Regulation of interleukin-6 promoter activation in gastric epithelial cells infected with Helicobacter pylori

Molecular Biology of the Cell

Volumn 16, Issue 10, 2005, Pages 4954-4966

  Lu, Hong ^a   Wu, Jeng Yih ^a,c   Kudo, Takahiko ^a   Ohno, Tomoyuki ^b   Graham, David Y ^a   Yamaoka, Yoshio ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; RAC1 PROTEIN; RAF PROTEIN; RAS PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

ARTICLE; BINDING SITE; CAG GENE; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; EPITHELIUM CELL; GEL MOBILITY SHIFT ASSAY; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; OIPA GENE; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REPORTER GENE; STOMACH EPITHELIUM;

CCAAT-ENHANCER-BINDING PROTEINS; CELLS, CULTURED; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GASTRIC MUCOSA; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTERLEUKIN-6; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMOTER REGIONS (GENETICS); SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

HELICOBACTER PYLORI;

EID: 26244445594     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-05-0426     Document Type: Article

References (47)

1. Aihara, M., Tsuchimoto, D., Takizawa, H., Azuma, A., Wakebe, H., Ohmoto, Y., Imagawa, K., Kikuchi, M., Mukaida, N., and Matsushima, K. (1997). Mechanisms involved in Helicobacter pylori-induced interleukin-8 production by a gastric cancer cell line, MKN45. Infect. Immun. 65, 3218-3224.
2. Akanuma, M. et al. (2002). The evaluation of putative virulence factors of Helicobacter pylori for gastroduodenal disease by use of a short-term Mongolian gerbil infection model. J. Infect. Dis. 185, 341-347.
3. Akira, S. (1997). IL-6-regulated transcription factors. Int. J. Biochem. Cell Biol. 29, 1401-1418.
4. Ando, T. et al. (1998). Differential normalization of mucosal interleukin-8 and interleukin-6 activity after Helicobacter pylori eradication. Infect. Immun. 66, 4742-4747.
5. Ando, T., Peek, R. M., Jr., Lee, Y. C., Krishna, U., Kusugami, K., and Blaser, M. J. (2002). Host cell responses to genotypically similar Helicobacter pylori isolates from United States and Japan. Clin. Diagn. Lab. Immunol. 9, 167-175.
6. Atherton, J. C., Cao, P., Peek, R. M., Jr., Tummuru, M. K., Blaser, M. J., and Cover, T. L. (1995). Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J. Biol. Chem. 270, 17771-17777.
7. Beyaert, R., Cuenda, A., Vanden Berghe, W., Plaisance, S., Lee, J. C., Haegeman, G., Cohen, P., and Fiers, W. (1996). The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 15, 1914-1923.
8. Brasier, A. R., Jamaluddin, M., Casola, A., Duan, W., Shen, Q., and Garofalo, R. P. (1998). A promoter recruitment mechanism for tumor necrosis factor-alpha-induced interleukin-8 transcription in type II pulmonary epithelial cells. Dependence on nuclear abundance of Rel A, NF-kappaB1, and c-Rel transcription factors. J. Biol. Chem. 273, 3551-3561.
9. Brunner, D., Ducker, K., Oellers, N., Hafen, E., Scholz, H., and Klambt, C. (1994). The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370, 386-389.
10. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., Ghiara, P., Borodovsky, M., Rappuoli, R., and Covacci, A. (1996). cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93, 14648-14653.
11. Coso, O. A., Chiariello, M., Yu, J. C., Teramoto, H., Crespo, P., Xu, N., Miki, T., and Gutkind, J. S. (1995). The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
12. Crabtree, J. E., Shallcross, T. M., Heatley, R. V., and Wyatt, J. I. (1991). Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut 32, 1473-1477.
13. Crawford, H. C., Krishna, U. S., Israel, D. A., Matrisian, L. M., Washington, M. K., and Peek, R. M., Jr. (2003). Helicobacter pylori strain-selective induction of matrix metalloproteinase-7 in vitro and within gastric mucosa. Gastroenterology 125, 1125-1136.
14. Frost, R. A., Nystrom, G. J., and Lang, C. H. (2003). Lipopolysaccharide and proinflammatory cytokines stimulate interleukin-6 expression in C2C12 myoblasts: role of the Jun NH2-terminal kinase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R1153-R1164.
15. Furukawa, K., Takahashi, T., Arai, F., Matsushima, K., and Asakura, H. (1998). Enhanced mucosal expression of interleukin-6 mRNA but not of interleukin-8 mRNA at the margin of gastric ulcer in Helicobacter pylori-positive gastritis. J. Gastroenterol. 33, 625-633.
16. Gille, H., Sharrocks, A. D., and Shaw, P. E. (1992). Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature 358, 414-417.
17. Gobert, A. P., Bambou, J. C., Werts, C., Balloy, V., Chignard, M., Moran, A. P., and Ferrero, R. L. (2004). Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J. Biol. Chem. 279, 245-250.
18. Heuermann, D., and Haas, R. (1998). A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol. Gen. Genet. 257, 519-528.
19. Hwang, I. R., Hsu, P. I., Peterson, L. E., Gutierrez, O., Kim, J. G., Graham, D. Y., and Yamaoka, Y. (2003). Interleukin-6 genetic polymorphisms are not related to Helicobacter pylori-associated gastroduodenal diseases. Helicobacter 8, 142-148.
20. Keates, S., Keates, A. C., Warny, M., Peek, R. M., Jr., Murray, P. G., and Kelly, C. P. (1999). Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J. Immunol. 163, 5552-5559.
21. Keates, S., Sougioultzis, S., Keates, A. C., Zhao, D., Peek, R. M., Jr., Shaw, L. M., and Kelly, C. P. (2001). cag+ Helicobacter pylori induce transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J. Biol. Chem. 276, 48127-48134.
22. Kudo, T., Nurgalieva, Z. Z., Conner, M. E., Crawford, S., Odenbreit, S., Haas, R., Graham, D. Y., and Yamaoka, Y. (2004). Correlation between Helicobacter pylori OipA protein expression and oipA gene switch status. J. Clin. Microbiol. 42, 2279-2281.
23. Meyer-ter-Vehn, T., Covacci, A., Kist, M., and Pahl, H. L. (2000). Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-jun. J. Biol. Chem. 275, 16064-16072.
24. Muraoka, O., Kaisho, T., Tanabe, M., and Hirano, T. (1993). Transcriptional activation of the interleukin-6 gene by HTLV-1 p40tax through an NF-kappa B-like binding site. Immunol. Lett. 37, 159-165.
25. Naumann, M., Wessler, S., Bartsch, C., Wieland, B., Covacci, A., Haas, R., and Meyer, T. F. (1999). Activation of activator protein 1 and stress response kinases in epithelial cells colonized by Helicobacter pylori encoding the cag pathogenicity island. J. Biol. Chem. 274, 31655-31662.
26. Odenbreit, S., Kavermann, H., Puls, J., and Haas, R. (2002). CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from alpAB, HopZ and bab group outer membrane proteins. Int. J. Med. Microbiol. 292, 257-266.
27. O'Neill, E. M., Rebay, I., Tjian, R., and Rubin, G. M. (1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137-147.
28. Plaisance, S., Vanden Berghe, W., Boone, E., Fiers, W., and Haegeman, G. (1997). Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kappaB site of the interleukin-6 promoter and acts as a negative regulatory factor. Mol. Cell Biol. 37, 3733-3743.
29. Pritts, T. A., Hungness, E. S., Hershko, D. D., Robb, B. W., Sun, X., Luo, G. J., Fischer, J. E., Wong, H. R., and Hasselgren, P. O. (2002). Proteasome inhibitors induce heat shock response and increase IL-6 expression in human intestinal epithelial cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1016-R1026.
30. Shibata, T., Imaizumi, T., Tamo, W., Matsumiya, T., Kumagai, M., Cui, X. F., Yoshida, H., Takaya, S., Fukuda, I., and Satoh, K. (2002). Proteasome inhibitor MG-132 enhances the expression of interleukin-6 in human umbilical vein endothelial cells: Involvement of MAP/ERK kinase. Immunol. Cell Biol. 80, 226-230.
31. Sun, Y., Wenger, L., Brinckerhoff, C. E., Misra, R. R., and Cheung, H. S. (2002). Basic calcium phosphate crystals induce matrix metalloproteinase-1 through the Ras/mitogen-activated protein kinase/c-Fos/AP-1/metalloproteinase 1 pathway. Involvement of transcription factor binding sites AP-1 and PEA-3. J. Biol. Chem. 277, 1544-1552.
32. Tanahashi, T., Kita, M., Kodama, T., Yamaoka, Y., Sawai, N., Ohno, T., Mitsufuji, S., Wei, Y. P., Kashima, K., and Imanishi, J. (2000). Cytokine expression and production by purified Helicobacter pylori urease in human gastric epithelial cells. Infect. Immun. 68, 664-671.
33. Vanden Berghe, W., De Bosscher, K., Boone, E., Plaisance, S., and Haegeman, G. (1999). The nuclear factor-kappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J. Biol. Chem. 274, 32091-32098.
34. Vanden Berghe, W., Plaisance, S., Boone, E., De Bosscher, K., Schmitz, M. L., Fiers, W., and Haegeman, G. (1998). p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor. J. Biol. Chem. 273, 3285-3290.
35. Vanden Berghe, W., Vermeulen, L., De Wilde, G., De Bosscher, K., Boone, E., and Haegeman, G. (2000). Signal transduction by tumor necrosis factor and gene regulation of the inflammatory cytokine interleukin-6. Biochem. Pharmacol. 60, 1185-1195.
36. Varro, A., Noble, P. J., Pritchard, D. M., Kennedy, S., Hart, C. A., Dimaline, R., and Dockray, G. J. (2004). Helicobacter pylori induces plasminogen activator inhibitor 2 in gastric epithelial cells through nuclear factor-kappaB and RhoA: implications for invasion and apoptosis. Cancer Res. 64, 1695-1702.
37. Vermeulen, L., De Wilde, G., Van Damme, P., Vanden Berghe, W., and Haegeman, G. (2003). Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324.
38. Watanabe, T., Tada, M., Nagai, H., Sasaki, S., and Nakao, M. (1998). Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gasrroenterology 115, 642-648.
39. Wessler, S., Hocker, M., Fischer, W., Wang, T. C., Rosewicz, S., Haas, R., Wiedenmann, B., Meyer, T. F., and Naumann, M. (2000). Helicobacter pylori activates the histidine decarboxylase promoter through a mitogen-activated protein kinase pathway independent of pathogenicity island-encoded virulence factors. J. Biol. Chem. 275, 3629-3636.
40. Wessler, S., Rapp, U. R., Wiedenmann, B., Meyer, T. F., Schoneberg, T., Hocker, M., and Naumann, M. (2002). B-Raf/Rap1 signaling, but not c-Raf-1/Ras, induces the histidine decarboxylase promoter in Helicobacter pylori infection. FASEB J. 16, 417-419.
41. Wroblewski, L. E., Noble, P. J., Pagliocca, A., Pritchard, D. M., Hart, C. A., Campbell, F., Dodson, A. R., Dockray, G. J., and Varro, A. (2003). Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J. Cell Sci. 116, 3017-3026.
42. Yamaoka, Y., Kikuchi, S., el-Zimaity, H. M., Gutierrez, O., Osato, M. S., and Graham, D.Y. (2002). Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology 123, 414-424.
43. Yamaoka, Y., Kita, M., Kodama, T., Sawai, N., and Imanishi, J. (1996). Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 110, 1744-1752.
44. Yamaoka, Y., Kita, M., Kodama, T., Sawai, N., Kashima, K., and Imanishi, J. (1997). Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 41, 442-451.
45. Yamaoka, Y., Kodama, T., Kita, M., Imanishi, J., Kashima, K., and Graham, D. Y. (2001). Relation between cytokines and Helicobacter pylori in gastric cancer. Helicobacter 6, 116-124.
46. Yamaoka, Y., Kudo, T., Lu, H., Casola, A., Brasier, A. R., and Graham, D. Y. (2004). Role of interferon-stimulated responsive element-like element in interleukin-8 promoter in Helicobacter pylori infection. Gastroenterology 126, 1030-1043.
47. Yamaoka, Y., Kwon, D. H., and Graham, D. Y. (2000). A M(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc. Natl. Acad. Sci. USA 97, 7533-7538.