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Am J Physiol Cell Physiol (October 6, 2004). doi:10.1152/ajpcell.00319.2004
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Submitted on July 6, 2004
Accepted on September 30, 2004

Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase Nox1 and its organizer NOXO1 in guinea pig gastric mucosal cells

Tsukasa Kawahara1, Motoyuki Kohjima2, Yuki Kuwano1, Hisano Mino1, Shigetada Teshima-Kondo3, Ryu Takeya2, Shohko Tsunawaki4, Akihiro Wada5, Hideki Sumimoto2, and Kazuhito Rokutan3*

1 Departments of Nutritional Physiology, Institute of Health Biosciences, The University of Tokushima Graduate School, Tokushima, Tokushima Prefecture, Japan
2 Medical Institute of Bioregulation, Kyushu University, Fukuoka, Fukuoka Prefecture, Japan
3 Department of Stress Science, Institute of Health Biosciences, The University of Tokushima Graduate School, Tokushima, Tokushima Prefecture, Japan
4 Department of Infectious Diseases, National Research Institute for Child Health and Development, Tokyo, Japan
5 Institute of Tropical Medicine, Nagasaki University, Nagasaki, Nagasaki Prefecture, Japan

* To whom correspondence should be addressed. E-mail: rokutan{at}basic.med.tokushima-u.ac.jp.

Primary cultures of guinea pig gastric mucosal cells express NADPH oxidase 1 (Nox1), a homologue of gp91phox, and produce superoxide anion (O2-) at a rate of about 100 nmol/mg protein/h in response to Helicobacter pylori (H. pylori) lipopolysaccharide (LPS) from virulent type I strains. The up-regulated O2- production additionally enhances H. pylori LPS-stimulated tumor necrosis factor-{alpha} or cyclooxygenase-2 mRNA expression, suggestive of a potential role of Nox1 in the pathogenesis of H. pylori-associated diseases. The H. pylori LPS-stimulated O2- production in cultured gastric mucosal cells was inhibited by actinomycin D as well as cycloheximide, suggesting that the induction is regulated at the transcriptional level. The LPS treatment not only increased the Nox1 mRNA to a greater extent but also induced expression of the message encoding Nox organizer 1 (NOXO1), a novel p47phox homologue, required for the Nox1 activity. In addition, H. pylori LPS activated Rac1, i.e., conversion of Rac1 to the GTP-bound state. A phosphoinositide 3-kinase inhibitor LY294002 blocked the H. pylori LPS-induced Rac1 activation and O2- generation without interference with the expression of Nox1 and NOXO1 mRNAs. The O2- production inhibited with LY294002 was completely restored by transfection of an adenoviral vector encoding a constitutively active Rac1, but not an inactive Rac1 or a constitutively active Cdc42. These findings indicate that Rac1 plays a crucial role in the Nox1 activation. Thus, the H. pylori LPS-stimulated O2- production in gastric mucosal cells appears to require two distinct events: transcriptional up-regulation of Nox1 and NOXO1, and activation of Rac1.




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