Specificity of the ModA11, ModA12 and ModD1 epigenetic regulator N6-adenine DNA methyltransferases of Neisseria meningitidis

Nucleic Acids Research

Volumn 43, Issue 8, 2015, Pages 4150-4162

  Seib, Kate L ^a   Jen, Freda E C ^a   Tan, Aimee ^a   Scott, Adeana L ^a   Kumar, Ritesh ^b   Power, Peter M ^a   Chen, Li Tzu ^c   Wu, Hsing Ju ^d   Wang, Andrew H J ^c   Hill, Dorothea M C ^e   Luyten, Yvette A ^f   Morgan, Richard D ^f   Roberts, Richard J ^f   Maiden, Martin C J ^e   Boitano, Matthew ^g   Clark, Tyson A ^g   Korlach, Jonas ^g   Rao, Desirazu N ^b   Jennings, Michael P ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f NEW ENGLAND BIOLABS   (United States)

^g PACIFIC BIOSCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ANTIBIOTIC AGENT; CYTOSINE; DNA METHYLTRANSFERASE; GUANINE; MODA11 PROTEIN; MODA12 PROTEIN; MODD1 PROTEIN; PYRIMIDINE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC);

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; DNA FLANKING REGION; DNA METHYLATION; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME SPECIFICITY; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENE SWITCHING; GENETIC ASSOCIATION; MUTAGENESIS; NEISSERIA MENINGITIDIS; NONHUMAN; PHASEVARION; PHENOTYPE; PRIORITY JOURNAL; REGULON; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; METHYLATION; MOLECULAR GENETICS;

NEISSERIA MENINGITIDIS;

BACTERIAL PROTEINS; DNA, BACTERIAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; METHYLATION; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

EID: 84930226213     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv219     Document Type: Article

References (47)

1. Moxon, R., Bayliss, C. and Hood, D. (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet., 40, 307-333.
2. Srikhanta, Y.N., Maguire, T.L., Stacey, K.J., Grimmond, S.M. and Jennings, M.P. (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc. Natl. Acad. Sci. U.S.A., 102, 5547-5551.
3. Srikhanta, Y.N., Fox, K.L. and Jennings, M.P. (2010) The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol., 8, 196-206.
4. Seib, K.L., Peak, I.R. and Jennings, M.P. (2002) Phase variable restriction-modification systems in Moraxella catarrhalis. FEMS Immunol. Med. Microbiol., 32, 159-165.
5. Blakeway, L.V., Power, P.M., Jen, F.E., Worboys, S.R., Boitano, M., Clark, T.A., Korlach, J., Bakaletz, L.O., Jennings, M.P., Peak, I.R. et al. (2014)ModM DNA methyltransferase methylome analysis reveals a potential role for Moraxella catarrhalis phasevarions in otitis media.FASEB J.,28,5197-5207.
6. Fox, K.L., Dowideit, S.J., Erwin, A.L., Srikhanta, Y.N., Smith, A.L. and Jennings, M.P. (2007) Haemophilus influenzae phasevarions have evolved from type III DNA restriction systems into epigenetic regulators of gene expression. Nucleic Acids Res., 35, 5242-5252.
7. Srikhanta, Y.N., Gorrell, R.J., Steen, J.A., Gawthorne, J.A., Kwok, T., Grimmond, S.M., Robins-Browne, R.M. and Jennings, M.P. (2011) Phasevarion mediated epigenetic gene regulation in Helicobacter pylori. PLoS One, 6, e27569.
8. Srikhanta, Y.N., Dowideit, S.J., Edwards, J.L., Falsetta, M.L., Wu, H.J., Harrison, O.B., Fox, K.L., Seib, K.L., Maguire, T.L., Wang, A.H. et al. (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog, 5, e1000400.
9. Jen, F.E., Seib, K.L. and Jennings, M.P. (2014) Phasevarions mediate epigenetic regulation of antimicrobial susceptibility in Neisseria meningitidis. Antimicrob. Agents Chemother., 58, 4219-4221.
10. Manso, A.S., Chai, M.H., Atack, J.M., Furi, L., De Ste Croix, M., Haigh, R., Trappetti, C., Ogunniyi, A.D., Shewell, L.K., Boitano, M. et al. (2014) A random six-phase switch regulates pneumococcal virulence via global epigenetic changes. Nat. Commun., 5, 5055.
11. Seib, K.L., Pigozzi, E., Muzzi, A., Gawthorne, J.A., Delany, I., Jennings, M.P. and Rappuoli, R. (2011) A novel epigenetic regulator associated with the hypervirulent Neisseria meningitidis clonal complex 41/44. FASEB J., 25, 3622-3633.
12. Gawthorne, J.A., Beatson, S.A., Srikhanta, Y.N., Fox, K.L. and Jennings, M.P. (2012) Origin of the diversity in DNA recognition domains in phasevarion associated modA genes of pathogenic Neisseria and Haemophilus influenzae. PLoS One, 7, e32337.
13. Roberts, R.J., Belfort, M., Bestor, T., Bhagwat, A.S., Bickle, T.A., Bitinaite, J., Blumenthal, R.M., Degtyarev, S., Dryden, D.T., Dybvig, K. et al. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res., 31, 1805-1812.
14. Murray, I.A., Clark, T.A., Morgan, R.D., Boitano, M., Anton, B.P., Luong, K., Fomenkov, A., Turner, S.W., Korlach, J. and Roberts, R.J. (2012) The methylomes of six bacteria. Nucleic Acids Res., 40, 11450-11462.
15. McGuinness, B.T., Clarke, I.N., Lambden, P.R., Barlow, A.K., Poolman, J.T., Jones, D.M. and Heckels, J.E. (1991) Point mutation in meningococcal por A gene associated with increased endemic disease. Lancet, 337, 514-517.
16. Maiden, M.C., Bygraves, J.A., Feil, E., Morelli, G., Russell, J.E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K., Caugant, D.A. et al. (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. U.S.A., 95, 3140-3145.
17. Bentley, S.D., Vernikos, G.S., Snyder, L.A., Churcher, C., Arrowsmith, C., Chillingworth, T., Cronin, A., Davis, P.H., Holroyd, N.E., Jagels, K. et al. (2007) Meningococcal genetic variation mechanisms viewed through comparative analysis of serogroup C strain FAM18. PLoS Genet., 3, e23.
18. Budroni, S., Siena, E., Hotopp, J.C., Seib, K.L., Serruto, D., Nofroni, C., Comanducci, M., Riley, D.R., Daugherty, S.C., Angiuoli, S.V. et al. (2011) Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc. Natl. Acad. Sci. U.S.A., 108, 4494-4499.
19. Seib, K.L., Oriente, F., Adu-Bobie, J., Montanari, P., Ferlicca, F., Giuliani, M.M., Rappuoli, R., Pizza, M. and Delany, I. (2010) Influence of serogroup B meningococcal vaccine antigens on growth and survival of the meningococcus in vitro and in ex vivo and in vivo models of infection. Vaccine, 28, 2416-2427.
20. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
21. Jen, F.E., Warren, M.J., Schulz, B.L., Power, P.M., Swords, W.E., Weiser, J.N., Apicella, M.A., Edwards, J.L. and Jennings, M.P. (2013) Dual pili post-translational modifications synergize to mediate meningococcal adherence to platelet activating factor receptor on human airway cells. PLoS Pathog, 9, e1003377.
22. Rubin, R.A. and Modrich, P. (1977) EcoRI methylase. Physical and catalytic properties of the homogeneous enzyme. J Biol Chem, 252, 7265-7272.
23. Clark, T.A., Murray, I.A., Morgan, R.D., Kislyuk, A.O., Spittle, K.E., Boitano, M., Fomenkov, A., Roberts, R.J. and Korlach, J. (2012) Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res., 40, e29.
24. R-Development-Core-Team.(2008)R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, http://www.R-project.org.
25. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A. and Barrell, B. (2000) Artemis: sequence visualization and annotation. Bioinformatics, 16, 944-945.
26. Humbelin, M., Suri, B., Rao, D.N., Hornby, D.P., Eberle, H., Pripfl, T., Kenel, S. and Bickle, T.A. (1988) Type III DNA restriction and modification systems EcoP1 and EcoP15. Nucleotide sequence of the EcoP1 operon, the EcoP15 mod gene and some EcoP1 mod mutants. J. Mol. Biol., 200, 23-29.
27. Roberts, R.J., Vincze, T., Posfai, J. and Macelis, D. (2010) REBASE-a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res., 38, D234-D236.
28. Virji, M., Makepeace, K., Peak, I.R., Ferguson, D.J., Jennings, M.P. and Moxon, E.R. (1995) Opc- and pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol. Microbiol., 18, 741-754.
29. Martin, P., Sun, L., Hood, D.W. and Moxon, E.R. (2004) Involvement of genes of genome maintenance in the regulation of phase variation frequencies in Neisseria meningitidis. Microbiology, 150, 3001-3012.
30. Bart, A., Pannekoek, Y., Dankert, J. and van der Ende, A. (2001) NmeSI restriction-modification system identified by representational difference analysis of a hypervirulent Neisseria meningitidis strain. Infect. Immun., 69, 1816-1820.
31. Bickle, T.A. and Kruger, D.H. (1993) Biology of DNA restriction. Microbiol. Rev., 57, 434-450.
32. Vasu, K. and Nagaraja, V. (2013) Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol. Mol. Biol. Rev., 77, 53-72.
33. Rao, D.N., Dryden, D.T. and Bheemanaik, S. (2014) Type III restriction-modification enzymes: a historical perspective. Nucleic Acids Res., 42, 45-55.
34. Fang, G., Munera, D., Friedman, D.I., Mandlik, A., Chao, M.C., Banerjee, O., Feng, Z., Losic, B., Mahajan, M.C., Jabado, O.J. et al. (2012) Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat. Biotechnol., 30, 1232-1239.
35. Drozdz, M., Piekarowicz, A., Bujnicki, J.M. and Radlinska, M. (2012) Novel non-specific DNA adenine methyltransferases. Nucleic Acids Res., 40, 2119-2130.
36. Kamps-Hughes, N., Quimby, A., Zhu, Z. and Johnson, E.A. (2013) Massively parallel characterization of restriction endonucleases. Nucleic Acids Res., 41, e119.
37. Wei, H., Therrien, C., Blanchard, A., Guan, S. and Zhu, Z. (2008) The Fidelity Index provides a systematic quantitation of star activity of DNA restriction endonucleases. Nucleic Acids Res., 36, e50.
38. Borgaro, J.G., Benner, N. and Zhu, Z. (2013) Fidelity index determination of DNA methyltransferases. PLoS One, 8, e63866.
39. Cohen, H.M., Tawfik, D.S. and Griffiths, A.D. (2004) Altering the sequence specificity of HaeIII methyltransferase by directed evolution using in vitro compartmentalization. Protein Eng. Des. Sel., 17, 3-11.
40. Rockah-Shmuel, L. and Tawfik, D.S. (2012) Evolutionary transitions to new DNA methyltransferases through target site expansion and shrinkage. Nucleic Acids Res., 40, 11627-11637.
41. Timar, E., Groma, G., Kiss, A. and Venetianer, P. (2004) Changing the recognition specificity of a DNA-methyltransferase by in vitro evolution. Nucleic Acids Res., 32, 3898-3903.
42. Adamczyk-Poplawska, M., Lower, M. and Piekarowicz, A. (2009) Characterization of the NgoAXP: phase-variable type III restriction-modification system in Neisseria gonorrhoeae. FEMS Microbiol. Lett., 300, 25-35.
43. Wion, D. and Casadesus, J. (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol., 4, 183-192.
44. Korlach, J. and Turner, S.W. (2012) Going beyond five bases in DNA sequencing. Curr. Opin. Struct. Biol., 22, 251-261.
45. Davis, B.M., Chao, M.C. and Waldor, M.K. (2013) Entering the era of bacterial epigenomics with single molecule real time DNA sequencing. Current Opin. Microbiol., 16, 192-198.
46. Krebes, J., Morgan, R.D., Bunk, B., Sproer, C., Luong, K., Parusel, R., Anton, B.P., Konig, C., Josenhans, C., Overmann, J. et al. (2014) The complex methylome of the human gastric pathogen Helicobacter pylori. Nucleic Acids Res., 42, 2415-2432.
47. Lluch-Senar, M., Luong, K., Llorens-Rico, V., Delgado, J., Fang, G., Spittle, K., Clark, T.A., Schadt, E., Turner, S.W., Korlach, J. et al. (2013) Comprehensive methylome characterization of Mycoplasma genitalium and Mycoplasma pneumoniae at single-base resolution. PLoS Genet., 9, e1003191.