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Volume 149, Issue 7

tissue tropism: mouse-colonizing strains can target different gastric niches Free

Abstract

Studies with the mouse-adapted strain SS1 had supported an idea that infections by this pathogen start in the gastric antrum and spread to the corpus after extensive mucosal damage. This paper shows that the unrelated strain X47 colonizes the corpus preferentially. Differences between strains in preferred gastric region were detected by co-inoculating mice with a mixture of SS1 and X47, and genotyping recovered after 2–8 weeks of infection by allele PCR and RAPD fingerprinting. Mixed infections were found in each of 59 co-inoculated young C57BL/6J mice. On average, however, SS1 was fourfold more abundant than X47 in the antrum and X47 was threefold more abundant than SS1 in the corpus. Similar results were obtained in mice inoculated first with one strain and then the other strain 2 weeks later. SS1 was even more abundant in the antrum of elderly (>1 year old) mice (97 % of isolates). Qualitatively similar SS1 and X47 tissue distributions were seen using unrelated mouse lines (AKR/J, A/J, DBA/2J, BALB/cJ, LG/J, SM/J), but with significantly different SS1 : X47 ratios in some cases. These results suggest the existence of at least two distinct gastric niches whose characteristics may be affected by host genotype and age (physiology), and indicate that strains differ in how effectively they colonize each niche. Differences among gastric regions and the mixed infections that these allow may contribute to diversity and genome evolution.

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  • Accepted:
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Keyword(s): RAPD, random amplified polymorphic DNA
SGM
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2003-07-01
2024-04-25
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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
     [Google Scholar]
  2. 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
     [Google Scholar]
  3. Allen L. A. 2000; Modulating phagocyte activation: the pros and cons of Helicobacter pylori virulence factors. J Exp Med 191:1451–1454
     [Google Scholar]
  4. 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
     [Google Scholar]
  5. Amieva M. R., Salama N. R., Tompkins L. S., Falkow S. 2002; Helicobacter pylori enter and survive within multivesicular vacuoles of epithelial cells. Cell Microbiol 4:677–690
     [Google Scholar]
  6. Anonymous 1986; Rapid identification of pyloric Campylobacter in Peruvians with gastritis. Dig Dis Sci 31:1089–1094
     [Google Scholar]
  7. Atherton J. C., Cao P., Peek R. M. Jr, Tummuru M. K., Blaser M. J., Cover T. L. 1995; Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori . Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem 270:17771–17777
     [Google Scholar]
  8. Bayerdorffer E., Oertel H., Lehn N., Kasper G., Mannes G. A., Sauerbruch T., Stolte M. 1989; Topographic association between active gastritis and Campylobacter pylori colonisation. J Clin Pathol 42:834–839
     [Google Scholar]
  9. Berg D. E., Gilman R. H., Lelwala-Guruge J. 9 other authors 1997; Helicobacter pylori populations in Peruvian patients. Clin Infect Dis 25:996–1002
     [Google Scholar]
  10. Bijlsma J. J., Lie-A-Ling M., Nootenboom I. C., Vandenbroucke-Grauls C. M., Kusters J. G. 2000; Identification of loci essential for the growth of Helicobacter pylori under acidic conditions. J Infect Dis 182:1566–1569
     [Google Scholar]
  11. Bjorkholm B., Sjolund M., Falk P. G., Berg O. G., Engstrand L., Andersson D. I. 2001; Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori . Proc Natl Acad Sci U S A 98:14607–14612
     [Google Scholar]
  12. Blaser M. J. 1993; Helicobacter pylori : microbiology of a ‘slow’ bacterial infection. Trends Microbiol 1:255–260
     [Google Scholar]
  13. Blaser M. J., Berg D. E. 2001; Helicobacter pylori genetic diversity and risk of human disease. J Clin Invest 107:767–773
     [Google Scholar]
  14. Brown S., Hochberg M., Grenfell B. 2002; Does multiple infection select for raised virulence?. Trends Microbiol 10:401–405
     [Google Scholar]
  15. Censini S., Lange C., Xiang Z. 5 other authors 1996; cag , a pathogenicity island of Helicobacter pylori , encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 93:14648–14653
     [Google Scholar]
  16. Cheverud J. M., Vaughn T. T., Pletscher L. S., Peripato A. C., Adams E. S., Erikson C. F., King-Ellison K. J. 2001; Genetic architecture of adiposity in the cross of LG/J and SM/J inbred mice. Mamm Genome 12:3–12
     [Google Scholar]
  17. Clyne M., Labigne A., Drumm B. 1995; Helicobacter pylori requires an acidic environment to survive in the presence of urea. Infect Immun 63:1669–1673
     [Google Scholar]
  18. Cover T. L., Berg D. E., Blaser M. J., Mobley H. L. T. 2001; H. pylori pathogenesis. In Principles of Bacterial Pathogensis pp  509–558 Edited by Groisman E. A. New York: Academic Press;
     [Google Scholar]
  19. Dixon M. F. 1994; Pathophysiology of Helicobacter pylori infection. Scand J Gastroenterol 201:7–10
     [Google Scholar]
  20. Dubois A., Berg D. E., Incecik E. T. 7 other authors 1999; Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 116:90–96
     [Google Scholar]
  21. Ermak T. H., Giannasca P. J., Nichols R. 6 other authors 1998; Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J Exp Med 188:2277–2288
     [Google Scholar]
  22. Evans D. J. Jr, Evans D. G. 2000; Helicobacter pylori adhesins: review and perspectives. Helicobacter 5:183–195
     [Google Scholar]
  23. Garner J. A., Cover T. L. 1995; Analysis of genetic diversity in cytotoxin-producing and non-cytotoxin-producing Helicobacter pylori strains. J Infect Dis 172:290–293
     [Google Scholar]
  24. Ilver D., Arnqvist A., Ogren J. 7 other authors 1998; Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279:373–377
     [Google Scholar]
  25. Israel D. A., Salama N., Arnold C. N. 8 other authors 2001; Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J Clin Invest 107:611–620
     [Google Scholar]
  26. Jeong J. Y., Mukhopadhyay A. K., Akada J. K., Dailidiene D., Hoffman P. S., Berg D. E. 2001; Roles of FrxA and RdxA nitroreductases of Helicobacter pylori in susceptibility and resistance to metronidazole. J Bacteriol 183:5155–5162
     [Google Scholar]
  27. Karita M., Blaser M. J. 1998; Acid-tolerance response in Helicobacter pylori and differences between cagA + and cagA − strains. J Infect Dis 178:213–219
     [Google Scholar]
  28. Kersulyte D., Chalkauskas H., Berg D. E. 1999; Emergence of recombinant strains of Helicobacter pylori during human infection. Mol Microbiol 31:31–43
     [Google Scholar]
  29. Kleanthous H., Tibbitts T. J., Gray H. L., Myers G. A., Lee C. K., Ermak T. H., Monath T. P. 2001; Sterilizing immunity against experimental Helicobacter pylori infection is challenge-strain dependent. Vaccine 19:4883–4895
     [Google Scholar]
  30. Lee A., O'Rourke J., De Ungria M. C., Robertson B., Daskalopoulos G., Dixon M. F. 1997; A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386–1397
     [Google Scholar]
  31. Lee E. R., Trasler J., Dwivwdi S., Leblond C. P. 1982; Division of the mouse gastric mucosa into zymogenic and mucous regions on the basis of gland features. Am J Anat 164:187–207
     [Google Scholar]
  32. Lenski R. E., Travisano M. 1994; Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A 91:6808–6814
     [Google Scholar]
  33. Londono-Arcila P., Freeman D., Kleanthous H. 8 other authors 2002; Attenuated Salmonella enterica serovar Typhi expressing urease effectively immunizes mice against Helicobacter pylori challenge as part of a heterologous mucosal priming-parenteral boosting vaccination regimen. Infect Immun 70:5096–5106
     [Google Scholar]
  34. Mahdavi J., Sonden B., Hurtig M. 20 other authors 2002; Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573–578
     [Google Scholar]
  35. Morales-Espinosa R., Castillo-Rojas G., Gonzalez-Valencia G., Ponce de Leon S., Cravioto A., Atherton J. C., Lopez-Vidal Y. 1999; Colonization of Mexican patients by multiple Helicobacter pylori strains with different vacA and cagA genotypes. J Clin Microbiol 37:3001–3004
     [Google Scholar]
  36. Mukhopadhyay A. K., Jeong J.-Y., Dailidiene D., Hoffman P. S., Berg D. E. 2003; The fdxA ferredoxin gene can down-regulate frxA nitroreductase gene expression and is essential in many strains of Helicobacter pylori . J Bacteriol 185:2927–2935
     [Google Scholar]
  37. Nolan K. J., McGee D. J., Mitchell H. M. 8 other authors 2002; In vivo behavior of a Helicobacter pylori SS1 nixA mutant with reduced urease activity. Infect Immun 70:685–691
     [Google Scholar]
  38. O'Rourke E. J., Chevalier C., Pinto A. V., Thiberge J. M., Ielpi L., Labigne A., Radicella J. P. 2003; Pathogen DNA as target for host-generated oxidative stress: role for repair of bacterial DNA damage in Helicobacter pylori colonization. Proc Natl Acad Sci U S A 100:2789–2791
     [Google Scholar]
  39. Salama N., Guillemin K., McDaniel T. K., Sherlock G., Tompkins L., Falkow S. 2000; A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci U S A 97:14668–14673
     [Google Scholar]
  40. Schade C., Flemström G., Holm L. 1994; Hydrogen ion concentration in the mucus layer on top of acid-stimulated and -inhibited rat gastric mucosa. Gastroenterology 107:180–188
     [Google Scholar]
  41. Sipponen P., Hyvarinen H., Seppala K., Blaser M. J. 1998; Review article: Pathogenesis of the transformation from gastritis to malignancy. Aliment Pharmacol Ther 12:Suppl 161–71
     [Google Scholar]
  42. Suerbaum S., Smith J. M., Bapumia K. 5 other authors 1998; Free recombination within Helicobacter pylori . Proc. Natl Acad Sci U S A 95:12619–12624
     [Google Scholar]
  43. 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
     [Google Scholar]
  44. Wang G., Humayun M. Z., Taylor D. E. 1999; Mutation as an origin of genetic variability in Helicobacter pylori . Trends Microbiol 7:488–493
     [Google Scholar]
  45. Wright S. 1982; The shifting balance theory and macroevolution. Annu Rev Genet 16:1–19
     [Google Scholar]
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Helicobacter pylori tissue tropism: mouse-colonizing strains can target different gastric niches
Microbiology 149, 1901 (2003); https://doi.org/10.1099/mic.0.26129-0
/content/journal/micro/10.1099/mic.0.26129-0
/content/journal/micro/10.1099/mic.0.26129-0
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