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
2019-10-15
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 3β 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 3β 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