Late reactivation of sonic hedgehog by Helicobacter pylori results in population of gastric epithelial cells that are resistant to apoptosis: Implication for gastric carcinogenesis

Cancer Letters

Volumn 287, Issue 1, 2010, Pages 44-53

  Lee, Kee Myung ^a   Lee, Jeong Sang ^b   Jung, Hyeon Sik ^b   Park, Dong Kyun ^b   Park, Hyun Sun ^b   Hahm, Ki Baik ^b  

^a Ajou University School of Medicine   (South Korea)

^b Lee Gil Ya Cancer and Diabetes Institute   (South Korea)

Author keywords

Anti apoptosis; Carcinogenesis; Helicobacter pylori; Proliferation; Sonic hedgehog

Indexed keywords

CYCLOPAMINE; SMALL INTERFERING RNA; SONIC HEDGEHOG PROTEIN;

ADENOMA; APOPTOSIS; ARTICLE; ATROPHIC GASTRITIS; CANCER CELL CULTURE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH ADENOCARCINOMA; STOMACH CANCER; STOMACH CARCINOGENESIS; STOMACH EPITHELIUM; WESTERN BLOTTING;

APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; CYCLIN D1; GASTRIC MUCOSA; HEDGEHOG PROTEINS; HELICOBACTER PYLORI; HUMANS; STOMACH NEOPLASMS; VERATRUM ALKALOIDS;

ERINACEIDAE; HELICOBACTER PYLORI;

EID: 72049104191     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.05.032     Document Type: Article

References (49)

1. Moss S.F., and Blaser M.J. Mechanisms of disease: inflammation and the origin of cancer. Nature Clin. Practice Oncol. 2 (2007) 90-97
2. Peek R.M., and Blaser M.J. Helicobacter pylori and gastrointestinal tract adenocarcinoma. Nature Rev. 2 (2002) 28-37
3. Uemura N., Okamoto S., Yamamoto S., et al. Helicobacter pylori infection and the development of gastric cancer. New Engl. J. Med. 345 (2001) 829-832
4. Kim D.H., Kim S.W., Song Y.J., et al. Long-term evaluation of mice model infected with Helicobacter pylori; focus on gastric pathology including gastric cancer. Aliment. Pharmacol. Ther. 18S (2003) 14-23
5. Honda S., Fujioka T., Tokieda M., Satoh R., Nishizono A., and Nasu M. Development of Helicobacter pylori-induced gastric carcinoma in Mongolian gerbils. Cancer Res. 58 (1998) 4255-4259
6. Tatematsu M., Nozaki K., and Tsukamoto T. Helicobacter pylori infection and gastric carcinogenesis in animal models. Gastric Cancer 6 (2003) 1-7
7. Kodama M., Murakami K., Sato R., Okimoto T., Nishizono A., and Fujioka T. Helicobacter pylori-infected animal models are extremely suitable for the investigation of gastric carcinogenesis. World J. Gastroenterol. 11 (2005) 7063-7071
8. Shirin H., and Moss S.F. Helicobacter pylori induced apoptosis. Gut 43 (1998) 584-592
9. Suzuki H., Miyazawa M., Nagahashi S., et al. Attenuated apoptosis in H. pylori-colonized gastric mucosa of Mongolian gerbils in comparison with mice. Dig. Dis. Sci. 47 (2002) 90-99
10. El-Omer E.M. The importance of interleukin 1 beta in Helicobacter pylori associated disease. Gut 48 (2001) 743-747
11. kip1 regulates the apoptotic responses of gastric epithelial cells to Helicobacter pylori. Gut 53 (2004) 797-804
12. Shiotani A., Iishi H., Uedo N., et al. Evidence that loss of sonic hedgehog is an indicator of Helicobacter pylori-induced atrophic gastritis progressing to gastric cancer. Am. J. Gastroenterol. 100 (2005) 581-587
13. Suzuki H., Minegishi Y., Nomoto Y., Ota T., Masaoka T., Van Den Brink G.R., and Hibi T. Down-regulation of a morphogen (sonic hedgehog) gradient in the gastric epithelium of Helicobacter pylori-infected Mongolian gerbils. J. Pathol. 206 (2005) 186-197
14. Wang L.H., Choi Y.L., Hua X.Y., et al. Increased expression of sonic hedgehog and altered methylation of its promoter region in gastric cancer and its related lesions. Mod. Pathol. 19 (2006) 675-683
15. Santos M.R., Melton D.A., and Mcmahon A.P. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 127 (2000) 2763-2772
16. Fu M., Lui V.C., Sham M.H., Pachnis V., and Tam P.K. Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J. Cell Biol. 166 (2004) 673-684
17. Nishimaki H., Kasai K., Kozaki K., et al. A role of activated sonic hedgehog signaling for the cellular proliferation of oral squamous cell carcinoma cell line. Biochem. Biophys. Res. Commun. 314 (2004) 313-320
18. Athar M., Tang X., Lee J.L., Kopelovich L., and Kim A.L. Hedgehog signaling in skin development and cancer. Exp. Dermatol. 15 (2006) 667-677
19. Datta S., and Datta M.W. Sonic hedgehog signaling in advanced prostate cancer. Cell. Mol. Life Sci. 63 (2006) 435-448
20. Sanchez P., Hernάndez A.M., Stecca B., et al. Inhibition of prostate cancer proliferation by interference with Sonic Hedgehog-gli1 signaling. PNAS 101 (2004) 12561-12566
21. Thayer S.P., Magllano M.P., Helser P.W., et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 425 (2003) 851-856
22. Merman D.M., Karhadkar S.S., Maitra A., et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 425 (2003) 846-851
23. Ma X., Sheng T., Zhang Y., et al. Hedgehog signaling is activated in subsets of esophageal cancers. Int. J. Cancer 118 (2006) 139-148
24. Ma X.L., Sun H.J., Wang Y.S., Huang S.H., Xie J.W., and Ahang H.W. Study of sonic hedgehog signaling pathway related molecules in gastric carcinoma. World J. Gastroenterol. 12 (2006) 3965-3969
25. Watkins D.N., Berman D.M., Burkholder S.G., Wang B., Beachy P.A., and Baylin S.B. Hedgehog signaling within airway epithelial progenitors and in small cell lung cancer. Nature 422 (2003) 313-317
26. Kubo M., Nakamura M., Tasaki A., et al. Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res. 64 (2004) 6071-6074
27. Qualtrough D., Buda A., Gaffield W., Wiliams A.C., and Paraskeva C. Hedgehog signaling in colorectal tumor cells; induction of apoptosis with cyclopamine treatment. Int. J. Cancer 110 (2004) 831-837
28. Nam K.T., Oh S.Y., Ahn B., et al. Decreased Helicobacter pylori associated gastric carcinogenesis in mice lacking inducible nitric oxide synthase. Gut 53 (2004) 1250-1255
29. Nam K.T., Hahm K.B., Oh S.Y., et al. The selective cyclooxygenase-2 inhibitor nimesulide prevents Helicobacter pylori -associated gastric cancer development in a mouse model. Clin. Cancer Res. 10 (2004) 8105-8113
30. Hahn H., Wojnowski L., Miller G., and Zimmer A. The patched signaling pathway in tumorigenesis and development: lessons from animal models. J. Mol. Med. 77 (1999) 459-468
31. Charrier J.B., Lapointe F., Douarin N.M., and Teillet M.A. Anti-apoptotic role of sonic hedgehog protein at the early stages of nervous system organogenesis. Development 128 (2001) 4011-4020
32. Mori Y., Okumura T., Tsunoda S., Sakai Y., and Shimada Y. Gli-1 expression is associated with lymph node metastasis and tumor progression in esophageal squamous cell carcinoma. Oncology 70 (2006) 378-389
33. Watkins D.N., and Peacock C.D. Hedgehog signaling in foregut malignancy. Biochem. Pharmacol. 68 (2004) 1055-1060
34. Fukuda K., and Yasugi S. Versatile roles for sonic hedgehog in gut development. J. Gastroenterol. 37 (2002) 239-246
35. Kayed H., Kleeff J., Osman T., Keleg S., Bu{combining double acute accent}chler M., and Friess H. Hedgehog signaling in the normal and diseased pancreas. Pancreas 32 (2006) 119-148
36. Brink G.R., Hardwick J.C., Nielsen C., et al. Sonic hedgehog expression correlates with fundic gland differentiation in the adult gastrointestinal tract. Gut 51 (2002) 628-633
37. Bagnoli F., Buti L., Tompkins L., Covacci A., and Amieva M.R. Helicobacter pylori CagA induces a transition from polarized to invasive phenotypes in MDCK cells. Proc. Natl. Acad. Sci. USA 102 (2005) 16339-16344
38. Brink G.R., Hardwick J.C., Tytgat G.N., Brink M.A., Kate F.J., Deventer S.J., and Peppelenbosch M.P. Sonic hedgehog regulates gastric gland morphogenesis in man and mouse. Gastroenterology 121 (2001) 317-328
39. Fukaya M., Isohata N., Ohta H., et al. Hedgehog signal activation in gastric pit cell and in diffuse type gastric cancer. Gastroenterology 131 (2006) 14-29
40. Tsukamoto T., Mizoshita T., and Tatematsu M. Gastric-and-intestinal mixed-type intestinal metaplasia: aberrant expression of transcription factors and stem cell intestinalization. Gastric Cancer 9 (2006) 156-166
41. Akbulut M., Demirkan N., and Du{combining double acute accent}Zcan E. PCNA expression in chronic gastric sue to Helicobacter pylori. Turk. J. Gastroenterol. 17 (2006) 84-89
42. Xia H.H., and Talley N.J. Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. Am. J. Gastroenterol. 96 (2001) 16-26
43. Ahmed A., Smoot D., Littleton G., et al. Helicobacter pylori inhibits gastric cell cycle progression. Microbes Infect. 2 (2000) 1159-1169
44. kip1 deficiency confers susceptibility to gastric carcinogenesis in Helicobacter pylori-infected mice. Gastroenterology 129 (2005) 1544-1556
45. Cao X., Tsukamoto T., Nozaki K., et al. Eradication of Helicobacter pylori induced apoptosis and inhibits proliferation of heterotopic proliferative glands in infected Mongolian gerbils. Cancer Sci. 95 (2004) 872-877
46. Hirata Y., Maeda S., Mitsuno Y., et al. Helicobacter pylori activates the cyclin D1 gene through mitogen-activated protein kinase pathway in gastric cancer cells. Infect. Immun. 69 (2001) 3965-3971
47. Shiotani S., Iishi H., Ishiguro S., Tatsuta M., Nakae Y., and Merchant J.L. Epithelial cell turnover in relation to ongoing damage of the gastric mucosa in patients with early gastric cancer: increase of cell proliferation in paramalignant lesions. J. Gastroenterol. 40 (2005) 337-344
48. Miyazawa M., Suzuki H., Masaoka T., et al. Suppressed apoptosis in the inflamed gastric mucosa of Helicobacter pylori-colonized iNOS-knockout mice. Free Rad. Biol. Med. 34 (2003) 1621-1630
49. Fox J.G., and Wang T.C. Inflammation, atrophy, and gastric cancer. J. Clin. Invest. 117 (2007) 60-69