Helicobacter pylori - A conundrum of genetic diversity

Microbiology

Volumn 144, Issue 11, 1998, Pages 2925-2939

  Marshall, David G ^a   Dundon, William G ^a   Beesley, Sarah M ^a   Smyth, Cyril J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Genetic diversity; Helicobacter pylori; Horizontal transfer; Natural transformation; Repetitive DNA

Indexed keywords

BACTERIAL GENE; BACTERIAL VIRULENCE; GENETIC VARIABILITY; GENOME; GENOTYPE; HELICOBACTER PYLORI; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; REVIEW;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 0031736760     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-144-11-2925     Document Type: Review

References (143)

1. Achtman, M. (1994). Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol Microbiol 11, 15-22.
2. Akopyants, N. S., Clifton, S. W., Kersulyte, D. & 7 other authors (1998). Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol 28, 37-53.
3. Akopyanz, N., Bukanov, N. O., Westblom, T. U., Kresovich, S. & Berg, D. E. (1992). DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res 20, 5137-5142.
4. Alloing, G., Granadel, C., Morrison, D. A. & Claverys, J.-P. (1996). Competence pheromone, oligopeptide permease, and induction of competence in Streptococcus pneumoniae. Mol Microbiol 21, 471-478.
5. Andrews, J. (1995). What if bacteria are modular organisms? ASM News 61, 627-632.
6. Appelmelk, B. J., Simoons-Smit, I., Negrini, R. & 17 other authors (1996). Potential role of molecular mimicry between Helicobacter pylori lipopolysaccharide and host Lewis blood group antigens in autoimmunity. Infect Immun 64, 2031-2040.
7. Appelmelk, B. J., Shiberu, B., Trinks, C. & 10 other authors (1998). Phase variation in Helicobacter pylori lipopolysaccharide. Infect Immun 66, 70-76.
8. Aspinall, G. O. & Monteiro, M. A. (1996). Lipopolysaccharides of Helicobacter pylori strains P466 and MO19: structures of the O antigen and core oligosaccharide chains. Biochemistry 35, 2498-2504.
9. Aspinall, G. O. & Moran, A. P. (1997). Helicobacter pylori lipopolysaccharide structure and mimicry of Lewis blood group antigens. In Pathogenesis and Host Response in Helicobacter pylori Infections, pp. 34-42. Edited by A. P. Moran & C. A. O'Morain. Bad Homburg: Normed Verlag.
10. Aspinall, G. O., Monteiro, M. A., Pang, H., Walsh, E. J. & Moran, A. P. (1994). O antigen chains in the lipopolysaccharide of Helicobacter pylori NCTC 11637. Carbohydr Lett 1, 151-156.
11. Atherton, J. C. (1997). The clinical relevance of strain types of Helicobacter pylori. Gut 40, 701-703.
12. Atherton, J. C., Cao, P., Peek, R. M., Tummuru, M. K. R., Blaser, M. J. & Cover, T. L. (1995). Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 270, 17771-17777.
13. Atherton, J., Peek, R. M., Jr, Tham, K. T., Cover, T. L. & Blaser, M. J. (1997). Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology 112, 92-99.
14. Bachellier, S., Gilson, E., Hofnung, M. & Hill, C. (1996). Repeated sequences. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, vol. 2, pp. 2588-2612. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
15. Berg, C. M. & Berg, D. E. (1996). Transposable elements: tools for microbial genetics. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, vol. 2, pp. 2012-2040. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
16. Berg, D. E., Hoffmann, P. S., Appelmelk, B. J. & Kusters, J. G. (1997a). The Helicobacter pylori genome sequence: genetic factors for long life in the gastric mucosa. Trends Microbiol 5, 468-474.
17. Berg, D. E., Gilman, R. H., Lelwala-Guruge, J. & 9 other authors (1997b). Helicobacter pylori populations in Peruvian patients. Clin Infect Dis 25, 996-1002.
18. Blaser, M. J. (1989). Campylobacter pylori in Gastritis and Peptic Ulcer Disease. New York: Igaku-Shoin Medical Publishers.
19. Blaser, M. J. (1996). Genetic basis for heterogeneity of Helicobacter pylori. In Helicobacter pylori: Basic Mechanisms to Clinical Cure 1996, pp. 33-39. Edited by R. H. Hunt & G. N. J. Tytgat. Dordrecht: Kluwer.
20. Blaser, M. J. (1997). Heterogeneity of Helicobacter pylori. Eur J Gastroenterol Hepatol 9 (suppl. 1), S3-S7.
21. Blaser, M. J., Perez-Perez, G. I., Kleanthous, H., Cover, T. L., Peek, R. M., Chyou, P. H., Stemmermann, G. N. & Normura, A. (1995). Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55, 2111-2115.
22. Buckley, M. J. M. & O'Morain, C. A. (1998). Helicobacter biology -discovery. Br Med Bull 54, 7-16.
23. Bukanov, N. O. & Berg, D. E. (1994). Ordered cosmid library and high-resolution physical-genetic map of Helicobacter pylori strain NCTC11638. Mol Microbiol 11, 509-523.
24. Calam, J. (1996). Clinician's Guide to Helicobacter pylori. London: Chapman & Hall Medical.
25. Cao, P. & Cover, T. L. (1997). High-level genetic diversity in the vapD chromosomal region of Helicobacter pylori. J Bacteriol 179, 2852-2856.
26. Catlin, B. W. (1981). Cell-to-cell transmission of chromosomal loci in Neisseria gonorrhoeae. In Genetic Exchange: a Celebration and a New Generation, Proceedings of the 25th Wind River Conference, pp. 310-325. Edited by U. Strieps. New York: Marcel Dekker.
27. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., Ghiara, P., Borodovsky, M., Rappuoli, R. & Covacci, A. (1996). cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93, 14648-14653.
28. Covacci, A. (1996). Mobilis in mobile: unexpected flexibility and quantum leaps in the Helicobacter pylori genome. In Helicobacter pylori: Basic Mechanisms to Clinical Cure 1996, pp. 40-49. Edited by R. H. Hunt & G. N. J. Tytgat. Dordrecht: Kluwer.
29. Covacci, A. & Rappuoli, R. (1998). Helicobacter pylori: molecular evolution of a bacterial quasi-species. Curr Opin Microbiol 1, 96-102.
30. Covacci, A., Censini, S., Bugnoli, M. & 8 other authors (1993). Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA 90, 5791-5795.
31. Covacci, A., Falkow, S., Berg, D. E. & Rappuoli, R. (1997a). Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori? Trends Microbiol 5, 205-208.
32. Covacci, A., Falkow, S., Censini, S. & 8 other authors (1997b). The cag pathogenicity island of Helicobacter pylori: origin, molecular biology and relevance to virulence. In Pathogenesis and Host Response in Helicobacter pylori Infections, pp. 88-100. Edited by A. P. Moran & C. A. O'Morain. Bad Homburg: Normed Verlag.
33. Cover, T. L. & Blaser, M. J. (1992). Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 267, 10570-10575.
34. Cover, T. L., Tummuru, M. K., Cao, P., Thompson, S. A. & Blaser, M. J. (1994). Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J Biol Chem 269, 10566-10577.
35. Crabtree, J. E., Xiang, Z., Lindley, I. J., Tompkins, D. S., Rappuoli, R. & Covacci, A. (1995). Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori. J Clin Pathol 48, 967-969.
36. Dempsey, J. A. F., Wallace, A. C. & Cannon, J. G. (1995). The physical map of the chromosome of a serotype A strain of Neisseria meningitidis shows complex rearrangements relative to the chromosome of the two mapped strains of the closely related species N. gonorrhoeae. J Bacteriol 177, 6390-6400.
37. van Doorn, L. J., Figueiredo, C., Rossau, R., Jannes, G., van Asbroeck, M., Sousa, J. C., Carneiro, F. & Quint, W. G. V. (1998a). Typing of Helicobacter pylori vacA gene and detection of cagA gene by PCR and reverse hybridization. J Clin Microbiol 36, 1271-1276.
38. van Doorn, L. J., Figueiredo, C., Sanna, R., Plaisier, A., Schneeberger, P., de Boer, W. & Quint, W. G. V. (1998b). Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 115, 58-66.
39. Dundon, W. G., Marshall, D. G., O'Moráin, C. A. & Smyth, C. J. (1998). The identification and characterization of a differentially expressed locus in Helicobacter pylori using arbitrarily primed PCR of RNA. Gastroenterology 114, abstract G3970, A968.
40. Dunn, B. E., Cohen, H. & Blaser, M. J. (1997). Helicobacter pylori. Clin Microbiol Rev 10, 720-741.
41. Dybvig, K. (1993). DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10, 465-471.
42. Eckloff, B. W., Podzorski, R. P., Kline, B. C. & Cockerill, F. R., III (1994). A comparison of 16S ribosomal DNA sequences from five isolates of Helicobacter pylori. Int J Syst Bacteriol 44, 320-323.
43. van der Ende, A., Rauws, E. A., Feller, M., Mulder, C. J., Tytgat, G. N. & Dankert, J. (1996). Heterogeneous Helicobacter pylori isolates from members of a family with a history of peptic ulcer disease. Gastroenterology 111, 638-647.
44. Farthing, M. J. G. & Patchett, S. E. (1998). Helicobacter Infection. London: The Royal Society of Medicine.
45. Fleischmann, R. D., Adams, M. D., White, O. & 37 other authors (1995). Whole-genome random sequencing and assembly of Haemophilus Rd. Science 269, 496-512.
46. Forbes, K. J., Fang, Z. & Pennington, T. H. (1995). Allelic variation of the Helicobacter pylori flagellin genes fla A and flaB: its consequences for strain typing schemes and population structures. Epidemiol Infect 114, 257-266.
47. Forsyth, M. H., Atherton, J. C., Blaser, M. J. & Cover, T. L. (1998). Heterogeneity in levels of vacuolating cytotoxin gene (vacA) transcription among Helicobacter pylori strains. Infect Immun 66, 3088-3094.
48. Foxall, P. A., Hu, L.-T. & Mobley, H. L. T. (1992). Use of polymerase chain reaction-amplified Helicobacter pylori urease structural genes for differentiation of isolates. J Clin Microbiol 30, 739-741.
49. Fujimoto, S., Marshall, B. & Blaser, M. J. (1994). PCR-based restriction fragment length polymorphism typing of Helicobacter pylori. J Clin Microbiol 32, 331-334.
50. Gálvez, A., Maqueda, M., Martinez-Bueno, M. & Valdivia, E. (1998). Publication rates reveal trends in microbiological research. ASM News 64, 269-275.
51. Ge, M. F., Chan, N. W. C., Palcic, M. & Taylor, D. E. (1997). Cloning and heterologous expression of an α1,3-fucosyltransferase gene from the gastric pathogen Helicobacter pylori. J Biol Chem 272, 21357-21363.
52. Go, M. F., Chan, Y. K., Yersalovk, J., Koeuth, T., Graham, D. Y. & Lupski, J. R. (1995). Cluster analysis of Helicobacter pylon genomic DNA fingerprints suggests gastroduodenal diseasespecific associations. Scand J Gastroenterol 30, 640-646.
53. Go, M. F., Kapur, V., Graham, D. Y. & Musser, J. M. (1996). Population genetic analysis of Helicobacter pylori by multilocus enzyme electrophoresis: extensive allelic diversity and recombinational population structure. J Bacteriol 178, 3934-3938.
54. Goldman, B. & Kranz, R. (1998). Evolution and horizontal transfer of an entire biosynthetic pathway for cytochrome c biogenesis: Helicobacter, Deinococcus, Archae and more. Mol Microbiol 27, 871-874.
55. Goodwin, C. S. & Worsley, B. W. (1993). Helicobacter pylori: Biology and Clinical Practice. Boca Raton, FL: CRC Press.
56. Hacker, J., Blum-Oehler, G., Mühldorfer, I. & Tschäpe, H. (1997). Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23, 1089-1097.
57. Hancock, R. E. W., Alm, R., Bina, J. & Trust, T. (1998). Helicobacter pylori: a surprisingly conserved bacterium. Nat Biotechnol 16, 216-218.
58. Hazell, S. L., Andrews, R. H., Mitchell, H. M. & Daskalopoulous, G. (1997). Genetic relationship among isolates of Helicobacter pylori: evidence for the existence of a Helicobacter pylori species complex. FEMS Microbiol Lett 150, 27-32.
59. Heintschel von Heinegg, E., Nalik, H. P. & Schmid, E. N. (1993). Characterisation of Helicobacter pylori phage (HP1). J Med Microbiol 38, 245-249.
60. Hobbs, M. M., Seiler, A., Achtman, M. & Cannon, J. G. (1994). Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol Microbiol 12, 171-180.
61. Hofreuter, D., Odenbreit, S., Henke, G. & Hass, R. (1998). Natural competence for DNA transformation in Helicobacter pylon: identification and genetic characterization of the comB locus. Mol Microbiol 28, 1027-1038.
62. Hood, D. W., Deadman, M. E., Jennings, M. P., Bisercic, M., Fleischmann, R. D., Venter, J. C. & Moxon, E. R. (1996). DNA repeats identify novel virulence genes in Haemophilus influenzae. Proc Natl Acad Sci USA 93, 11121-11125.
63. Höök-Nikanne, J., Berg, D. E., Peek, R. M., Jr, Kersulyte, D., Tummuru, M. K. R. & Blaser, M. J. (1998). DNA sequence conservation and diversity in transposable element IS606 of Helicobacter pylori. Helicobacter 3, 79-85.
64. Hunt, R. H. & Tytgat, G. N. J. (1996). Helicobacter pylori: Basic Mechanisms to Clinical Cure 1996. Dordrecht: Kluwer.
65. Ilver, D., Arnquist, A., Ögren, J. & 7 other authors (1998). Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279, 373-377.
66. Ito, Y., Azuma, T., Ito, S. & 7 other authors (1997). Analysis and typing of the vacA gene from cagA-positive strains of Helicobacter pylori isolated in Japan. J Clin Microbiol 35, 1710-1714.
67. Jiang, Q., Hiratsuka, K. & Taylor, D. E. (1996). Variability of gene order in different Helicobacter pylori strains contributes to genome diversity. Mol Microbiol 20, 833-842.
68. Jorgensen, M., Daskalopoulos, G., Warburton, C., Mitchell, H. M. & Hazell, S. L. (1996). Multiple strain colonization and metronidazole resistance in Helicobacter pylori-infected patients: identification from sequential and multiple biopsy specimens. J Infect Dis 174, 631-635.
69. Josenhans, C. & Suerbaum, S. (1997). Flagella and motility of Helicobacter pylori. In Pathogenesis and Host Response in Helicobacter pylori Infections, pp. 6-15. Edited by A. P. Moran & C. A. O'Morain. Bad Homburg: Normed Verlag.
70. Kleanthous, H., Clayton, C. L. & Tabaqchali, S. (1991). Characterisation of a plasmid from Helicobacter pylori encoding a replication protein common to plasmids in Gram-positive bacteria. Mol Microbiol 5, 2377-2389.
71. Krawiec, S. & Riley, M. (1990). Organization of the bacterial chromosome. Microbiol Rev 54, 502-539.
72. Kuipers, E. J. & Blaser, B. J. (1998). Helicobacter pylori and gastroduodenal disorders. In Emerging Pathogens, pp. 191-206. Edited by W. M. Scheld, D. Armstrong & J. M. Hughes. Washington, DC: American Society for Microbiology.
73. Kuipers, E. J., Israel, D. A., Kusters, J. G. & Blaser, B. J. (1998). Evidence for a conjugation-like mechanism of DNA transfer in Helicobacter pylori. J Bacteriol 180, 2901-2905.
74. Langenberg, W., Rauws, E. A. J., Widjojokusumo, A., Tytgat, G. N. J. & Zanen, H. C. (1986). Identification of Campylobacter pyloridis isolates by restriction endonuclease DNA analysis. J Clin Microbiol 24, 414-417.
75. Lee, A. & Hazell, S. L. (1988). Campylobacter pylori in health and disease: an ecological perspective. Microb Ecol Health Dis 1, 1-16.
76. Lee, A. & Mégraud, F. (1996). Helicobacter pylori: Techniques for Clinical Diagnosis and Basic Research. London: W. B. Saunders.
77. Levinson, G. & Gutman, G. A. (1987). Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4, 203-221.
78. Lloyd, R. G. & Low, K. B. (1996). Homologous recombination. In Escherichia coli and Salmonella : Cellular and Molecular Biology, 2nd edn, vol. 2, pp. 2236-2255. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
79. Logan, R. P. H. & Berg, D. E. (1996). Genetic diversity of Helicobacter pylori. Lancet 348, 1462-1463.
80. Lorenz, M. G. & Wackernagel, W. (1994). Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58, 563-602.
81. Maeda, S., Ogura, K., Yoshida, H., Funai, F., Ikenoue, T., Kato, N., Shiratori, Y. & Omata, M. (1998). Major virulence factors, VacA and CagA, are commonly positive in Helicobacter pylori isolates in Japan. Gut 42, 338-343.
82. Malfertheiner, P. & Ditschuneit, H. (1990). Helicobacter pylori, Gastritis and Peptic Ulcer. Berlin: Springer.
83. Marshall, B. J. (1989). History of the discovery of C. pylori. In Campylobacter pylori in Gastritis and Peptic Ulcer Disease, pp. 7-23. Edited by M. J. Blaser. New York: Igaku-Skoin Medical Publishers.
84. Marshall, B. J. & Warren, J. R. (1984). Unidentified curved bacilli in the stomachs of patients with gastritis and peptic ulceration. Lancet i, 1311-1315.
85. Marshall, B. J., McCallum, R. W. & Guerrant, R. L. (1991). Helicobacter pylori in Peptic Ulceration and Gastritis. Oxford: Blackwell Scientific Publications.
86. Marshall, D. G. (1996). Population analysis of Helicobacter pylori. PhD thesis, Trinity College, University of Dublin.
87. Marshall, D. G., Chua, A., Keeling, P. W. N., Sullivan, D. J., Coleman, D. C. & Smyth, C. J. (1995). Molecular analysis of Helicobacter pylori populations in antral biopsies from individual patients using randomly amplified polymorphic DNA (RAPD) fingerprinting. FEMS lmmunol Med Microbiol 10, 317-324.
88. Marshall, D. G., Coleman, D. C., Sullivan, D. J., Xia, H., O'Morain, C. A. & Smyth, C. J. (1996). Genomic DNA fingerprinting of clinical isolates of Helicobacter pylori using oligonucleotide probes containing repetitive sequences. J Appl Bacteriol 81, 509-517.
89. Martin, S. L., Edbroke, M. R., Hodgman, T. C., van den Eijnden, D. H. & Bird, M. I. (1997). Lewis x biosynthesis in Helicobacter pylori: molecular cloning of an α-(1,3)-fucosyltransferase gene. J Biol Chem 272, 21349-21356.
90. Matic, I., Taddei, F. & Radman, M. (1996). Genetic barriers among bacteria. Trends Microbiol 4, 69-73.
91. Maynard Smith, J. (1995). Do bacteria have population genetics ? In Population Genetics of Bacteria, pp. 1-12. Edited by S. Baumberg, J. P. W. Young, E. M. H. Wellington & J. R. Saunders. Cambridge: Cambridge University Press.
92. Maynard Smith, J., Dowson, C. G. & Spratt, B. G. (1991). Localized sex in bacteria. Nature 349, 29-31.
93. Miehlke, S., Kibler, K., Kim, J. G., Figura, N., Small, S. M., Graham, D. Y. & Go, M. F. (1996). Allelic variation in the cagA gene of Helicobacter pylori obtained from Korea compared to the United States. Am J Gastroenterol 91, 1322-1325.
94. Mobley, H. L. T., Fulkerson, J., Jr, Hendricks, J. K. & Garner, R. M. (1997). Expression of catalytically active urease by Helicobacter pylori. In Pathogenesis and Host Response in Helicobacter pylori Infections, pp. 58-66. Edited by A. P. Moran & C. A. O'Morain. Bad Homburg: Normed Verlag.
95. Moran, A. P. & O'Morain, C. A. (1997). Pathogenesis and Host Response in Helicobacter pylori Infections. Bad Homburg: Normed Verlag.
96. Moxon, E. R., Rainey, P. B., Nowak, M. A. & Lenski, R. E. (1994). Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4, 24-33.
97. Nedenskov-Sørensen, P., Bukholm, G. & Boøvre, K. (1990). Natural competence for genetic transformation in Campylobacter pylori. J Infect Dis 161, 365-366.
98. Negrini, R., Savio, M., Graffeo, M., Rolfi, F. & Ghielmi, S. (1993). Auto-antibodies and gastric Helicobacter pylori infection: does autoimmunity affect progression to atrophic gastritis? Eur J Gastroenterol Hepatol 5 (suppl. 2), S27-S29.
99. NIH Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease (1994). Helicobacter pylori in peptic ulcer disease. J Am Med Assoc 272, 65-69.
100. Nwokolo, C. U., Bickley, J., Attard, A. R., Owen, R. J., Costas, M. & Fraser, I. A. (1992). Evidence of clonal variants of Helicobacter pylori in three generations of a duodenal ulcer disease family. Gut 33, 1323-1327.
101. Ohta-Tada, U., Takagi, A., Koga, Y., Kamiya, S. & Miwa, T. (1997). Flagellin gene diversity among Helicobacter pylori strains and IL-8 secretion from gastric epithelial cells. Scand J Gastroenterol 32, 455-459.
102. Ó'Moráin, C. A. & O'Connor, H. (1994). Helicobacter pylori: Implications and Practice. Bad Homburg: Normed Verlag.
103. Oudbier, J. H., Langenberg, W., Rauws, E. A. J. & Bruin-Mosch, C. (1990). Genotypic variation of Campylobacter pylori from gastric mucosa. J Clin Microbiol 28, 559-565.
104. Owen, R. J., Hunton, C., Bickley, J., Moreno, M. & Linton, D. (1992). Ribosomal RNA gene restriction patterns of Helicobacter pylori: analysis and appraisal of HaeIII digests as a molecular typing system. Epidemiol Infect 109, 35-47.
105. Pan, Z.-J., van der Hulst, R. W. M., Feller, M., Xiao, S.-D., Tytgat, G. N. J., Dankert, J. & van der Ende, A. (1997). Equally high prevalences of infection with cagA-positive Helicobacter pylori in Chinese patients with peptic ulcer disease and those with chronic gastritis-associated dyspepsia. J Clin Microbiol 35, 1344-1347.
106. Pan, Z.-J., Berg, D. E., van der Hulst, R. W. M., Su, W.-W., Raudonikiene, A., Xiao, S.-D., Dankert, J., Tytgat, G. N. J. & van der Ende, A. (1998). Presence of vacuolating cytotoxin production and distribution of distinct vacA alleles in Helicobacter pylori from China. J Infect Dis 178, 220-226.
107. Peek, R. M., Jr, Thompson, S. A., Atherton, J. C., Blaser, M. J. & Miller, G. G. (1996). Expression of iceA, a novel ulcer-associated H. pylori gene, is induced by contact with gastric epithelial cells and is associated with enhanced mucosal IL-8. Gut 39 (suppl. 2), A71.
108. Pérez-Pérez, G. I. & Parsonnet, J. (1994). Epidemiology of Helicobacter pylori infections. In Helicobacter pylori: Implications and Practice, pp. 52-57. Edited by C. A. Ó'Moráin & H. O'Connor. Bad Homburg: Normed Verlag.
109. Pestova, E. V., Håvarstein, L. S. & Morrison, D. A. (1996). Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Mol Microbiol 21, 853-862.
110. Phadnis, S. H., Parlow, M. H., Levy, L., Ilver, D., Caulkins, C. M., Connors, J. B. & Dunn, B. E. (1996). Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect Immun 64, 905-912.
111. Rathbone, B. J. & Heatley, R. V. (1989a). Campylobacter pylori and Gastroduodenal Disease. Oxford: Blackwell Scientific Publications.
112. Rathbone, B. J. & Heatley, R. V. (1989b). The historical associations between bacteria and peptic-ulcer disease. In Campylobacter pylori and Gastroduodenal Disease, pp. 1-4. Oxford: Blackwell Scientific Publications.
113. Riccardi, V. M. & Rotter, J. I. (1994). Familial Helicobacter pylori infection. Societal factors, human genetics, and bacterial genetics. Ann Intern Med 120, 1043-1045.
114. Rudi, J., Kolb, C., Maiwald, M., Kuck, D., Sieg, A., Galle, P. R. & Stremmel, W. (1998). Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA expression, cytotoxin production, and associated diseases. J Clin Microbiol 36, 944-948.
115. Saunders, K. E., McGovern, K. J. & Fox, J. G. (1997). Use of pulse-field gel electrophoresis to determine genomic diversity in strains of Helicobacter hepaticus from geographically distant locations. J Clin Microbiol 35, 2859-2863.
116. Saunders, N. J., Peden, J. F., Hood, D. W. & Moxon, E. R. (1998). Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27, 1091-1098.
117. Shimoyama, T., Fukuda, S., Tanaka, M., Mikami, T., Saito, Y. & Munakata, A. (1997). High prevalence of CagA-positive Helicobacter pylori strains in Japanese asymptomatic patients and gastric cancer patients. Scand J Gastroenterol 32, 465-468.
118. Shortridge, V. D., Stone, G. G., Flamm, R. K., Beyer, J., Versalovic, J., Graham, D.W. & Tanaka, S. K. (1997). Molecular typing of Helicobacter pylori isolates from a multicenter US clinical trial by ureC restriction fragment length polymorphism. J Clin Microbiol 35, 471-473.
119. Simor, A. E., Shames, B., Drumm, B., Sherman, P., Low, D. E. & Penner, J. L. (1990). Typing of Campylobacter pylori by bacterial DNA restriction endonuclease analysis and determination of plasmid profile. J Clin Microbiol 28, 83-86.
120. Smith, H. O., Tomb, J.-F., Dougherty, B. A., Fleischmann, R. D. & Venter, J. C. (1995). Frequency and distribution of DNA uptake signal sequences in the Haemophilus influenzae Rd genome. Science 269, 538-540.
121. Solnick, J. V., Hansen, L. M. & Syvanen, M. (1997). The major sigma factor (RpoD) from Helicobacter pylori and other Gram-negative bacteria shows an enhanced rate of divergence. J Bacteriol 179, 6196-6200.
122. Strobel, S., Bereswill, S., Balig, P., Allgaier, P., Sonntag, H.-G. & Kist, M. (1998). Identification and analysis of a new vacA genotype variant of Helicobacter pylori in different patient groups in Germany. J Clin Microbiol 36, 1285-1289.
123. Suerbaum, S. (1995). The complex flagella of gastric Helicobacter species. Trends Microbiol 3, 168-170.
124. Taddei, F., Matic, I., Godelle, B. & Radman, M. (1997). To be a mutator, or how pathogenic and commensal bacteria can evolve rapidly. Trends Microbiol 5, 427-429.
125. Takami, S., Hayashi, T., Tonokatsu, Y., Shimoyama, T. & Tamura, T. (1993). Chromosomal heterogeneity of Helicobacter pylori by pulsed-field gel electrophoresis. Int J Med Microbiol Virol Parasitol Infect Dis 280, 120-127.
126. Takami, S., Hayashi, T., Akashi, H., Shimoyama, T. & Tamura, T. (1994). Genetic heterogeneity of Helicobacter pylori by pulse-field electrophoresis and re-evaluation of DNA homology. Eur J Gastroenterol Hepatol 6 (suppl. 1), S53-S56.
127. Taylor, D. E. & Blaser, M. J. (1991). The epidemiology of Helicobacter pylori infection. Epidemiol Rev 13, 42-59.
128. Taylor, D. E., Eaton, M., Chang, N. & Salama, S. M. (1992). Construction of a Helicobacter pylori genome map and demonstration of diversity at the genome level. J Bacteriol 174, 6800-6806.
129. Taylor, D. E., Chang, N., Taylor, N. S. & Fox, J. G. (1994). Genome conservation in Helicobacter mustelae as determined by pulse-field gel electrophoresis. FEMS Microbiol Lett 118, 31-36.
130. Taylor, D. N. & Parsonnet, J. (1995). Epidemiology and natural history of H. pylori infections. In Infections of the Gastrointestinal Tract, pp. 551-564. Edited by M. J. Blaser, P. F. Smith, J. Ravdin, H. Greenberg & R. L. Guerrant. New York: Raven Press.
131. Taylor, N. S., Fox, J. G., Akopyants, N. S. & 8 other authors (1995). Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol 33, 918-923.
132. Tomb, J.-F., White, O., Kerlavage, A. R. & 39 other authors (1997). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547.
133. Trun, N. J. & Marko, J. F. (1998). Architecture of a bacterial chromosome. ASM News 64, 276-283.
134. Tummuru, M. K., Cover, T. L. & Blaser, M. J. (1993). Cloning and expression of a high molecular-mass major antigen of Helicobacter pylon: evidence of linkage to cytotoxin production. Infect Immun 61, 1799-1809.
135. Tummuru, M. K., Cover, T. L. & Blaser, M. J. (1994). Mutation of the cytotoxin-associated cagA gene does not affect the vacuolating cytotoxin activity of Helicobacter pylori. Infect Immun 62, 2609-2613.
136. Vanet, A. & Labigne, A. (1998). Evidence for specific secretion rather than autolysis in the release of some Helicobacter pylori proteins. Infect Immun 66, 1023-1027.
137. Wang, H.-J., Kuo, C.-H., Yeh, A. A. M., Chang, P. C. L & Wang, W.-C. (1998). Vacuolating toxin production in clinical isolates of Helicobacter pylori with different vacA genotypes. J Infect Dis 178, 207-212.
138. Wang, Y., Roos, K. P. & Taylor, D. E. (1993). Transformation of Helicobacter pylori by chromosomal metronidazole resistance and by a plasmid with a selectable chloramphenicol resistance marker. J Gen Microbiol 139, 2485-2493.
139. Warren, J. R. & Marshall, B. J. (1983). Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet i, 1273-1275.
140. Xiang, Z., Censini, S., Bayeli, P. F., Telford, J. L., Figura, N., Rappuoli, R. & Covacci, A. (1995). Analysis and expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two major types and that CagA is not necessary for expression of the vacuolating cytotoxin. Infect Immun 63, 94-98.
141. Xu, Q., Peek, R. M., Jr, Miller, G. G. & Blaser, M. J. (1997). The Helicobacter pylori genome is modified at CATG by the product of hpyIM. J Bacteriol 179, 6807-6815.
142. Yamaoka, Y., Kodama, T., Kashima, K., Graham, D. Y. & Sepulveda, A. R. (1998). Variants of the 3′ region of the cagA gene in Helicobacter pylori isolates from patients with different H. pylori-associated diseases. J Clin Microbiol 36, 2258-2263.
143. Yoshimura, H. H., Evans, D. G. & Graham, D. Y. (1993). DNA-DNA hybridization demonstrates apparent genetic differences between Helicobacter pylori from patients with duodenal ulcer and asymptomatic gastritis. Dig Dis Sci 38, 1128-1131.