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Volume 150, Issue 1

Analysis of geospecific markers for variants in patients from Japan and Nigeria by triple-locus nucleotide sequence typing Free

Abstract

Human migrations and geographical separation over long periods may have resulted in ecologically distinct populations of infecting individuals in different continents. This study used nucleotide sequence analysis with the aim of defining population-specific genomic motifs in isolates from East Asian and African dyspeptic patients. Sequences of internal fragments (542–627 bp) of three housekeeping genes (, and ) were analysed for 85 isolates from individuals in Japan and China (30 isolates), Nigeria and South Africa (14 isolates), the United Kingdom (32 isolates), and nine miscellaneous reference strains. Phylogenetic analyses showed a high degree of intra-set relatedness amongst sequences from the Japanese and Nigerian isolates, with each robustly segregated as distinct lineages irrespective of presence and allelic type. All strains had unique combined sequence types except for identical paired (antrum/corpus) isolates. Population-specific polymorphisms were identified within each gene which were combined to provide unique motifs defining the Japanese and Nigerian regional populations. The alleles were present at variable frequencies in UK and South African isolates. The findings provide unique evidence of positive selection for conserved nucleotide sites linked to the geographical separation in Japan of a strain subpopulation for which we propose the designation geovar ‘orientalis’.

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2004-01-01
2024-04-27
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References

  1. Achtman M., Azuma T., Berg D. E. & 7 other authors; 1999; Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 32:459–470 [CrossRef]
     [Google Scholar]
  2. Alm R. A., Ling L. S., Moir D. T. & 20 other authors; 1999; Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176–180 [CrossRef]
     [Google Scholar]
  3. Ando I., Peek R. M., Pride D. & 8 other authors; 2002; Polymorphisms of Helicobacter pylori HP0638 reflect geographic origin and correlate with cagA status. J Clin Microbiol 40:239–246 [CrossRef]
     [Google Scholar]
  4. Atherton J. C., Cover T. L., Twells R. J., Hawkey C. J., Blaser M. J. 1999; Simple and accurate PCR-based system for typing vacuolating cytotoxin alleles of Helicobacter pylori. J Clin Microbiol 37:2979–2982
     [Google Scholar]
  5. Blaser M. J. 1998; Helicobacters are indigenous to the human stomach: duodenal ulceration is due to changes in gastric microecology in the modern era. Gut 43:721–727 [CrossRef]
     [Google Scholar]
  6. Calam J., Baron J. H. 2001; Pathophysiology of duodenal and gastric ulcer and gastric cancer. Br Med J 323:980–982 [CrossRef]
     [Google Scholar]
  7. Campbell S., Fraser A., Holliss B., Schmid J., O’Toole P. W. 1997; Evidence for ethnic tropism of Helicobacter pylori. Infect Immun 65:3708–3712
     [Google Scholar]
  8. Campbell D. I., Warren B. F., Thomas J. E., Figura N., Telford J. L. K., Sullivan P. B. 2001; The African Enigma: low prevalence of gastric atrophy, high prevalence of chronic inflammation in West African adults and children. Helicobacter 6:263–267 [CrossRef]
     [Google Scholar]
  9. Covacci A., Telford J. L., Del Guidice G., Parsonnet J., Rappuoli R. 1999; Helicobacter pylori virulence and genetic geography. Science 284:1328–1333 [CrossRef]
     [Google Scholar]
  10. Dunn B. E., Cohen H., Blaser M. J. 1997; Helicobacter pylori. Clin Microbiol Rev 10:720–741
     [Google Scholar]
  11. Falush D., Kraft C., Taylor N. S., Correa P., Fox J. G., Achtman M., Suerbaum S. 2001; Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98:15056–15061 [CrossRef]
     [Google Scholar]
  12. Falush D., Wirth T., Linz B. & 15 other authors; 2003; Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585 [CrossRef]
     [Google Scholar]
  13. 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
     [Google Scholar]
  14. Glupczynski Y., Mégraud F., Lopez-Brea M., Andersen L. P. 2001; European multicentre survey of in vitro antimicrobial resistance in Helicobacter pylori. Eur J Clin Microbiol Infect Dis 20:820–823 [CrossRef]
     [Google Scholar]
  15. Hall T. A. 1999; BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
     [Google Scholar]
  16. Holcombe C., Omotara B. A., Eldridge J., Jones D. M. 1992; H. pylori, the most common bacterial infection in Africa: a random serological study. Am J Gastroenterol 97:28–30
     [Google Scholar]
  17. Holcombe C., Kaluba J., Lucas S. B. 1994; Helicobacter pylori infection and gastritis in healthy Nigerians. Eur J Epidemiol 10:223–225 [CrossRef]
     [Google Scholar]
  18. Hynes S. O., Broutet N. Eurohepygast Study Group Wadstrom T., Mikelsaar M., O’Toole P. W. 2002; Phenotypic variation of Helicobacter pylori isolates from geographically distinct regions detected by lectin typing. J Clin Microbiol 40:227–232 [CrossRef]
     [Google Scholar]
  19. 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
     [Google Scholar]
  20. Jukes T. H., Cantor C. R. 1969; Evolution of protein molecules. In Mammalian Protein Metabolism III pp. 21–132Edited by Munro H. N. New York: Academic Press;
     [Google Scholar]
  21. Kersulyte D., Mukhopadhyay A. K., Velapatiño B. & 28 other authors; 2000; Differences in genotypes of Helicobacter pylori from different human populations. J Bacteriol 182:3210–3218 [CrossRef]
     [Google Scholar]
  22. Lambert R., Guilloux A., Oshima A., Pompe-Kirn V., Bray F., Parkin M., Ajiki W., Tsukuma H. 2002; Incidence and mortality from stomach cancer in Japan, Slovenia and the USA. Int J Cancer 97:811–818 [CrossRef]
     [Google Scholar]
  23. Lee A., O’Rourke J., Corazon De Ungria M., Robertson B., Daskalopoulos G., Dixon M. F. 1997; A standardised mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386–1397 [CrossRef]
     [Google Scholar]
  24. Lundstrom A. M., Sundaeus V., Bolin I. 2001; The 26-kilodalton, AhpC homologue, of Helicobacter pylori is also produced by other Helicobacter species. Helicobacter 6:44–54 [CrossRef]
     [Google Scholar]
  25. McGowan C. C., Cover T. L., Blaser M. J. 1997; Analysis of F1F0-ATPase fromHelicobacter pylori.. Infect Immun 65:2640–2647
     [Google Scholar]
  26. Mobley H. L. T. 2001; Urease. In Helicobacter pylori: Physiology and Genetics pp. 179–191Edited by Mobley H. L. T., Mendz G. L., Hazell S. L. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  27. Owen R. J., Xerry J. 2003; Tracing clonality of Helicobacter pylori infecting family members from analysis of DNA sequences of three housekeeping genes (ureI,atpA and ahpC), deduced amino acid sequences, and pathogenicity-associated markers (cagA and vacA). J Med Microbiol 52:515–524 [CrossRef]
     [Google Scholar]
  28. Owen R. J., Bickley J., Lastovica A., Dunn J. P., Borman P., Hunton C. 1992; Ribosomal RNA gene patterns of Helicobacter pylori from surgical patients with healed and recurrent peptic ulcers. J Epidemiol Infect 108:39–50 [CrossRef]
     [Google Scholar]
  29. Owen R. J., Peters T. M., Varea R., Teare E. L., Saverymuttu S. 2001a; Molecular epidemiology of Helicobacter pylori in England: prevalence of cag pathogenicity island markers and IS605 presence in relation to patient age and severity of gastric disease. FEMS Immunol Med Microbiol 30:65–71 [CrossRef]
     [Google Scholar]
  30. Owen R. J., Taylor D. E., Wang G., van Doorn L.-J. 2001b; Heterogeneity and subtyping. In Helicobacter pylori: Physiology and Genetics pp. 343–378Edited by Mobley H. L. T., Mendz G. L., Hazell S. L. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  31. Owen R. J., Xerry J., Peters T. M., Teare E. L. 2002; Surveillance and clinical relevance of vacA genotypes of Helicobacter pylori infecting dyspeptic patients in mid-Essex. Commun Dis Public Health 5:106–111
     [Google Scholar]
  32. Owen R. J., Sharp S., Lawson A. J., Durrani Z., Rijpkema S., Kidd M. 2003; Investigation of the biological relevance of Helicobacter pylori cagE locus diversity, presence of CagA tyrosine phosphorylation motifs and vacuolating cytotoxin genotype on IL-8 induction in gastric epithelial cells. FEMS Imunol Med Microbiol 36:135–140 [CrossRef]
     [Google Scholar]
  33. Pan Z. J., Berg D. E., van der Hulst R. W., Su W. W., Raudonikiene A., Xiao S. D., Dankert J., Tytgat G. N., van der Ende A. 1998; Prevalence of vacuolating cytotoxin production and distribution of distinct vacA alleles in Helicobacter pylori from China. . J Infect Dis 178:220–226 [CrossRef]
     [Google Scholar]
  34. Pounder R. E., Ng D. 1995; The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther 9:33–39
     [Google Scholar]
  35. Rozas J., Rozas R. 1995; DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetics parameters from DNA sequence data. Comput Appl Biosci 11:621–625
     [Google Scholar]
  36. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees.. Mol Biol Evol 4:406–425
     [Google Scholar]
  37. Slater E., Owen R. J., Williams M., Pounder R. 1999; Conservation of the cag pathogenicity island of Helicobacter pylori and associations with vacuolating cytotoxin alleles and IS605. Gastroenterology 117:1308–1315 [CrossRef]
     [Google Scholar]
  38. Solca N. M., Bernasconi M. V., Valsangiacomo C., Van Doorn L.-J., Piffaretti J.-C. 2001; Population genetics of Helicobacter pylori in the southern part of Switzerland analysed by sequencing of four housekeeping genes(atpD, glnA, scoB and recA), and by vacA, cagA, iceA and IS605 genotyping. Microbiology 147:1693–1707
     [Google Scholar]
  39. Staley J. T. 1999; Bacterial biodiversity: a time for place. ASM News 65:681–687
     [Google Scholar]
  40. Suerbaum S., Smith J. M., Bapumia K., Morelli G., Smith N. H., Kunstmann E., Dyrek I., Achtman M. 1998; Free recombination within Helicobacter pylori.. Proc Natl Acad Sci U S A 95:12619–12624 [CrossRef]
     [Google Scholar]
  41. Suerbaum S., Kraft C., Dewhirst F. E., Fox J. G. 2002; Helicobacter nemestrinae ATCC 4939T is a strain of Helicobacter pylori(Marshall et al., 1985) Goodwin et al. 1989, and H. nemestrinae Bronsdon et al., 1991 is therefore a junior heterotypic synonym of Helicobacter pylori. Int J Syst Evol Microbiol 52:437–439
     [Google Scholar]
  42. 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 [CrossRef]
     [Google Scholar]
  43. Van de Peer Y., De Wachter R. 1994; TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570
     [Google Scholar]
  44. van Doorn L. J., Figueiredo C., Sanna R.7 other authors 1998; Expanding allelic diversity of Helicobacter pylori vacA.. J Clin Microbiol 36:2597–2603
     [Google Scholar]
  45. van der Ende A., Pan Z. J., Bart A., Rene W., van der Hulst M., Feller M., Xiao S. D., Tytgat G. N. J. 1998; cagA-positive Helicobacter pylori populations in China and The Netherlands are distinct. Infect Immun 66:1822–1826
     [Google Scholar]
  46. Weeks D. L., Eskandari S., Scott D. R., Sachs G. 2000; A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287:482–485 [CrossRef]
     [Google Scholar]
  47. Wilson K. 1987; Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology pp. 241–245Edited by Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Smith J. A., Seidman J. G., Struh K. New York: Wiley;
     [Google Scholar]
  48. 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-associated diseases. J Clin Microbiol 36:2258–2263
     [Google Scholar]
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Analysis of geospecific markers for Helicobacter pylori variants in patients from Japan and Nigeria by triple-locus nucleotide sequence typing
Microbiology 150, 151 (2004); https://doi.org/10.1099/mic.0.26467-0
/content/journal/micro/10.1099/mic.0.26467-0
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