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Infection and Immunity, July 2003, p. 3748-3756, Vol. 71, No. 7
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.7.3748-3756.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Helicobacter pylori Induces RANTES through Activation of NF-{kappa}B

Naoki Mori,1* Alan M. Krensky,2 Romas Geleziunas,3 Akihiro Wada,4 Toshiya Hirayama,4 Chihiro Sasakawa,5 and Naoki Yamamoto6

Department of Virology, Faculty of Medicine, University of the Ryukyus, Okinawa,1 Department of Bacteriology, Institute of Tropical Medicine, Nagasaki University, Nagasaki,4 Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo,5 Department of Molecular Virology, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan,6 Department of Pediatrics, Stanford University School of Medicine, Stanford, California,2 Merck Research Laboratories, Merck & Company, Inc., West Point, Pennsylvania3

Received 26 November 2002/ Returned for modification 23 January 2003/ Accepted 31 March 2003

Helicobacter pylori-infected gastric mucosa displays a conspicuous infiltration of mononuclear cells and neutrophils. RANTES (short for "regulated upon activation, normal T cell expressed and secreted") is a chemoattractant cytokine (chemokine) important in the infiltration of T lymphocytes and monocytes. RANTES may therefore contribute to the cellular infiltrate in the H. pylori-infected gastric mucosa. The aim of this study was to analyze the molecular mechanism responsible for H. pylori-mediated RANTES expression. We observed that gastric epithelial cells produced RANTES upon coculture with H. pylori. In addition, H. pylori induced RANTES mRNA expression and an increase in luciferase activity in cells which were transfected with a luciferase reporter construct derived from the RANTES promoter, in gastric epithelial cells, indicating that the induction of RANTES production occurred at the transcriptional level. Induction of RANTES was dependent on an intact cag pathogenicity island. Activation of the RANTES promoter by H. pylori occurred through the action of NF-{kappa}B. Transfection of kinase-deficient mutants of I{kappa}B kinase (IKK) and NF-{kappa}B-inducing kinase (NIK) inhibited H. pylori-mediated RANTES activation. In contrast, tumor necrosis factor alpha- or interleukin-1/Toll-like receptor signaling molecules—such as mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1, MyD88, and interleukin-1 receptor-associated kinase—did not play a role in RANTES activation by H. pylori. Collectively, H. pylori induced NF-{kappa}B activation through an intracellular signaling pathway that involved IKK and NIK, leading to RANTES gene transcription. RANTES induction by H. pylori may play an important role in gastric inflammation.

* Corresponding author. Mailing address: Department of Virology, Faculty of Medicine, University of the Ryukyus, 207 Uehara, Nishihara, Okinawa 903-0215, Japan. Phone: 81-98-895-1130. Fax: 81-98-895-1410. E-mail: n-mori{at}med.u-ryukyu.ac.jp.

Editor: J. D. Clements

Infection and Immunity, July 2003, p. 3748-3756, Vol. 71, No. 7
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.7.3748-3756.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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