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Infection and Immunity, November 2005, p. 7602-7612, Vol. 73, No. 11
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.11.7602-7612.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Regulation of RANTES Promoter Activation in Gastric Epithelial Cells Infected with Helicobacter pylori

Takahiko Kudo,1 Hong Lu,1 Jeng Yih Wu,1 David Y. Graham,1 Antonella Casola,2 and Yoshio Yamaoka1*

Department of Medicine, Michael E. DeBakey Veterans Affairs Medical Center, and Baylor College of Medicine, Houston, Texas 77030,1 Department of Pediatrics, University of Texas Medical Branch, Galveston, Texas 775552

Received 7 June 2005/ Returned for modification 15 July 2005/ Accepted 22 July 2005

RANTES, a CC chemokine, plays an important role in the inflammatory response associated with Helicobacter pylori infection. However, the mechanism by which H. pylori induces RANTES expression in the gastric mucosa is unknown. We cocultured gastric epithelial cells with wild-type H. pylori, isogenic oipA mutants, cag pathogenicity island (PAI) mutants, or double knockout mutants. Reverse transcriptase PCR showed that RANTES mRNA was induced by H. pylori and that the expression was both OipA and cag PAI dependent. Luciferase reporter gene assays and electrophoretic mobility shift assays showed that maximal H. pylori-induced RANTES gene transcription required the presence of the interferon-stimulated responsive element (ISRE), the cyclic AMP-responsive element (CRE), nuclear factor-interleukin 6 (NF-IL-6), and two NF-{kappa}B sites. OipA- and cag PAI-dependent pathways included NF-{kappa}B->NF-{kappa}B/NF-IL-6/ISRE pathways, and cag PAI-dependent pathways additionally included Jun N-terminal kinase->CRE/NF-{kappa}B pathways. The OipA-dependent pathways additionally included p38->CRE/ISRE pathways. We confirmed the in vitro effects in vivo by examining RANTES mRNA levels in biopsy specimens from human gastric antral mucosa. RANTES mRNA levels in the antral mucosa were significantly higher for patients infected with cag PAI/OipA-positive H. pylori than for those infected with cag PAI/OipA-negative H. pylori or uninfected patients. The mucosal inflammatory response to H. pylori infection involves different signaling pathways for activation of the RANTES promoter, with both OipA and the cag PAI being required for full activation of the RANTES promoter.

* Corresponding author. Mailing address: Department of Medicine, Michael E. DeBakey Veterans Affairs Medical Center, 2002 Holcombe Blvd., (111D) Rm. 3A-320, Houston, TX 77030. Phone: (713) 794-7597. Fax: (713) 790-1040. E-mail: yyamaoka{at}bcm.tmc.edu.

Editor: J. D. Clements

Infection and Immunity, November 2005, p. 7602-7612, Vol. 73, No. 11
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.11.7602-7612.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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