Helicobacter pylori infection stimulates plasminogen activator inhibitor 1 production by gastric epithelial cells

Infection and Immunity

Volumn 76, Issue 9, 2008, Pages 3992-3999

  Keates, A C ^a   Tummala, S ^a   Peek Jr , R M ^b   Csizmadia, E ^a   Kunzli, B ^c   Becker, K ^c   Correa, P ^b   Romero Gallo, J ^b   Piazuelo, M B ^b   Sheth, S ^a   Kelly, C P ^a   Robson, S C ^a   Keates, S ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SMALL INTERFERING RNA;

ADULT; ANGIOGENESIS; ARTICLE; BIOPSY; CAGA GENE; CAGE GENE; CARCINOGENESIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; GASTRITIS; GENE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; STOMACH; UPREGULATION;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FEMALE; GASTRIC MUCOSA; GENE DELETION; GENE EXPRESSION PROFILING; HELICOBACTER PYLORI; HUMANS; MALE; MIDDLE AGED; PLASMINOGEN ACTIVATOR INHIBITOR 1; UP-REGULATION;

EID: 51949083035     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00584-08     Document Type: Article

References (39)

1. Backert, S., E. Ziska, V. Brinkmann, U. Zimny-Arndt, A. Fauconnier, P. R. Jungblut, M. Naumann, and T. F. Meyer. 2000. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2:155-164.
2. Bagnoli, F., L. Buti, L. Tompkins, A. Covacci, and M. R. Amieva. 2005. Helicobacter pylori CagA induces a transition from polarized to invasive phenotypes in MDCK cells. Proc. Natl. Acad. Sci. USA 102:16339-16344.
3. Berger, D. H. 2002. Plasmin/plasminogen system in colorectal cancer. World J. Surg. 26:767-771.
4. Beyer, B. C, M. M. Heiss, E. H. Simon, K. U. Gruetzner, R. Babic, K. W. Jauch, F. W. Schildberg, and H. Allgayer. 2006. Urokinase system expression in gastric carcinoma: prognostic impact in an independent patient series and first evidence of predictive value in preoperative biopsy and intestinal metaplasia specimens. Cancer 106:1026-1035.
5. Censini, S., C. Lange, Z. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 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.
6. Chorostowska-Wynimko, J., E. Skrzypczak-Jankun, and J. Jankun. 2004. Plasminogen activator inhibitor type-1: its structure, biological activity and role in tumorigenesis. Int. J. Mol. Med. 13:759-766.
7. Crawford, H. C, U. S. Krishna, D. A. Israel, L. M. Matrisian, M. K. Washington, and R. M. Peek, Jr. 2003. Helicobacter pylori strain-selective induction of matrix metalloproteinase-7 in vitro and within gastric mucosa. Gastroenterology 125:1125-1136.
8. Czekay, R. P., and D. J. Loskutoff. 2004. Unexpected role of plasminogen activator inhibitor 1 in cell adhesion and detachment. Exp. Biol. Med. (Maywood) 229:1090-1096.
9. Demyanets, S., C. Kaun, K. Rychli, G. Rega, S. Pfaffenberger, T. Afonyushkin, V. N. Bochkov, G. Maurer, K. Huber, and J. Wojta. 2007. The inflammatory cytokine oncostatin M induces PAI-1 in human vascular smooth muscle cells in vitro via PI 3-kinase and ERKl/2-dependent pathways. Am. J. Physiol. Heart Circ. Physiol. 293:H1962-H1968.
10. Franco, A. T., D. A. Israel, M. K. Washington, U. Krishna, J. G. Fox, A. B. Rogers, A. S. Neish, L. Collier-Hyams, G. I. Perez-Perez, M. Hatakeyama, R. Whitehead, K. Gaus, D. P. O'Brien, J. Romero-Gallo, and R. M. Peek, Jr. 2005. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc. Natl. Acad. Sci. USA 102:10646-10651.
11. Fujii, T., T. Obara, S. Tanno, H. Ura, and Y. Kongo. 1999. Urokinase-type plasminogen activator and plasminogen activator inhibitor-1 as a prognostic factor in human colorectal carcinomas. Hepatogastroenterology 46:2299-2308.
12. Handa, O., Y. Naito, and T. Yoshikawa. 2007. CagA protein of Helicobacter pylori: a hijacker of gastric epithelial cell signaling. Biochem. Pharmacol. 73:1697-1702.
13. Higashi, H, R. Tsutsumi, S. Muto, T. Sugiyama, T. Azuma, M. Asaka, and M. Hatakeyama. 2002. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295:683-686.
14. Iwamoto, J., Y. Mizokami, K. Takahashi, K. Nakajima, T. Ohtsubo, S. Miura, T. Narasaka, H. Takeyama, T. Omata, K. Shimokobe, M. Ito, H. Takehara, and T. Matsuoka. 2005. Expressions of urokinase-type plasminogen activator, its receptor and plasminogen activator inhibitor-1 in gastric cancer cells and effects of Helicobacter pylori. Scand. J. Gastroenterol. 40:783-793.
15. Kaneko, T., H. Konno, M. Baba, T. Tanaka, and S. Nakamura. 2003. Urokinase-type plasminogen activator expression correlates with tumor angiogen-esis and poor outcome in gastric cancer. Cancer Sci. 94:43-49.
16. Keates, S., A. C. Keates, E. Mizoguchi, A. Bhan, and C. P. Kelly. 1997. Enterocytes are the primary source of the chemokine ENA-78 in normal colon and ulcerative colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 273:G75-G82.
17. Keates, S., A. C. Keates, S. Nath, R. M. Peek, Jr., and C. P. Kelly. 2005. Transactivation of the epidermal growth factor receptor by cag+ Helicobacter pylori induces upregulation of the early growth response gene Egr-1 in gastric epithelial cells. Gut 54:1363-1369.
18. Keates, S., A. C. Keates, M. Warny, R. M. Peek, Jr., P. G. Murray, and C. P. Kelly. 1999. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J. Immunol. 163:5552-5559.
19. Keates, S., S. Sougioultzis, A. C. Keates, D. Zhao, R. M. Peek, Jr., L. M. Shaw, and C. P. Kelly. 2001. cag+ Helicobacter pylori induce transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J. Biol. Chem. 276:48127-48134.
20. Kim, K. R., T. Yoshizaki, H. Miyamori, K. Hasegawa, T. Horikawa, M. Furukawa, S. Harada, M. Seiki, and H. Sato. 2000. Transformation of Madin-Darby canine kidney (MDCK) epithelial cells by Epstein-Barr virus latent membrane protein 1 (LMP1) induces expression of Etsl and invasive growth. Oncogene 19:1764-1771.
21. Krueger, S., T. Hundertmark, T. Kalinski, U. Peitz, T. Wex, P. Malfertheiner, M. Naumann, and A. Roessner. 2006. Helicobacter pylori encoding the pathogenicity island activates matrix metalloproteinase 1 in gastric epithelial cells via JNK and ERK. J. Biol. Chem. 281:2868-2875.
22. -ΔΔCT method. Methods 25:402-408.
23. Mimuro, II.. T. Suzuki, J. Tanaka, M. Asahi, R. Haas, and C. Sasakawa. 2002. Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol. Cell 10:745-755.
24. Montuori, N., G. Rossi, and P. Ragno. 2002. Post-transcriptional regulation of gene expression in the plasminogen activation system. Biol. Chem. 383:47-53.
25. Mueller, A., S. Falkow, and M. R. Amieva. 2005. Helicobacter pylori and gastric cancer: what can be learned by studying the response of gastric epithelial cells to the infection? Cancer Epidemiol. Biomarkers Prev. 14: 1859-1864.
26. Odenbreit, S., J. Puls, B. Sedlmaier, E. Gerland, W. Fischer, and R. Haas. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497-1500.
27. Oliveira, M. J., A. C. Costa, A. M. Costa, L. Henriques, G. Suriano, J. C. Atherton, J. C. Machado, F. Carneiro, R. Seruca, M. Mareel, A. Leroy, and C. Figueiredo. 2006. Helicobacter pylori induces gastric epithelial cell invasion in a c-Met and type IV secretion system-dependent manner. J. Biol. Chem. 281:34888-34896.
28. Parsonnet, J. 1993. Helicobacter pylori and gastric cancer. Gastroenterol. Clin. North Am. 22:89-104.
29. Peek, R. M., Jr., G. G. Miller, K. T. Tham, G. I. Perez-Perez, X. Zhao, J. C. Atherton, and M. J. Blaser. 1995. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab. Investig. 73:760-770.
30. Pillinger, M. H., N. Marjanovic, S. Y. Kim, Y. C. Lee, J. U. Scher, J. Roper, A. M. Abeles, P. I. Izmirly, M. Axelrod, M. Y. Pillinger, S. Tolani, V. Dinsell, S. B. Abramson, and M. J. Blaser. 2007. Helicobacter pylori stimulates gastric epithelial cell MMP-1 secretion via CagA-dependent and -independent ERK activation. J. Biol. Chem. 282:18722-18731.
31. Price, A. B. 1991. The Sydney System: histological division. J. Gastroenterol. Hepatol. 6:209-222.
32. Providence, K. M., and P. J. Higgins. 2004. PAI-1 expression is required for epithelial cell migration in two distinct phases of in vitro wound repair. J. Cell Physiol. 200:297-308.
33. Sakakibara, T., K. Hibi, M. Koike, M. Fujiwara, Y. Kodera, K. Ito, and A. Nakao. 2006. Plasminogen activator inhibitor-1 as a potential marker for the malignancy of gastric cancer. Cancer Sci. 97:395-399.
34. Son, D. S., and K. K. Rozman. 2002. 2,3,7,8-Tetrachlorodibenzo-p- dioxin (TCDD) induces plasminogen activator inhibitor-1 through an aryl hydrocarbon receptor-mediated pathway in mouse hepatoma cell lines. Arch. Toxicol. 76:404-413.
35. Stamenkovic, I. 2000. Matrix metalloproteinases in tumor invasion and metastasis. Semin. Cancer Biol. 10:415-433.
36. Stein, M., F. Bagnoli, R. Halenbeck, R. Rappuoli, W. J. Fantl, and A. Covacci. 2002. c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol. Microbiol. 43:971-980.
37. Stein, M., R. Rappuoli, and A. Covacci. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA 97:1263-1268.
38. .Varro, A., P. J. Noble, D. M. Pritchard, S. Kennedy, C. A. Hart, R. Dimaline, and G. J. Dockray. 2004. Helicobacter pylori induces plasminogen activator inhibition in gastric epithelial cells through nuclear factor-KB and Rho: implications for invasion and apoptosis. Cancer Res. 64:1695-1702.
39. Vidal, B., M. Parra, M. Jardi, S. Saito, E. Appella, and P. Munoz-Canoves. 2005. The alkylating carcinogen N-methyl-N'-nitro-N- nitrosoguanidine activates the plasminogen activator inhibitor-1 gene through sequential phosphorylation of p53 by ATM and ATR kinases. Thromb. Haemost. 93:584-591.