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Originally published In Press as doi:10.1074/jbc.M102061200 on June 11, 2001

J. Biol. Chem., Vol. 276, Issue 32, 30188-30198, August 10, 2001
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Lipopolysaccharide Induces Rac1-dependent Reactive Oxygen Species Formation and Coordinates Tumor Necrosis Factor-alpha Secretion through IKK Regulation of NF-kappa B*

Salih SanliogluDagger §, Carl M. WilliamsDagger §, Lobelia SamavatiDagger , Noah S. ButlerDagger , Guoshun Wang||, Paul B. McCray Jr.||, Teresa C. Ritchie§**, Gary W. HunninghakeDagger , Ebrahim ZandiDagger Dagger §§, and John F. EngelhardtDagger §**¶¶

From the Dagger  Department of Internal Medicine-Division of Pulmonary and Critical Care, the § Center for Gene Therapy, ** Department of Anatomy and Cell Biology, and || Department of Pediatrics, the University of Iowa College of Medicine, Iowa City, Iowa 52242, the Dagger Dagger  Department of Molecular Microbiology & Immunology, Norris Cancer Center, Los Angeles, California 90033, and the  Department of Medical Biology and Genetics, Akdeniz University, College of Medicine, Antalya, Turkey 07070

Reactive oxygen species (ROS) are important second messengers generated in response to many types of environmental stress. In this setting, changes in intracellular ROS can activate signal transduction pathways that influence how cells react to their environment. In sepsis, a dynamic proinflammatory cellular response to bacterial toxins (e.g. lipopolysaccharide or LPS) leads to widespread organ damage and death. The present study demonstrates for the first time that the activation of Rac1 (a GTP-binding protein), and the subsequent production of ROS, constitutes a major pathway involved in NFkappa B-mediated tumor necrosis factor-alpha (TNFalpha ) secretion following LPS challenge in macrophages. Expression of a dominant negative mutant of Rac1 (N17Rac1) reduced Rac1 activation, ROS formation, NFkappa B activation, and TNFalpha secretion following LPS stimulation. In contrast, expression of a dominant active form of Rac1 (V12Rac1) mimicked these effects in the absence of LPS stimulation. IKKalpha and IKKbeta were both required downstream modulators of LPS-activated Rac1, since the expression of either of the IKK dominant mutants (IKKalpha KM or IKKbeta KA) drastically reduced NFkappa B-dependent TNFalpha secretion. Moreover, studies using CD14 blocking antibodies suggest that Rac1 induces TNFalpha secretion through a pathway independent of CD14. However, a maximum therapeutic inhibition of LPS-induced TNFalpha secretion occurred when both CD14 and Rac1 pathways were inhibited. Our results suggest that targeting both Rac1- and CD14-dependent pathways could be a useful therapeutic strategy for attenuating the proinflammatory cytokine response during the course of sepsis.

* This work was supported by National Institutes of Health NHLBI Grants HL60316 and DK54759 (to J. F. E.). A Leukemia and Lymphoma Special Fellow.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.

§§ A Leukemia and Lymphoma Special Fellow.

¶¶ To whom correspondence should be addressed: Dept. of Anatomy and Cell Biology, University of Iowa, College of Medicine, 51 Newton Rd., Rm. 1-111 BSB, Iowa City, IA 52242. Tel.: 319-335-7744; Fax: 319-335-7198; E-mail: john-engelhardt@uiowa.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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M. M. Monick, R. K. Mallampalli, M. Bradford, D. McCoy, T. J. Gross, D. M. Flaherty, L. S. Powers, K. Cameron, S. Kelly, A. H. Merrill Jr., et al.
Cooperative Prosurvival Activity by ERK and Akt in Human Alveolar Macrophages is Dependent on High Levels of Acid Ceramidase Activity
J. Immunol., July 1, 2004; 173(1): 123 - 135.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
I. Tritto and G. Ambrosio
The multi-faceted behavior of nitric oxide in vascular "inflammation": catchy terminology or true phenomenon?
Cardiovasc Res, July 1, 2004; 63(1): 1 - 4.
[Full Text] [PDF]

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 J. Immunol.Home page
O. Equils, Z. Madak, C. Liu, K. S. Michelsen, Y. Bulut, and D. Lu
Rac1 and Toll-IL-1 Receptor Domain-Containing Adapter Protein Mediate Toll-Like Receptor 4 Induction of HIV-Long Terminal Repeat
J. Immunol., June 15, 2004; 172(12): 7642 - 7646.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
W. G. Li, D. Gavrila, X. Liu, L. Wang, S. Gunnlaugsson, L. L. Stoll, M. L. McCormick, C. D. Sigmund, C. Tang, and N. L. Weintraub
Ghrelin Inhibits Proinflammatory Responses and Nuclear Factor-{kappa}B Activation in Human Endothelial Cells
Circulation, May 11, 2004; 109(18): 2221 - 2226.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
T. Wang, B. Liu, W. Zhang, B. Wilson, and J.-S. Hong
Andrographolide Reduces Inflammation-Mediated Dopaminergic Neurodegeneration in Mesencephalic Neuron-Glia Cultures by Inhibiting Microglial Activation
J. Pharmacol. Exp. Ther., March 1, 2004; 308(3): 975 - 983.
[Abstract] [Full Text] [PDF]

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 J. Am. Coll. Nutr.Home page
Y. Zhao, S. Joshi-Barve, S. Barve, and L. H. Chen
Eicosapentaenoic Acid Prevents LPS-Induced TNF-{alpha} Expression by Preventing NF-{kappa}B Activation
J. Am. Coll. Nutr., February 1, 2004; 23(1): 71 - 78.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. Qin, Y. Liu, T. Wang, S.-J. Wei, M. L. Block, B. Wilson, B. Liu, and J.-S. Hong
NADPH Oxidase Mediates Lipopolysaccharide-induced Neurotoxicity and Proinflammatory Gene Expression in Activated Microglia
J. Biol. Chem., January 9, 2004; 279(2): 1415 - 1421.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
M. Song, J. A. Kellum, H. Kaldas, and M. P. Fink
Evidence That Glutathione Depletion Is a Mechanism Responsible for the Anti-Inflammatory Effects of Ethyl Pyruvate in Cultured Lipopolysaccharide-Stimulated RAW 264.7 Cells
J. Pharmacol. Exp. Ther., January 1, 2004; 308(1): 307 - 316.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
R. F. Schwabe, R. Bataller, and D. A. Brenner
Human hepatic stellate cells express CCR5 and RANTES to induce proliferation and migration
Am J Physiol Gastrointest Liver Physiol, November 1, 2003; 285(5): G949 - G958.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
M. M. Monick, L. S. Powers, N. S. Butler, and G. W. Hunninghake
Inhibition of Rho Family GTPases Results in Increased TNF-{alpha} Production After Lipopolysaccharide Exposure
J. Immunol., September 1, 2003; 171(5): 2625 - 2630.
[Abstract] [Full Text] [PDF]

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 JEMHome page
N. J. Horwood, T. Mahon, J. P. McDaid, J. Campbell, H. Mano, F. M. Brennan, D. Webster, and B. M.J. Foxwell
Bruton's Tyrosine Kinase Is Required For Lipopolysaccharide-induced Tumor Necrosis Factor {alpha} Production
J. Exp. Med., June 16, 2003; 197(12): 1603 - 1611.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Xiong, H. She, H. Takeuchi, B. Han, J. F. Engelhardt, C. H. Barton, E. Zandi, C. Giulivi, and H. Tsukamoto
Signaling Role of Intracellular Iron in NF-kappa B Activation
J. Biol. Chem., May 9, 2003; 278(20): 17646 - 17654.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
X.-L. Chen, Q. Zhang, R. Zhao, X. Ding, P. E. Tummala, and R. M. Medford
Rac1 and Superoxide Are Required for the Expression of Cell Adhesion Molecules Induced by Tumor Necrosis Factor-alpha in Endothelial Cells
J. Pharmacol. Exp. Ther., May 1, 2003; 305(2): 573 - 580.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
J. Zabner, P. Karp, M. Seiler, S. L. Phillips, C. J. Mitchell, M. Saavedra, M. Welsh, and A. J. Klingelhutz
Development of cystic fibrosis and noncystic fibrosis airway cell lines
Am J Physiol Lung Cell Mol Physiol, May 1, 2003; 284(5): L844 - L854.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
C. Fan, J. Yang, and J. F. Engelhardt
Temporal pattern of NF{kappa}B activation influences apoptotic cell fate in a stimuli-dependent fashion
J. Cell Sci., March 14, 2003; 115(24): 4843 - 4853.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Peng, X. Lu, M. Lei, and Q. Feng
Endothelial Nitric-oxide Synthase Enhances Lipopolysaccharide-stimulated Tumor Necrosis Factor-alpha Expression via cAMP-mediated p38 MAPK Pathway in Cardiomyocytes
J. Biol. Chem., February 28, 2003; 278(10): 8099 - 8105.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
C. Ritter, M. Andrades, J. C. F. Moreira, F. Dal-Pizzol, and S. N. A. Hussain
Superoxide production during sepsis development
Am. J. Respir. Crit. Care Med., February 1, 2003; 167(3): 474 - 475.
[Full Text] [PDF]

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 Mol. Biol. CellHome page
V. L. Vega and A. De Maio
Geldanamycin Treatment Ameliorates the Response to LPS in Murine Macrophages by Decreasing CD14 Surface Expression
Mol. Biol. Cell, February 1, 2003; 14(2): 764 - 773.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Fan, Q. Li, D. Ross, and J. F. Engelhardt
Tyrosine Phosphorylation of Ikappa Balpha Activates NFkappa B through a Redox-regulated and c-Src-dependent Mechanism Following Hypoxia/Reoxygenation
J. Biol. Chem., January 10, 2003; 278(3): 2072 - 2080.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
B. Liu and J.-S. Hong
Role of Microglia in Inflammation-Mediated Neurodegenerative Diseases: Mechanisms and Strategies for Therapeutic Intervention
J. Pharmacol. Exp. Ther., January 1, 2003; 304(1): 1 - 7.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
S. S. Deshpande, B. Qi, Y. C. Park, and K. Irani
Constitutive Activation of rac1 Results in Mitochondrial Oxidative Stress and Induces Premature Endothelial Cell Senescence
Arterioscler. Thromb. Vasc. Biol., January 1, 2003; 23(1): e1 - 6.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
H. J. Forman and M. Torres
Reactive Oxygen Species and Cell Signaling: Respiratory Burst in Macrophage Signaling
Am. J. Respir. Crit. Care Med., December 15, 2002; 166(12): S4 - 8.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. E. Marshall and J. S. Stamler
Nitrosative Stress-induced Apoptosis through Inhibition of NF-kappa B
J. Biol. Chem., September 6, 2002; 277(37): 34223 - 34228.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
Y. Liu, L. Qin, B. C. Wilson, L. An, J.-S. Hong, and B. Liu
Inhibition by Naloxone Stereoisomers of beta -Amyloid Peptide (1-42)-induced Superoxide Production in Microglia and Degeneration of Cortical and Mesencephalic Neurons
J. Pharmacol. Exp. Ther., September 1, 2002; 302(3): 1212 - 1219.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. M. Monick, P. K. Robeff, N. S. Butler, D. M. Flaherty, A. B. Carter, M. W. Peterson, and G. W. Hunninghake
Phosphatidylinositol 3-Kinase Activity Negatively Regulates Stability of Cyclooxygenase 2 mRNA
J. Biol. Chem., August 30, 2002; 277(36): 32992 - 33000.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
M. M. Monick, L. Powers, N. Butler, T. Yarovinsky, and G. W. Hunninghake
Interaction of matrix with integrin receptors is required for optimal LPS-induced MAP kinase activation
Am J Physiol Lung Cell Mol Physiol, August 1, 2002; 283(2): L390 - L402.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
T. Kizaki, K. Suzuki, Y. Hitomi, N. Taniguchi, D. Saitoh, K. Watanabe, K. Onoe, N. K. Day, R. A. Good, and H. Ohno
Uncoupling protein 2 plays an important role in nitric oxide production of lipopolysaccharide-stimulated macrophages
PNAS, July 9, 2002; 99(14): 9392 - 9397.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
R. F. Schwabe and D. A. Brenner
Role of glycogen synthase kinase-3 in TNF-alpha -induced NF-kappa B activation and apoptosis in hepatocytes
Am J Physiol Gastrointest Liver Physiol, July 1, 2002; 283(1): G204 - G211.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H.-Y. Hsu and M.-H. Wen
Lipopolysaccharide-mediated Reactive Oxygen Species and Signal Transduction in the Regulation of Interleukin-1 Gene Expression
J. Biol. Chem., June 14, 2002; 277(25): 22131 - 22139.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
A. Denys, I. A. Udalova, C. Smith, L. M. Williams, C. J. Ciesielski, J. Campbell, C. Andrews, D. Kwaitkowski, and B. M. J. Foxwell
Evidence for a Dual Mechanism for IL-10 Suppression of TNF-{alpha} Production That Does Not Involve Inhibition of p38 Mitogen-Activated Protein Kinase or NF-{kappa}B in Primary Human Macrophages
J. Immunol., May 15, 2002; 168(10): 4837 - 4845.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
K. Y. Kim, B. G. Kim, S.-O. Kim, S.-E. Yoo, Y.-G. Kwak, S.-W. Chae, and K. W. Hong
Prevention of Lipopolysaccharide-Induced Apoptosis by (2S,3S,4R)-N""-Cyano-N-(6-amino-3,4-dihydro-3-hydroxy-2-methyl-2-dimethoxymethyl-2H-benzopyran-4-yl)-N'-benzylguanidine, a Benzopyran Analog, in Endothelial Cells
J. Pharmacol. Exp. Ther., February 1, 2002; 300(2): 535 - 542.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Q. Ma and K. Kinneer
Chemoprotection by Phenolic Antioxidants. INHIBITION OF TUMOR NECROSIS FACTOR alpha INDUCTION IN MACROPHAGES
J. Biol. Chem., January 18, 2002; 277(4): 2477 - 2484.
[Abstract] [Full Text] [PDF]


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