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Originally published In Press as doi:10.1074/jbc.M111883200 on April 8, 2002

J. Biol. Chem., Vol. 277, Issue 25, 22131-22139, June 21, 2002
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Lipopolysaccharide-mediated Reactive Oxygen Species and Signal Transduction in the Regulation of Interleukin-1 Gene Expression*

Hsien-Yeh HsuDagger § and Meng-Hsuan WenDagger

From the Dagger  Faculty of Medical Technology, Institute of Biotechnology in Medicine, National Yang-Ming University, 112 Taipei, Taiwan

Lipopolysaccharide (LPS) stimulates macrophages to release inflammatory cytokines, interleukin-1beta (IL-1), and tumor necrosis factor (TNF). LPS-induced TNF suppresses scavenger receptor functions in macrophages (van Lenten, B. J., and Fogelman, A. M. (1992) J. Immunol. 148, 112-116), which is regulated by TNF-mediated protein kinases (Hsu, H. Y., and Twu, Y. C. (2000) J. Biol. Chem. 275, 41035-41048). To examine the molecular mechanism for LPS induction of IL-1 in macrophages, we demonstrated that LPS quickly stimulated reactive oxygen species (ROS), and 3 h later induced prointerleukin-1beta (pro-IL-1, precursor of IL-1) production and IL-1 secretion. LPS stimulated pro-IL-1 message/protein between 3 and 10 h; however, there was a 40% reduction of pro-IL-1 in preincubation of the antioxidant, N-acetylcysteine (NAC). Moreover, NAC moderated LPS-induced IL-1 secretion partially via interleukin 1-converting enzyme. The maximal activity of LPS-induced ERK, JNK, and p38 was 12- (30 min), 5- (30 min), and 16-fold (15 min), respectively. In contrast, NAC reduced ERK activity to 60% and decreased p38 activity to the basal level, but JNK activity was induced 2-fold. Furthermore, the pharmacological antagonists LY294002, SB203580, curcumin, calphostin C, and PD98059 revealed the diverse roles of LPS-mediated protein kinases in pro-IL-1. On the other hand, NAC and diphenyleneiodonium chloride partially inhibited LPS-induced Rac activity and protein-tyrosine kinase (PTK), indicating that LPS-mediated ROS and NADPH oxidase correspond to Rac activation and IL-1 expression. Our findings establish for the first time that LPS-mediated PTK/phosphatidylinositol 3-kinase/Rac/p38 pathways play a more important role than pathways of PTK/PKC/MEK/ERK and of PTK/phosphatidylinositol 3-kinase/Rac/JNK in the regulation of pro-IL-1/IL-1. The findings also further elucidate the critical role of LPS-mediated ROS in signal transduction pathways. Our results suggest that understanding LPS-transduced signals in IL-1 induction upon the antibacterial action of macrophages should provide a therapeutic strategy for aberrant inflammatory responses leading to severe cellular injury or concurrent multiorgan septic damage.

* This work was supported by Research Grants NSC 90-2321-B-010-005 (to H.-Y. H.) from the National Science Council, Taiwan, NHRI-EX90-8937SL (to H.-Y. H.) from the National Health Research Institutes, Taiwan, and A-91-B-FA09-2-4 (to H.-Y. H.) Program for Promoting Academic Excellence of Universities from the Ministry of Education, Taiwan.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ To whom reprint requests and correspondence should be addressed: Faculty of Medical Technology, Institute of Biotechnology in Medicine, National Yang-Ming University, 155 Li-Nong St., Shih-Pai, Taipei, Taiwan. Tel.: 11-886-2-2826-7252; Fax: 11-886-2-2826-4092, E-mail: hyhsu@ym.edu.tw.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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