Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori

Journal of Bacteriology

Volumn 184, Issue 23, 2002, Pages 6615-6623

  De Vries, Nicolette ^a   Duinsbergen, Dirk ^a   Kuipers, Ernst J ^a   Pot, Raymond G J ^a   Wiesenekker, Patricia ^a   Penn, Charles W ^a   Van Vliet, Arnoud H M ^a   Vandenbroucke Grauls, Christina M J E ^a   Kusters, Johannes G ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BETA GALACTOSIDASE; DNA METHYLTRANSFERASE; ENDONUCLEASE; GENE PRODUCT; PROTEIN MOD; UNCLASSIFIED DRUG;

ADAPTATION; ANTIGENICITY; ARTICLE; BASE PAIRING; CONTROLLED STUDY; FUSION GENE; GENE EXPRESSION; GENE LOCATION; GENE STRUCTURE; GENETIC CODE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HELICOBACTER PYLORI; IMMUNE RESPONSE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PATHOGENESIS; PRIORITY JOURNAL; RESTRICTION MAPPING; RNA TRANSLATION; SEQUENCE HOMOLOGY;

BASE PAIR MISMATCH; BASE SEQUENCE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA RESTRICTION ENZYMES; DNA RESTRICTION-MODIFICATION ENZYMES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; LAC OPERON; MOLECULAR SEQUENCE DATA; PROTEIN BIOSYNTHESIS; TRANSCRIPTION, GENETIC; VARIATION (GENETICS);

ANIMALIA; BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI;

EID: 0036889446     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.184.23.6615-6624.2002     Document Type: Article

References (45)

1. Alifano, P., F. Rivellini, D. Limauro, C. B. Bruni, and M. S. Carlomagno. 1991. A consensus motif common to all Rho-dependent prokaryotic transcription terminators. Cell 64:553-563.
2. Aim, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
3. Appelmelk, B. J., S. L. Martin, M. A. Monteiro, C. A. Clayton, A. A. McColm, P. Zheng, T. Verboom, J. J. Maaskant, D. H. van den Eijnden, C. H. Hokke, M. B. Perry, C. M. Vandenbroucke-Grauls, and J. G. Kusters. 1999. Phase variation in Helicobacter pylori lipopolysaccharide due to changes in the lengths of poly(C) tracts in α3-fucosyltransferase genes. Infect. Immun. 67:5361-5366.
4. Appelmelk, B. J., M. C. Martino, E. Veenhof, M. A. Montelro, J. J. Maaskant, R. Negrini, F. Lindh, M. Perry, G. Del Giudice, and C. M. J. E. Vandenbroucke-Grauls. 2000. Phase variation in H type I and Lewis a epitopes of Helicobacter pylori lipopolysaccharide. Infect. Immun. 68:5928-5932.
5. Bijlsma, J. J., C. M. Vandenbroucke-Grauls, S. H. Phadnis, and J. G. Kusters. 1999. Identification of virulence genes of Helicobacter pylori by random insertion mutagenesis. Infect. Immun. 67:2433-2440.
6. Blyn, L. B., B. A. Braaten, and D. A. Low. 1990. Regulation ofpap pilin phase variation by a mechanism involving differential dam methylation states. EMBO J. 9:4045-4054.
7. Butler, D., and G. F. Fitzgerald. 2001. Transcriptional analysis and regulation of expression of the ScrFI restriction-modification system of Lactococcus lactis subsp. cremoris UC503. J. Bacteriol. 183:4668-4673.
8. Cover, T. L., and M. J. Blaser. 1992. Helicobacter pylori and gastroduodenal disease. Annu. Rev. Med. 43:135-145.
9. Davies, B. J., N. de Vries, S. G. Rijpkema, A. H. M. van Vliet, and C. W. Penn. 2002. Transcriptional and mutational analysis of the Helicobacter pylori urease promoter. FEMS Microbiol. Lett. 213:27-32.
10. De Bolle, X., C. D. Bayliss, D. Field, T. van de Ven, N. J. Saunders, D. W. Hood, and E. R. Moxon. 2000. The length of a tetranucleotide repeat tract in Haemophilus infiuenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol. Microbiol. 35:211-222.
11. de Vries, N., E. J. Kuipers, N. E. Kramer, A. H. M. van Vliet, J. J. E. Bijlsma, M. Kist, S. Bereswill, C. M. J. E. Vandenbroucke-Grauls, and J. G. Kusters. 2001. Identification of environmental stress-regulated genes in Helicobacter pylori by a lacZ reporter gene fusion system. Helicobacter 6:300-309.
12. Dunn, B. E., H. Cohen, and M. J. Blaser. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10:720-741.
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. USA 95:13923-13928.
14. Freitag, C. S., J. M. Abraham, J. R. Clements, and B. I. Eisenstein. 1985. Genetic analysis of the phase variation control of expression of type 1 fimbriae in Escherichia coli. J. Bacteriol. 162:668-675.
15. Goodwin, A., D. Kersulyte, G. Sisson, V. Z. Veldhuyzen, D. E. Berg, and P. S. Hoffman. 1998. Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygen-insensitive NADPH nitroreductase. Mol. Microbiol. 28:383-393.
16. Govantes, F., and E. Santero. 1996. Transcription termination within the regulatory nifLA operon of Klebsiella pneumoniae. Mol. Gen. Genet. 250:447-454.
17. Gumulak-Smith, J., A. Teachman, A. H. Tu, J. W. Simecka, J. R. Lindsey, and K. Dybvig. 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.
18. Heithoff, D. M., R. L. Sinsheimer, D. A. Low, and M. J. Mahan. 1999. An essential role for DNA adenine methylation in bacterial virulence. Science 284:967-970.
19. Humbelin, M., B. Suri, D. N. Rao, D. P. Hornby, H. Eberle, T. Pripfl, S. Kenel, and T. A. Bickle. 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.
20. Jones, A. C., R. P. Logan, S. Foynes, A. Cockayne, B. W. Wren, and C. W. Penn. 1997. A flagellar sheath protein of Helicobacter pylori is identical to HpaA, a putative N-acetylneuraminyllactose-binding hemagglutinin, but is not an adhesin for AGS cells. J. Bacteriol. 179:5643-5647.
21. Josenhans, C., K. A. Eaton, T. Thevenot, and S. Suerbaum. 2000. Switching of fiagellar motility in Helicobacter pylori by reversible length variation of a short homopolymeric sequence repeat in flip, a gene encoding a basal body protein. Infect. Immun. 68:4598-4603.
22. Kobayashi, I. 2001. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29:3742-3756.
23. Lavitola, A., C. Bucci, P. Salvatore, G. Maresca, C. B. Bruni, and P. Alifano. 1999. Intracistronic transcription termination in polysialyl transferase gene (siaD) affects phase variation in Neisseria meningitidis. Mol. Microbiol. 33:119-127.
24. Meisel, A., T. A. Bickle, D. H. Kruger, and C. Schroeder. 1992. Type III restriction enzymes need two inversely oriented recognition sites for DNA cleavage. Nature 355:467-469.
25. Merino, E., P. Babitzke, and C. Yanofsky. 1995. trp RNA-binding attenuation protein (TRAP)-trp leader RNA interactions mediate translational as well as transcriptional regulation of the Bacillus subtilis trp operon. J. Bacteriol. 177:6362-6370.
26. Murray, N. E. 2002. 2001 Fred Griffith review lecture. Immigration control of DNA in bacteria: Self versus non-self. Microbiology 148:3-20.
27. Nobusato, A., I. Uchiyama, S. Ohashi, and I. Kobayashi. 2000. Insertion with long target duplication: A mechanism for gene mobility suggested from comparison of two related bacterial genomes. Gene 259:99-108.
28. Odenbreit, S., B. Wieland, and R. Haas. 1996. Cloning and genetic characterization of Helicobacter pylori catalase and construction of a catalasedeficient mutant strain. J. Bacteriol. 178:6960-6967.
29. Peck, B., M. Ortkamp, K. D. Diehl, E. Hundt, and B. Knapp. 1999. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res. 27:3325-3333.
30. Perez-Martin, J., F. Rojo, and V. de Lorenzo. 1994. Promoters responsive to DNA bending: A common theme in prokaryotic gene expression. Microbiol. Rev. 58:268-290.
31. Saha, S., I. Ahmad, Y. V. Reddy, V. Krishnamurthy, and D. N. Rao. 1998. Functional analysis of conserved motifs in type III restriction-modification enzymes. Biol. Chem. 379:511-517.
32. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
33. Saunders, N. J., J. F. Peden, D. W. Hood, and E. R. Moxon. 1998. Simple sequence repeats in the Helicobacter pylori genome. Mol. Microbiol. 27:1091-1098.
34. Scott, T. N., and M. I. Simon. 1982. Genetic analysis of the mechanism of the Salmonella phase variation site specific recombination system. Mol. Gen. Genet. 188:313-321.
35. Sheridan, S. D., M. L. Opel, and G. W. Hatfield. 2001. Activation and repression of transcription initiation by a distant DNA structural transition. Mol. Microbiol. 40:684-690.
36. Tannaes, T., N. Dekker, G. Bukholm, J. J. Bijlsma, and B. J. Appelmelk. 2001. Phase variation in the Helicobacter pylori phospholipase A gene and its role in acid adaptation. Infect. Immun. 69:7334-7340.
37. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
38. van der Ende, A., C. T. Hopman, S. Zaat, B. B. Essink, B. Berkhout, and J. Dankert. 1995. Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the -10 and -35 regions of the promoter. J. Bacteriol. 177:2475-2480.
39. van Doorn, N. E., F. Namavar, J. G. Kusters, E. P. van Rees, E. J. Kuipers, and J. de Graaff. 1998. Genomic DNA fingerprinting of clinical isolates of Helicobacter pylori by REP-PCR and restriction fragment end-labelling. FEMS Microbiol. Lett. 160:145-150.
40. Vanet, A., L. Marsan, A. Labigne, and M. F. Sagot. 2000. Inferring regulatory elements from a whole genome. An analysis of Helicobacterpylori sigma(80) family of promoter signals. J. Mol. Biol. 297:335-353.
41. Wang, G., D. A. Rasko, R. Sherburne, and D. E. Taylor. 1999. Molecular genetic basis for the variable expression of Lewis Y antigen in Helicobacter pylori: Analysis of the alpha (1,2) fucosyltransferase gene. Mol. Microbiol. 31:1265-1274.
42. Weiser, J. N., and N. Pan. 1998. Adaptation of Haemophilus influenzae to acquired and innate humoral immunity based on phase variation of lipopolysaccharide. Mol. Microbiol. 30:767-775.
43. Yakhnin, H., J. E. Babiarz, A. V. Yakhnin, and P. Babitzke. 2001. Expression of the Bacillus subtilis trpEDCFBA operon is influenced by translational coupling and Rho termination factor. J. Bacteriol. 183:5918-5926.
44. r 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA 97:7533-7538.
45. Zhao, H., X. Li, D. E. Johnson, I. Blomfield, and H. L. Mobley. 1997. In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Mol. Microbiol. 23:1009-1019.