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

Journal of Bacteriology

Volumn 193, Issue 23, 2011, Pages 6750-6759

  Adamczyk Poplawska, Monika ^a   Lower, Michal ^a   Piekarowicz, Andrzej ^a  

^a UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE; NUCLEOTIDE; PALINDROMIC DNA; POLYGUANYLIC ACID; RESTRICTION ENDONUCLEASE; BACTERIAL PROTEIN; HSDS PROTEIN, BACTERIA; TYPE I SITE SPECIFIC DEOXYRIBONUCLEASE;

AMINO TERMINAL SEQUENCE; ARTICLE; DNA METHYLATION; DNA MODIFICATION; DNA RESTRICTION; DNA SEQUENCE; ESCHERICHIA COLI; FRAMESHIFT MUTATION; GENE; GENE DELETION; GENE EXPRESSION; GENE FUSION; GENE LOCUS; HSDS GENE; IN VIVO STUDY; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; POINT MUTATION;

ESCHERICHIA COLI; NEISSERIA GONORRHOEAE;

BACTERIAL PROTEINS; DEOXYRIBONUCLEASES, TYPE I SITE-SPECIFIC; DNA RESTRICTION-MODIFICATION ENZYMES; NEISSERIA GONORRHOEAE; POINT MUTATION; SEQUENCE DELETION; SUBSTRATE SPECIFICITY;

EID: 84855380901     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05672-11     Document Type: Article

References (48)

1. Abadjieva, A., J. Patel, M. Webb, V. Zinkevich, and K. Firman. 1993. A deletion mutant of the type IC restriction endonuclease EcoR1241 expressing a novel DNA specificity. Nucleic Acids Res. 21:4435-4443.
2. Abadjieva, A., M. Webb, J. Patel, V. Zinkevich, and K. Firman. 1994. Deletions within the DNA recognition subunit of M. EcoR124I that identify a region involved in protein-protein interactions between HsdS and HsdM. J. Mol. Biol. 241:35-43.
3. Adamczyk-Poplawska, M., A. Kondrzycka, K. Urbanek, and A. Piekarowicz. 2003. Tetra-amino-acid tandem repeats are involved in HsdS complementation in type IC restriction-modification systems. Microbiology 149:3311-3319.
4. Adamczyk-Poplawska, M., M. Lower, and A. Piekarowicz. 2009. Characterization of the NgoAXP: phase-variable type III restriction-modification system in Neisseria gonorrhoeae. FEMS Microbiol. Lett. 300:25-35.
5. Argos, P. 1985. Evidence for a repeating domain in type I restriction enzymes. EMBO J. 4:1351-1355.
6. Bayliss, C. D., M. J. Callaghan, and E. R. Moxon. 2006. High allelic diversity in the methyltransferase gene of a phase variable type III restriction-modification system has implications for the fitness of Haemophilus influenzae. Nucleic Acids Res. 34:4046-4059.
7. Bickle, T. A. 2004. Restricting restriction. Mol. Microbiol. 51:3-5.
8. Bille, E., et al. 2005. A chromosomally integrated bacteriophage in invasive meningococci. J. Exp. Med. 201:1905-1913.
9. Broadbent, S. E., M. R. Davies, and M. W. van der Woude. 2010. Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Mol. Microbiol. 77:337-353.
10. De Bolle, X., et al. 2000. The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol. Microbiol. 35:211-222.
11. de Vries, N., et al. 2002. Transcriptional phase variation of a type III restriction- modification system in Helicobacter pylori. J. Bacteriol. 184:6615-6623.
12. Donahue, J. P., et al. 2000. Analysis of iceA1 transcription in Helicobacter pylori. Helicobacter 5:1-12.
13. Dybvig, K., R. Sitaraman, and C. T. French. 1998. A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. Proc. Natl. Acad. Sci. U. S. A. 95:13923-13928.
14. Edwards, J. L., and M. A. Apicella. 2004. The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin. Microbiol. Rev. 17:965-981.
15. Fox, K. L., et al. 2007. Haemophilus influenzae phasevarions have evolved from type III DNA restriction systems into epigenetic regulators of gene expression. Nucleic Acids Res. 35:5242-5252.
16. Fox, K. L., Y. N. Srikhanta, and M. P. Jennings. 2007. Phase variable type III restriction-modification systems of host-adapted bacterial pathogens. Mol. Microbiol. 65:1375-1379.
17. Ghosh, S. K., et al. 2004. Pathogenic consequences of Neisseria gonorrhoeae pilin glycan variation. Microbes Infect. 6:693-701.
18. Gubler, M., and T. A. Bickle. 1991. Increased protein flexibility leads to promiscuous protein-DNA interactions in type IC restriction-modification systems. EMBO J. 10:951-957.
19. Gubler, M., D. Braguglia, J. Meyer, A. Piekarowicz, and T. A. Bickle. 1992. Recombination of constant and variable modules alters DNA sequence recognition by type IC restriction-modification enzymes. EMBO J. 11:233-240.
20. Gumulak-Smith, J., et al. 2001. Variations in the surface proteins and restriction enzyme systems of Mycoplasma pulmonis in the respiratory tract of infected rats. Mol. Microbiol. 40:1037-1044.
21. Henderson, I. R., P. Owen, and J. P. Nataro. 1999. Molecular switches-the ON and OFF of bacterial phase variation. Mol. Microbiol. 33:919-932.
22. Hill, S. A., and J. K. Davies. 2009. Pilin gene variation in Neisseria gonorrhoeae: reassessing the old paradigms. FEMS Microbiol. Rev. 33:521-530.
23. Hoskisson, P. A., and M. C. Smith. 2007. Hypervariation and phase variation in the bacteriophage 'resistome.' Curr. Opin. Microbiol. 10:396-400.
24. Janscak, P., A. Abadjieva, and K. Firman. 1996. The type I restriction endonuclease R. EcoR124I: over-production and biochemical properties. J. Mol. Biol. 257:977-991.
25. Jordan, P. W., L. A. Snyder, and N. J. Saunders. 2005. Strain-specific differences in Neisseria gonorrhoeae associated with the phase variable gene repertoire. BMC Microbiol. 5:21.
26. Kellogg, D. S., Jr., W. L. Peacock, Jr., W. E. Deacon, L. Brown, and D. I. Pirkle. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
27. Kneale, G. G. 1994. A symmetrical model for the domain structure of type I DNA methyltransferases. J. Mol. Biol. 243:1-5.
28. Lehours, P., et al. 2007. Genetic diversity of the HpyC1I restriction modification system in Helicobacter pylori. Res. Microbiol. 158:265-271.
29. MacWilliams, M. P., and T. A. Bickle. 1996. Generation of new DNA binding specificity by truncation of the type IC EcoDXXI hsdS gene. EMBO J. 15:4775-4783.
30. Mayer, M. P. 1995. A new set of useful cloning and expression vectors derived from pBlueScript. Gene 163:41-46.
31. Meister, J., et al. 1993. Macroevolution by transposition: drastic modification of DNA recognition by a type I restriction enzyme following Tn5 transposition. EMBO J. 12:4585-4591.
32. Meyer, T. F. 1991. Evasion mechanisms of pathogenic Neisseriae. Behring Inst. Mitt. 1991:194-199.
33. Murray, N. E. 2000. Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol. Mol. Biol. Rev. 64:412-434.
34. Piekarowicz, A., A. Klyz, A. Kwiatek, and D. C. Stein. 2001. Analysis of type I restriction modification systems in the Neisseriaceae: genetic organization and properties of the gene products. Mol. Microbiol. 41:1199-1210.
35. Price, C., J. Lingner, T. A. Bickle, K. Firman, and S. W. Glover. 1989. Basis for changes in DNA recognition by the EcoR124 and EcoR124/3 type I DNA restriction and modification enzymes. J. Mol. Biol. 205:115-125.
36. Price, C., T. Pripfl, and T. A. Bickle. 1987. EcoR124 and EcoR124/3: the first members of a new family of type I restriction and modification systems. Eur. J. Biochem. 167:111-115.
37. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2007. REBASE- enzymes and genes for DNA restriction and modification. Nucleic Acids Res. 35:D269-D270.
38. Ryan, K. A., and R. Y. Lo. 1999. Characterization of a CACAG pentanucleotide repeat in Pasteurella haemolytica and its possible role in modulation of a novel type III restriction-modification system. Nucleic Acids Res. 27:1505-1511.
39. Sambrook, J., and D. Russell (ed.). 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Saunders, N. J., et al. 2000. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 37:207-215.
41. Srikhanta, Y. N., et al. 2009. Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog. 5:e1000400.
42. Srikhanta, Y. N., K. L. Fox, and M. P. Jennings. 2010. The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol. 8:196-206.
43. Stein, D. C., J. S. Gunn, M. Radlinska, and A. Piekarowicz. 1995. Restriction and modification systems of Neisseria gonorrhoeae. Gene 157:19-22.
44. Torres-Cruz, J., and M. W. van der Woude. 2003. Slipped-strand mispairing can function as a phase variation mechanism in Escherichia coli. J. Bacteriol. 185:6990-6994.
45. Ullmann, A., F. Jacob, and J. Monod. 1968. On the subunit structure of wild-type versus complemented beta-galactosidase of Escherichia coli. J. Mol. Biol. 32:1-13.
46. van der Woude, M. W., and A. J. Baumler. 2004. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17:581-611.
47. van Putten, J. P. 1993. Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae. EMBO J. 12:4043-4051.
48. Wassenaar, T. M., et al. 2002. Homonucleotide stretches in chromosomal DNA of Campylobacter jejuni display high frequency polymorphism as detected by direct PCR analysis. FEMS Microbiol. Lett. 212:77-85.