New insights into the inactivation of gastric tumor suppressor RUNX3: The role of H. pylori infection

Journal of Cellular Biochemistry

Volumn 112, Issue 2, 2011, Pages 381-386

  Tsang, Ying Hung Nicole ^a,b   Lamb, Acacia ^a   Chen, Lin Feng ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

gastric cancer; H. pylori; RUNX3; tumor suppressor

Indexed keywords

PROTEASOME; TRANSCRIPTION FACTOR RUNX3;

ARTICLE; GENE SILENCING; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; STOMACH CANCER; TRANSCRIPTION INITIATION;

ANIMALS; CORE BINDING FACTOR ALPHA 3 SUBUNIT; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; STOMACH NEOPLASMS;

HELICOBACTER PYLORI;

EID: 79251644456     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22964     Document Type: Article

References (49)

1. Altekruse SF, McGlynn KA, Reichman ME,. 2009. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol 27: 1485-1491.
2. Bae SC, Lee YH,. 2006. Phosphorylation, acetylation and ubiquitination: The molecular basis of RUNX regulation. Gene 366: 58-66.
3. Bornschein J, Rokkas T, Selgrad M, Malfertheiner P,. 2009. Helicobacter pylori and clinical aspects of gastric cancer. Helicobacter 14 (Suppl. 1): 41-45.
4. Chang TL, Ito K, Ko TK, Liu Q, Salto-Tellez M, Yeoh KG, Fukamachi H, Ito Y,. 2009. Claudin-1 has tumor suppressive activity and is a direct target of RUNX3 in gastric epithelial cells. Gastroenterology
5. Chi XZ, Kim J, Lee YH, Lee JW, Lee KS, Wee H, Kim WJ, Park WY, Oh BC, Stein GS, Ito Y, van Wijnen AJ, Bae SC,. 2009. Runt-related transcription factor RUNX3 is a target of MDM2-mediated ubiquitination. Cancer Res 69: 8111-8119.
6. Chi XZ, Yang JO, Lee KY, Ito K, Sakakura C, Li QL, Kim HR, Cha EJ, Lee YH, Kaneda A, Ushijima T, Kim WJ, Ito Y, Bae SC,. 2005. RUNX3 suppresses gastric epithelial cell growth by inducing p21(WAF1/Cip1) expression in cooperation with transforming growth factor {beta}-activated SMAD. Mol Cell Biol 25: 8097-8107.
7. Chuang LS, Ito Y,. 2010. RUNX3 is multifunctional in carcinogenesis of multiple solid tumors. Oncogene 29: 2605-2615.
8. Cover TL, Blaser MJ,. 2009. Helicobacter pylori in health and disease. Gastroenterology 136: 1863-1873.
9. Farinati F, Cardin R, Cassaro M, Bortolami M, Nitti D, Tieppo C, Zaninotto G, Rugge M,. 2008. Helicobacter pylori, inflammation, oxidative damage and gastric cancer: A morphological, biological and molecular pathway. Eur J Cancer Prev 17: 195-200.
10. Fukamachi H,. 2006. Runx3 controls growth and differentiation of gastric epithelial cells in mammals. Dev Growth Differ 48: 1-13.
11. Guo WH, Weng LQ, Ito K, Chen LF, Nakanishi H, Tatematsu M, Ito Y,. 2002. Inhibition of growth of mouse gastric cancer cells by Runx3, a novel tumor suppressor. Oncogene 21: 8351-8355.
12. Higashi H, Tsutsumi R, Fujita A, Yamazaki S, Asaka M, Azuma T, Hatakeyama M,. 2002a. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci USA 99: 14428-14433.
13. Higashi H, Tsutsumi R, Muto S, Sugiyama T, Azuma T, Asaka M, Hatakeyama M,. 2002b. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295: 683-686.
14. Hodge DR, Peng B, Cherry JC, Hurt EM, Fox SD, Kelley JA, Munroe DJ, Farrar WL,. 2005. Interleukin 6 supports the maintenance of p53 tumor suppressor gene promoter methylation. Cancer Res 65: 4673-4682.
15. Hsu PI, Hsieh HL, Lee J, Lin LF, Chen HC, Lu PJ, Hsiao M,. 2009. Loss of RUNX3 expression correlates with differentiation, nodal metastasis, and poor prognosis of gastric cancer. Ann Surg Oncol 16: 1686-1694.
16. Huang G, Shigesada K, Ito K, Wee HJ, Yokomizo T, Ito Y,. 2001. Dimerization with PEBP2beta protects RUNX1/AML1 from ubiquitin-proteasome- mediated degradation. EMBO J 20: 723-733.
17. Ito K, Liu Q, Salto-Tellez M, Yano T, Tada K, Ida H, Huang C, Shah N, Inoue M, Rajnakova A, Hiong KC, Peh BK, Han HC, Ito T, Teh M, Yeoh KG, Ito Y,. 2005. RUNX3, a novel tumor suppressor, is frequently inactivated in gastric cancer by protein mislocalization. Cancer Res 65: 7743-7750.
18. Ito Y,. 2004. Oncogenic potential of the RUNX gene family: 'Overview'. Oncogene 23: 4198-4208.
19. Ito Y, Miyazono K,. 2003. RUNX transcription factors as key targets of TGF-beta superfamily signaling. Curr Opin Genet Dev 13: 43-47.
20. Jaiswal M, LaRusso NF, Gores GJ,. 2001. Nitric oxide in gastrointestinal epithelial cell carcinogenesis: Linking inflammation to oncogenesis. Am J Physiol Gastrointest Liver Physiol 281: G626-G634.
21. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ, Lee KY, Bae SC,. 2004. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J Biol Chem 279: 29409-29417.
22. Jones PA, Baylin SB,. 2007. The epigenomics of cancer. Cell 128: 683-692.
23. Jung Y, Park J, Kim TY, Park JH, Jong HS, Im SA, Robertson KD, Bang YJ,. 2007. Potential advantages of DNA methyltransferase 1 (DNMT1)-targeted inhibition for cancer therapy. J Mol Med 85: 1137-1148.
24. Katayama Y, Takahashi M, Kuwayama H,. 2009. Helicobacter pylori causes runx3 gene methylation and its loss of expression in gastric epithelial cells, which is mediated by nitric oxide produced by macrophages. Biochem Biophys Res Commun 388: 496-500.
25. Kim JH, Choi JK, Cinghu S, Jang JW, Lee YS, Li YH, Goh YM, Chi XZ, Lee KS, Wee H, Bae SC,. 2009. Jab1/CSN5 induces the cytoplasmic localization and degradation of RUNX3. J Cell Biochem 107: 557-565.
26. Kim TY, Lee HJ, Hwang KS, Lee M, Kim JW, Bang YJ, Kang GH,. 2004. Methylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma. Lab Invest 84: 479-484.
27. Kitajima Y, Ohtaka K, Mitsuno M, Tanaka M, Sato S, Nakafusa Y, Miyazaki K,. 2008. Helicobacter pylori infection is an independent risk factor for Runx3 methylation in gastric cancer. Oncol Rep 19: 197-202.
28. Kulis M, Esteller M,. 2010. DNA methylation and cancer. Adv Genet 70: 27-56.
29. Lamb A, Yamaguchi H, Chen LF,. 2010. The many roads traveled by Helicobacter pylori to NF-kappaB activation. Gut Microbes 1: 109-113.
30. Lamb A, Yang XD, Tsang YH, Li JD, Higashi H, Hatakeyama M, Peek RM, Blanke SR, Chen LF,. 2009. Helicobacter pylori CagA activates NF-kappaB by targeting TAK1 for TRAF6-mediated Lys 63 ubiquitination. EMBO Rep 10: 1242-1249.
31. Lee SH, Kim J, Kim WH, Lee YM,. 2009. Hypoxic silencing of tumor suppressor RUNX3 by histone modification in gastric cancer cells. Oncogene 28: 184-194.
32. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, Lee KY, Nomura S, Lee CW, Han SB, Kim HM, Kim WJ, Yamamoto H, Yamashita N, Yano T, Ikeda T, Itohara S, Inazawa J, Abe T, Hagiwara A, Yamagishi H, Ooe A, Kaneda A, Sugimura T, Ushijima T, Bae SC, Ito Y,. 2002. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109: 113-124.
33. Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, Arii K, Kaneda A, Tsukamoto T, Tatematsu M, Tamura G, Saito D, Sugimura T, Ichinose M, Ushijima T,. 2006. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 12: 989-995.
34. Mimuro H, Suzuki T, Nagai S, Rieder G, Suzuki M, Nagai T, Fujita Y, Nagamatsu K, Ishijima N, Koyasu S, Haas R, Sasakawa C,. 2007. Helicobacter pylori dampens gut epithelial self-renewal by inhibiting apoptosis, a bacterial strategy to enhance colonization of the stomach. Cell Host Microbe 2: 250-263.
35. Niwa T, Tsukamoto T, Toyoda T, Mori A, Tanaka H, Maekita T, Ichinose M, Tatematsu M, Ushijima T,. 2010. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res 70: 1430-1440.
36. Peek RM, Jr., Blaser MJ,. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2: 28-37.
37. Peek RM, Jr., Crabtree JE,. 2006. Helicobacter infection and gastric neoplasia. J Pathol 208: 233-248.
38. Peng Z, Wei D, Wang L, Tang H, Zhang J, Le X, Jia Z, Li Q, Xie K,. 2006. RUNX3 inhibits the expression of vascular endothelial growth factor and reduces the angiogenesis, growth, and metastasis of human gastric cancer. Clin Cancer Res 12: 6386-6394.
39. Pickart CM,. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
40. Sugiura H, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Mori Y, Ogawa R, Katada T, Harata K, Fujii Y,. 2008. Decreased expression of RUNX3 is correlated with tumor progression and poor prognosis in patients with esophageal squamous cell carcinoma. Oncol Rep 19: 713-719.
41. Suzuki M, Suzuki H, Minegishi Y, Ito K, Nishizawa T, Hibi T,. 2010 H. pylori-eradication therapy increases RUNX3 expression in the glandular epithelial cells in enlarged-fold gastritis. J Clin Biochem Nutr 46: 259-264.
42. Tsang YH, Lamb A, Romero-Gallo J, Huang B, Ito K, Peek RM, Jr., Ito Y, Chen LF,. 2010. Helicobacter pylori CagA targets gastric tumor suppressor RUNX3 for proteasome-mediated degradation. Oncogene 29: 5643-5650.
43. Tsuji S, Tsujii M, Murata H, Nishida T, Komori M, Yasumaru M, Ishii S, Sasayama Y, Kawano S, Hayashi N,. 2006. Helicobacter pylori eradication to prevent gastric cancer: Underlying molecular and cellular mechanisms. World J Gastroenterol 12: 1671-1680.
44. Vauhkonen M, Vauhkonen H, Sipponen P,. 2006. Pathology and molecular biology of gastric cancer. Best Pract Res Clin Gastroenterol 20: 651-674.
45. Wei D, Gong W, Oh SC, Li Q, Kim WD, Wang L, Le X, Yao J, Wu TT, Huang S, Xie K,. 2005. Loss of RUNX3 expression significantly affects the clinical outcome of gastric cancer patients and its restoration causes drastic suppression of tumor growth and metastasis. Cancer Res 65: 4809-4816.
46. Weissman AM,. 2001. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2: 169-178.
47. Yamamura Y, Lee WL, Inoue K, Ida H, Ito Y,. 2006. RUNX3 cooperates with FoxO3a to induce apoptosis in gastric cancer cells. J Biol Chem 281: 5267-5276.
48. Yang B, Kumar S,. 2010. Nedd4 and Nedd4-2: Closely related ubiquitin-protein ligases with distinct physiological functions. Cell Death Differ 17: 68-77.
49. Yano T, Ito K, Fukamachi H, Chi XZ, Wee HJ, Inoue K, Ida H, Bouillet P, Strasser A, Bae SC, Ito Y,. 2006. The RUNX3 tumor suppressor upregulates Bim in gastric epithelial cells undergoing transforming growth factor beta-induced apoptosis. Mol Cell Biol 26: 4474-4488.