1887

Abstract

eradication can reverse gastric intestinal metaplasia (IM) in some but not all patients. induces high levels of nuclear -catenin staining in IM tissues, as well as overexpression of cyclooxygenase-2 (COX-2). This study investigated whether the Wnt/-catenin pathway plays a role in IM regression following eradication. Sixty-five -infected patients with IM who had achieved successful eradication provided paired gastric samples before and after eradication to analyse the persistence of IM, and to assess COX-2 and nuclear -catenin expression. The host genotypes of single nucleotide polymorphisms (SNPs) of the , -catenin () and adenomatous polyposis coli () genes were analysed. In addition, expression of -catenin, E-cadherin and phosphorylated and unphosphorylated glycogen synthase kinase 3 (GSK-3) in cell lines challenged with isolates from patients with and without IM persistence was compared by immunoanalysis. After a mean 33.9-month follow-up after eradication, 44 patients (67.7 %) with IM persistence had a higher rate of high-level nuclear -catenin expression in IM tissue than those without IM persistence (=0.008). The patients with IM persistence had a higher rate of AA, GG and AA SNP genotypes at positions 4479, 5268 and 5465, respectively, than the patients without IM persistence (=0.022). The isolates from the patients with IM regression after eradication induced more phospho-GSK-3 in AGS cells than isolates from patients with IM persistence (=0.011). It is likely that interactions with and the patient's Wnt/-catenin genetic predisposition determine the outcome of IM persistence following eradication.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.007310-0
2009-05-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jmm/58/5/567.html?itemId=/content/journal/jmm/10.1099/jmm.0.007310-0&mimeType=html&fmt=ahah

References

  1. Cheung T. K., Xia H. H., Wong B. C. 2007; Helicobacter pylori eradication for gastric cancer prevention. J Gastroenterol 42 (Suppl. 17):10–15 [CrossRef]
    [Google Scholar]
  2. Clevers H. 2006; Wnt/ β -catenin signaling in development and disease. Cell 127:469–480 [CrossRef]
    [Google Scholar]
  3. Cohen P., Frame S. 2001; The renaissance of GSK3. Nat Rev Mol Cell Biol 2:769–776 [CrossRef]
    [Google Scholar]
  4. Correa P., Houghton J. 2007; Carcinogenesis of Helicobacter pylori . Gastroenterology 133:659–672 [CrossRef]
    [Google Scholar]
  5. Correa P., Fontham E. T., Bravo J. C., Bravo L. E., Ruiz B., Zarama G., Realpe J. L., Malcom G. T., Li D. other authors 2000; Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti- Helicobacter pylori therapy. J Natl Cancer Inst 92:1881–1888 [CrossRef]
    [Google Scholar]
  6. Dixon M. F., Genta R. M., Yardley J. H., Correa P. 1996; Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis Houston: 1994 Am J Surg Pathol 20:1161–1181
    [Google Scholar]
  7. Franco A. T., Israel D. A., Washington M. K., Krishna U., Fox J. G., Rogers A. B., Neish A. S., Collier-Hyams L., Perez-Perez G. I. other authors 2005; Activation of β -catenin by carcinogenic Helicobacter pylori . Proc Natl Acad Sci U S A 102:10646–10651 [CrossRef]
    [Google Scholar]
  8. Ikenoue T., Ijichi H., Kato N., Kanai F., Masaki T., Rengifo W., Okamoto M., Matsumura M., Kawabe T. other authors 2002; Analysis of the β -catenin/T cell factor signaling pathway in 36 gastrointestinal and liver cancer cells. Jpn J Cancer Res 93:1213–1220 [CrossRef]
    [Google Scholar]
  9. Jeng Y. M., Wu M. Z., Mao T. L., Chang M. H., Hsu H. C. 2000; Somatic mutations of β -catenin play a crucial role in the tumorigenesis of sporadic hepatoblastoma. Cancer Lett 152:45–51 [CrossRef]
    [Google Scholar]
  10. Kurashima Y., Murata-Kamiya N., Kikuchi K., Higashi H., Azuma T., Kondo S., Hatakeyama M. 2008; Deregulation of β -catenin signal by Helicobacter pylori CagA requires the CagA-multimerization sequence. Int J Cancer 122:823–831 [CrossRef]
    [Google Scholar]
  11. Leung W. K., Lin S. R., Ching J. Y., To K. F., Ng E. K., Chan F. K., Lau J. Y., Sung J. J. 2004; Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 53:1244–1249 [CrossRef]
    [Google Scholar]
  12. Lim H. Y., Joo H. J., Choi J. H., Yi J. W., Yang M. S., Cho D. Y., Kim H. S., Nam D. K., Lee K. B., Kim H. C. 2000; Increased expression of cyclooxygenase-2 protein in human gastric carcinoma. Clin Cancer Res 6:519–525
    [Google Scholar]
  13. Lu C. C., Sheu B. S., Chen T. W., Yang H. B., Hung K. H., Kao A. W., Chuang C. H., Wu J. J. 2005; Host TNF - α -1031 and -863 promoter single nucleotide polymorphisms determine the risk of benign ulceration after H. pylori infection. Am J Gastroenterol 100:1274–1282 [CrossRef]
    [Google Scholar]
  14. McCarthy C. J., Crofford L. J., Greenson J., Scheiman J. M. 1999; Cyclooxygenase-2 expression in gastric antral mucosa before and after eradication of Helicobacter pylori infection. Am J Gastroenterol 94:1218–1223 [CrossRef]
    [Google Scholar]
  15. Murata-Kamiya N., Kurashima Y., Teishikata Y., Yamahashi Y., Saito Y., Higashi H., Aburatani H., Akiyama T., Peek R. M. Jr other authors 2007; Helicobacter pylori CagA interacts with E-cadherin and deregulates the β -catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene 26:4617–4626 [CrossRef]
    [Google Scholar]
  16. Nakayama M., Hisatsune J., Yamasaki E., Isomoto H., Kurazono H., Hatakeyama M., Azuma T., Yamaoka Y., Yahiro K. other authors 2009; Helicobacter pylori VacA-induced inhibition of GSK3 through the PI3K/Akt signaling pathway. J Biol Chem 284:1612–1619
    [Google Scholar]
  17. Nathke I. 2006; Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat Rev Cancer 6:967–974 [CrossRef]
    [Google Scholar]
  18. Ogasawara N., Tsukamoto T., Mizoshita T., Inada K., Cao X., Takenaka Y., Joh T., Tatematsu M. 2006; Mutations and nuclear accumulation of β -catenin correlate with intestinal phenotypic expression in human gastric cancer. Histopathology 49:612–621 [CrossRef]
    [Google Scholar]
  19. Ohkusa T., Fujiki K., Takashimizu I., Kumagai J., Tanizawa T., Eishi Y., Yokoyama T., Watanabe M. 2001; Improvement in atrophic gastritis and intestinal metaplasia in patients in whom Helicobacter pylori was eradicated. Ann Intern Med 134:380–386 [CrossRef]
    [Google Scholar]
  20. Powell S. M., Zilz N., Beazer-Barclay Y., Bryan T. M., Hamilton S. R., Thibodeau S. N., Vogelstein B., Kinzler K. 1992; APC mutations occur early during colorectal tumorigenesis. Nature 359:235–237 [CrossRef]
    [Google Scholar]
  21. Prall F., Weirich V., Ostwald C. 2007; Phenotypes of invasion in sporadic colorectal carcinomas related to aberrations of the adenomatous polyposis coli ( APC ) gene. Histopathology 50:318–330 [CrossRef]
    [Google Scholar]
  22. Romiti A., Zullo A., Borrini F., Sarcina I., Hassan C., Winn S., Tomao S., Vecchione A., Morini S., Mingazzini P. 2005; Relationship between β -catenin expression and epithelial cell proliferation in gastric mucosa with intestinal metaplasia. World J Gastroenterol 11:4400–4403
    [Google Scholar]
  23. Sheu B. S., Yang H. B., Sheu S. M., Huang A. H., Wu J. J. 2003; Higher gastric cycloxygenase-2 expression and precancerous change in Helicobacter pylori -infected relatives of gastric cancer patients. Clin Cancer Res 9:5245–5251
    [Google Scholar]
  24. Sheu B. S., Odenbreit S., Hung K. H., Liu C. P., Sheu S. M., Yang H. B., Wu J. J. 2006; Interaction between host gastric sialyl-Lewis X and H. pylori SabA enhances H. pylori density in patients lacking gastric Lewis B antigen. Am J Gastroenterol 101:36–44 [CrossRef]
    [Google Scholar]
  25. Slattery M. L., Samowitz W., Ballard L., Schaffer D., Leppert M., Potter J. D. 2001; A molecular variant of the APC gene at codon 1822: its association with diet, lifestyle, and risk of colon cancer. Cancer Res 61:1000–1004
    [Google Scholar]
  26. Sokolova O., Bozko P. M., Naumann M. 2008; Helicobacter pylori suppresses glycogen synthase kinase 3 β to promote β -catenin activity. J Biol Chem 283:29367–29374 [CrossRef]
    [Google Scholar]
  27. Sung J. J., Leung W. K., Go M. Y., To K. F., Cheng A. S., Ng E. K., Chan F. K. 2000a; Cyclooxygenase-2 expression in Helicobacter pylori -associated premalignant and malignant gastric lesions. Am J Pathol 157:729–735 [CrossRef]
    [Google Scholar]
  28. Sung J. J., Lin S. R., Ching J. Y., Zhou L. Y., To K. F., Wang R. T., Leung W. K., Ng E. K., Lau J. Y. other authors 2000b; Atrophy and intestinal metaplasia one year after cure of H. pylori infection: a prospective, randomized study. Gastroenterology 119:7–14 [CrossRef]
    [Google Scholar]
  29. Tabassam F. H., Graham D. Y., Yamaoka Y. 2009; Helicobacter pylori activate epidermal growth factor receptor- and phosphatidylinositol 3-OH kinase-dependent Akt and glycogen synthase kinase 3 β phosphorylation. Cell Microbiol 11:70–82 [CrossRef]
    [Google Scholar]
  30. Tajima Y., Yamazaki K., Makino R., Nishino N., Aoki S., Kato M., Morohara K., Kaetsu T., Kusano M. 2006; Gastric and intestinal phenotypic marker expression in early differentiated-type tumors of the stomach: clinicopathologic significance and genetic background. Clin Cancer Res 12:6469–6479 [CrossRef]
    [Google Scholar]
  31. Uemura N., Mukai T., Okamoto S., Yamaguchi S., Mashiba H., Taniyama K., Sasaki N., Haruma K., Sumii K., Kajiyama G. 1997; Effect of Helicobacter pylori eradication on subsequent development of cancer after endoscopic resection of early gastric cancer. Cancer Epidemiol Biomarkers Prev 6:639–642
    [Google Scholar]
  32. van der Hulst R. W., van der Ende A., Dekker F. W., Ten Kate F. J., Weel J. F., Keller J. J., Kruizinga S. P., Dankert J., Tytgat G. N. 1997; Effect of Helicobacter pylori eradication on gastritis in relation to cagA : a prospective 1-year follow-up study. Gastroenterology 113:25–30 [CrossRef]
    [Google Scholar]
  33. Walker M. M. 2003; Is intestinal metaplasia of the stomach reversible?. Gut 52:1–4 [CrossRef]
    [Google Scholar]
  34. Wei S. C., Su Y. N., Tsai-Wu J. J., Wu C. H., Huang Y. L., Sheu J. C., Wang C. Y., Wong J. M. 2004; Genetic analysis of the APC gene in Taiwanese familial adenomatous polyposis. J Biomed Sci 11:260–265 [CrossRef]
    [Google Scholar]
  35. Wong B. C., Lam S. K., Wong W. M., Chen J. S., Zheng T. T., Feng R. E., Lai K. C., Hu W. H., Yuen S. T. other authors 2004; Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 291:187–194 [CrossRef]
    [Google Scholar]
  36. Yang H. B., Cheng H. C., Sheu B. S., Hung K. H., Liou M. F., Wu J. J. 2007; Chronic celecoxib users more often show regression of gastric intestinal metaplasia after Helicobacter pylori eradication. Aliment Pharmacol Ther 25:455–461
    [Google Scholar]
  37. Yokozaki H. 2000; Molecular characteristics of eight gastric cancer cell lines established in Japan. Pathol Int 50:767–777 [CrossRef]
    [Google Scholar]
  38. Zhang X., Miao X., Tan W., Ning B., Liu Z., Hong Y., Song W., Guo Y., Shen Y. other authors 2005; Identification of functional genetic variants in cyclooxygenase-2 and their association with risk of esophageal cancer. Gastroenterology 129:565–576
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.007310-0
Loading
/content/journal/jmm/10.1099/jmm.0.007310-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error