190]  R J Roberts,et al.  Predictive motifs derived from cytosine methyltransferases. , 1989, Nucleic acids research.

[191]  T. Trautner,et al.  Cytosine-specific type II DNA methyltransferases. A conserved enzyme core with variable target-recognizing domains. , 1989, Journal of molecular biology.

[192]  M. Marinus,et al.  The great GATC: DNA methylation in E. coli. , 1989, Trends in genetics : TIG.

[193]  Arthur Kornberg,et al.  A model for initiation at origins of DNA replication , 1988, Cell.

[194]  N. Kleckner,et al.  IS10 transposition is regulated by DNA adenine methylation , 1985, Cell.

[195]  T. Gingeras,et al.  The isolation and characterization of the Escherichia coli DNA adenine methylase (dam) gene. , 1983, Nucleic acids research.

[196]  M. Marinus,et al.  Isolation of Deoxyribonucleic Acid Methylase Mutants of Escherichia coli K-12 , 1973, Journal of bacteriology.