Induction of cyclooxygenase-2 overexpression in human gastric epithelial cells by Helicobacter pylori involves TLR2/TLR9 and c-Src-dependent nuclear factor-κB activation

Molecular Pharmacology

Volumn 66, Issue 6, 2004, Pages 1465-1477

  Chang, Ya Jen ^a   Wu, Ming Shiang ^a   Lin, Jaw Town ^a   Sheu, Bor Shyang ^b   Muta, Tatsushi ^c   Inoue, Hiroyasu ^d   Chen, Ching Chow ^a,e  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c KYUSHU UNIVERSITY   (Japan)

^d NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; I KAPPA B; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; NEUTRALIZING ANTIBODY; NIK PROTEIN; NUCLEAR FACTOR INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TYROSINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BABA2 GENE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CAGA GENE; CARCINOGENESIS; CONTROLLED STUDY; COX 2 GENE; CYCLIC AMP RESPONSIVE ELEMENT; DNA PROTEIN COMPLEX; DUODENUM ULCER; DYSPEPSIA; FF GENE; GASTRITIS; GENE; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HRGA GENE; HUMAN; HUMAN CELL; ICEA GENE; METHYLATION; ONCOGENE SRC; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STOMACH CANCER; STOMACH EPITHELIUM; STOMACH ULCER; VACA GENE; Y188F GENE; Y199F GENE;

CCAAT-ENHANCER-BINDING PROTEINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLOOXYGENASE 2; ENZYME ACTIVATION; GASTRIC MUCOSA; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, SRC; HELICOBACTER PYLORI; HUMANS; KINETICS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; METHYLATION; NF-KAPPA B; PROMOTER REGIONS (GENETICS); PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTORS, CELL SURFACE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TOLL-LIKE RECEPTORS;

EID: 9444252934     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.104.005199     Document Type: Article

References (44)

1. Akhtar M, Cheng Y, Magno RM, Ashktorab H, Smoot DT, Meltzer SJ, and Wilson KT (2001) Promoter methylation regulates Helicobacter pylori-stimulated cyclooxygenase-2 expression in gastric epithelial cells. Cancer Res 61:2399-2403.
2. Ando T, Wassenaar TM, Peek RM Jr, Aras RA, Tschumi AI, van Doom LJ, Kusugami K, and Blaser MJ (2002) A Helicobacter pylori restriction endonuclease-replacing gene, hrgA, is associated with gastric cancer in Asian strains. Cancer Res 62:2385-2389.
3. Barton GM and Medzhitov R (2003) Toll-like receptor signaling pathways. Science (Wash DC). 300:1524-1525.
4. Blaser MJ (2002) Polymorphic bacteria persisting in polymorphic hosts: assessing Helicobacter pylori-related risks for gastric cancer. J Natl Cancer Inst 94:1662-1663.
5. Bodger K and Crabtree JE (1998) Helicobacter pylori and gastric inflammation. Br Med Bull 54:139-150.
6. Bravo LE, van Doom LJ, Reakpe JL, and Correa P (2002) Virulence associated genotypes of Helicobacter pylori: do they explain the African enigma? Am J Gastroenterol 97:2839-2842.
7. Busiello I, Acquaviva R, Di Popolo A, Blanchard TG, Ricci V, Romano M, and Zarrilli R (2004) Helicobacter pylori gamma-glutamyltranspeptidase upregulates COX-2 and EGF-related peptide expression in human gastric cells. Cell Microbiol 6:255-267.
8. Caputo R, Tuccillo C, Manzo BA, Zarrilli R, Tortora G, Blanco Cdel V, Ricci V, Ciardiello F, and Romano M (2003) Helicobacter pylori VacA toxin up-regulates vascular endothelial growth factor expression in MKN 28 gastric cells through an epidermal growth factor receptor-, cyclooxygenase-2-dependent mechanism. Clin Cancer Res 9:2015-2021.
9. Chang YJ, Holtzman MJ, and Chen CC (2002) Interferon-γ-induced epithelial ICAM-1 expression and monocyte adhesion. Involvement of protein kinase C-dependent c-Src tyrosine kinase activation pathway. J Biol Chem 277:7118-7126.
10. Chang YJ, Holtzman MJ, and Chen CC (2004) Differential role of Janus family kinases (JAKs) in interferon-γ-induced lung epithelial ICAM-1 expression: involving protein interactions between JAKs, phospholipase Cγ, c-Src, and STAT1. Mol Pharmacol 65:589-598.
11. Chen CN, Sung CT, Lin MT, Lee PH, and Chang KJ (2001) Clinicopathologic association of cyclooxygenase 1 and cyclooxygenase 2 expression in gastric adenocarcinoma. Ann Surg 233:183-188,
12. Deva R, Shankaranarayanan P, Ciccoli R, and Nigam S (2003) Candida albicans induces selectively transcriptional activation of cyclooxygenase-2 in HeLa cells: pivotal roles of Toll-like receptors, p38 mitogen-activated protein kinase and NF-kappa B. J Immunol. 171:3047-3055.
13. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, et al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature (Lond) 408:740-745.
14. Huang WC, Chen JJ, and Chen CC (2003a) c-Src-dependent tyrosine phosphorylation of IKKβ is involved in tumor necrosis factor-α- induced intercellular adhesion molecule-1 expression. J Biol Chem 278:9944-9952.
15. Huang WC, Chen JJ, Inoue H, and Chen CC (2003b) Tyrosine phosphorylation of I-κB kinase α/β by protein kinase C-dependent c-Src activation is involved in TNF-α-induced cyclooxygenase-2 expression. J Immunol 170:4767-4775.
16. Inoue H, Yokoyama C, Hara S, Tone Y, and Tanabe T (1995) Transcriptional regulation of human prostaglandin-endoperoxide synthase-2 gene by lipopolysaccharide and phorbol ester in vascular endothelial cells. Involvement of both nuclear factor for interleukin-6 expression site and cAMP response element. J Biol Chem 270:24965-24971.
17. Jackson LM, Wu KC, Mahida YR, Jenkins D, and Hawkey CJ (2000) Cyclooxygenase 1 and 2 in normal, inflamed and ulcerated human gastric mucosa. Gut 47:762-770.
18. Juttner S, Cramer T, Wessler S, Walduck A, Gao F, Schmitz F, Wunder C, Weber M, Fischer SM, Schmidt WE, et al. (2003) Helicobacter pylori stimulates host cyclooxygenase-2 gene transcription: critical importance of MEK/ERK-dependent activation of USF1/-2 and CREB transcription factors. Cell Microbiol 5:821-834.
19. Keates S, Hitti YS, Upton M, and Kelly CP (1997) Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells. Gastroenterology 113:1099-1109.
20. Kidd M, Peek RM, Lastovica AJ, Israel DA, Kummer AF, and Louw JA (2001) Analysis of iceA genotypes in South African Helicobacter pylori strains and relationship to clinically significant disease. Gut 49:629-635.
21. Kosaka T, Miyata A, Ihara H, Kara S, Sugimoto T, Takeda O, Takahashi E, and Tanabe T (1994) Characterization of the human gene (PTGS2) encoding prostaglandin-endoperoxide synthase 2. Eur J Biochem. 221:889-897.
22. Malinin NL, Boldin MP, Rovalenko AV, and Wallach D (1997) MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature (Lond) 385:540-544.
23. Muta T and Takeshige K (2001) Essential roles of CD14 and lipopolysaccharide-binding protein for activation of toll-like receptor (TLR)2 as well as TLR4 Reconstitution of TLR2- and TLR4-activation by distinguishable ligands in LPS preparations. Eur J Biochem 268:4580-4589.
24. Nogueira C, Figueiredo C, Carneiro F, Gomes AT, Barreira R, Figueira P, Salgado C, Belo L, Peixoto A, Bravo JC, et al. (2001) Helicobacter pylori genotypes may determine gastric histopathology. Am J Pathol 158:647-654.
25. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, and Sibley RK (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127-1131.
26. Passaro DJ, Chosy EJ, and Parsonnet J (2002) Helicobacter pylori: consensus and controversy. Clin Infect Dis 35:298-304.
27. Peek RM and Blaser MJ (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2:28-37.
28. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, et al. (1998) Defective LPS signaling in C3H/Hel and C57BL/ 10ScCr mice: mutation in TLR4 gene. Science (Wash DC) 282:2085-2088.
29. Prinz C, Schoniger M, Rad R, Becker I, Keiditsch E, Wagenpfeil S, Classen M, Rosch T, Schepp W, and Gerhard M (2001) Key importance of the Helicobacter pylori adherence factor blood group antigen binding adhesin during chronic gastric inflammation. Cancer Res 61:1903-1909,
30. Rock FL, Hardiman G, Timans JC, Kastelein RA, and Bazan JF (1998) A family of human receptors structurally related to Drosophila Toll. Proc Natl Acad Sci 95:588-593.
31. Romano M, Ricci V, Memoli A, Tuccillo C, Di Popolo A, Sommi P, Acquaviva AM, Del Vecchio Blanco C, Bruni CB, and Zarrilli R (1998) Helicobacter pylori up-regulates cyclooxygenase-2 mRNA expression and prostaglandin E2 synthesis in MKN 28 gastric mucosal cells in vitro. J Biol Chem 273:28560-28563.
32. Sheu BS, Sheu SM, Yang HB, Huang AH, and Wu JJ (2003) Host gastric Lewis expression determines the bacterial density of Helicobacter pylori in babA2 genopositive infection. Gut 52:927-932.
33. Smith MF Jr, Mitchell A, Li G, Ding S, Fitzmaurice AM, Ryan K, Crowe S, and Goldberg JB (2003) Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-κB activation and chemokine expression by epithelial cells. J Biol Chem 278:32552-32560.
34. Song SH, Jong HS, Choi HH, Inoue H, Tanabe T, Kim NK, and Bang YJ (2001) Transcriptional silencing of Cyclooxygenase-2 by hyper-methylation of the 5′ CpG island in human gastric carcinoma cells. Cancer Res 61:4628-4635.
35. Sung JJ, Leung WK, Go MY, To KF, Cheng AS, Ng EK, and Chan FK (2000) Cyclooxygenase-2 expression in Helicobacter pylori-associated premalignant and malignant gastric lesions. Am J Pathol 157:729-735.
36. Takahashi S, Fujita T, and Yamamoto A (2000) Role of cyclooxygenase-2 in Helicobacter pylori- induced gastritis in Mongolian gerbils. Am J Physiol 279:G791-G798.
37. Takeshita F, Leifer CA, Gursel I, Ishii KJ, Takeshita S, Gursel M, and Klinman DM (2001) Role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J Immunol 167:3555-3558.
38. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, and Akira S (1999) Differential role of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacteria cell wall components. Immunity 11:443-451.
39. van Rees BP, Saukkonen K, Ristimaki A, Polkowski W, Tytgat GN, Drillenburg P, and Offerhaus GJ (2002) Cyclooxygenase-2 expression during carcinogenesis in the human stomach. J Pathol 196:171-199.
40. Wambura C, Aoyama N, Shirasaka D, Sakai T, Ikemura T, Sakashita M, Maekawa S, Kuroda K, Inoue T, Ebara S, et al. (2002) Effect of Helicobacter pylori-induced cyclooxygenase-2 on gastric epithelial cell kinetics: implication for gastric carcinogenesis. Helicobacter 7:129-138.
41. Wang HJ, Kuo CH, Yeh AM, Chang CL, and Wang WC (1998) Vacuolating toxin production in clinical isolates of Helicobacter pylori with different vacA genotypes. J Infect Dis 178:207-212.
42. Yamamoto K, Arakawa T, Ueda N, and Yamamoto S (1995) Transcriptional roles of NF-κB NF-IL6 in the TNAα-dependent induction of cyclooxygenase-2 in MC3T3-E1 cells. J Biol Chem 270:31315-31320.
43. Yamaoka Y, Kodama T, Kashima K, Graham DY, and Sepulveda AE (1998) Variants of the 3′ region of the cagA gene in Helicobacter pylori isolates from patients with different H. pylori-associated diseases. J Clin Microbiol 36:2258-2263.
44. Yang RB, Mark MR, Gray A, Huang A, Xie MH, Zhang M, Goddard A, Wood WI, Gurney AL, and Godowski PJ (1998) Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature (Lond) 395:284-288.