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B
Degradation, Induction of Nitric Oxide Synthase, Induction of Proinflammatory Mediators, and Cardiovascular Dysfunction1
,¶
,
*
Inotek Corporation, Beverly, MA 01915;
Critical Care Medicine,
Pulmonary Biology, and
Pulmonary Medicine, Allergy, and Clinical Immunology Division, Children’s Hospital Medical Center, Cincinnati, OH 45229; and
¶ Department of Surgery, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, NJ 01703
Gram-negative sepsis is mediated by the actions of proinflammatory
genes induced in response to microbes and their products. We report
that flagellin, the monomeric subunit of flagella, is a potent
proinflammatory species released by Salmonella.
Flagellin (1 µg/ml) induces I
B
degradation, NF-B nuclear
translocation, and inducible NO synthase expression in cultured
intestinal epithelial cells (IEC). Aflagellic Salmonella
mutants do not induce NF-B activation or NO production by cultured
IEC. Antiserum to flagellin blocks NO production in IEC induced by
medium conditioned by a variety of motile Gram-negative enteric
pathogens (Escherichia coli, Salmonella
muenchen, Serratia marcescens, Proteus
mirabilis, and Proteus vulgaris). Flagellin,
when injected systemically (
10 µg/mouse), induces systemic
inflammation characterized by the systemic expression of a range of
proinflammatory cytokines and chemokines and of inducible NO synthase.
At higher doses (300 µg/mouse), flagellin induces shock,
characterized by hypotension, reduced vascular contractility in mice,
and death. The effects of flagellin do not diminish in C3H/HeJ
LPS-resistant mice, indicating that the Toll-like receptor-4 receptor
is not involved in flagellin’s actions. In LPS-resistant mice, i.p.
injection of S. dublin flagellin or medium conditioned
by wild-type S. dublin induces serum IFN-
and
TNF-, whereas medium conditioned by aflagellic mutants has no
effect. Flagellin can be detected in the blood of rats with septic
shock induced by live bacteria at approximately 1 µg/ml. We
propose that flagellin released by Gram-negative pathogens may
contribute to the inflammatory response by an LPS- and Toll-like
receptor-4-independent pathway.
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Y. S. Lopez-Boado, M. Espinola, S. Bahr, and A. Belaaouaj Neutrophil Serine Proteinases Cleave Bacterial Flagellin, Abrogating Its Host Response-Inducing Activity J. Immunol., January 1, 2004; 172(1): 509 - 515. [Abstract] [Full Text] [PDF]
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 T. R. Hawn, A. Verbon, K. D. Lettinga, L. P. Zhao, S. S. Li, R. J. Laws, S. J. Skerrett, B. Beutler, L. Schroeder, A. Nachman, et al. A Common Dominant TLR5 Stop Codon Polymorphism Abolishes Flagellin Signaling and Is Associated with Susceptibility to Legionnaires' Disease J. Exp. Med., November 17, 2003; 198(10): 1563 - 1572. [Abstract] [Full Text] [PDF]
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J. Zhang, K. Xu, B. Ambati, and F.-S. X. Yu Toll-like Receptor 5-Mediated Corneal Epithelial Inflammatory Responses to Pseudomonas aeruginosa Flagellin Invest. Ophthalmol. Vis. Sci., October 1, 2003; 44(10): 4247 - 4254. [Abstract] [Full Text] [PDF]
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H. Zeng, A. Q. Carlson, Y. Guo, Y. Yu, L. S. Collier-Hyams, J. L. Madara, A. T. Gewirtz, and A. S. Neish Flagellin Is the Major Proinflammatory Determinant of Enteropathogenic Salmonella J. Immunol., October 1, 2003; 171(7): 3668 - 3674. [Abstract] [Full Text] [PDF]
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 G. Pinhal-Enfield, M. Ramanathan, G. Hasko, S. N. Vogel, A. L. Salzman, G.-J. Boons, and S. J. Leibovich An Angiogenic Switch in Macrophages Involving Synergy between Toll-Like Receptors 2, 4, 7, and 9 and Adenosine A2A Receptors Am. J. Pathol., August 1, 2003; 163(2): 711 - 721. [Abstract] [Full Text] [PDF]
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S. B. Mizel, A. N. Honko, M. A. Moors, P. S. Smith, and A. P. West Induction of Macrophage Nitric Oxide Production by Gram-Negative Flagellin Involves Signaling Via Heteromeric Toll-Like Receptor 5/Toll-Like Receptor 4 Complexes J. Immunol., June 15, 2003; 170(12): 6217 - 6223. [Abstract] [Full Text] [PDF]
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X. Zhou, J. A. Giron, A. G. Torres, J. A. Crawford, E. Negrete, S. N. Vogel, and J. B. Kaper Flagellin of Enteropathogenic Escherichia coli Stimulates Interleukin-8 Production in T84 Cells Infect. Immun., April 1, 2003; 71(4): 2120 - 2129. [Abstract] [Full Text]
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 J Berkes, V K Viswanathan, S D Savkovic, and G Hecht Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation Gut, March 1, 2003; 52(3): 439 - 451. [Abstract] [Full Text] [PDF]
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 J. M. C. Robertson, N. H. McKenzie, M. Duncan, E. Allen-Vercoe, M. J. Woodward, H. J. Flint, and G. Grant Lack of flagella disadvantages Salmonella enterica serovar Enteritidis during the early stages of infection in the rat J. Med. Microbiol., January 1, 2003; 52(1): 91 - 99. [Abstract] [Full Text] [PDF]
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M. E. Hobert, K. A. Sands, R. J. Mrsny, and J. L. Madara Cdc42 and Rac1 Regulate Late Events in Salmonella typhimurium-induced Interleukin-8 Secretion from Polarized Epithelial Cells J. Biol. Chem., December 20, 2002; 277(52): 51025 - 51032. [Abstract] [Full Text] [PDF]
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M. A. Donnelly and T. S. Steiner Two Nonadjacent Regions in Enteroaggregative Escherichia coli Flagellin Are Required for Activation of Toll-like Receptor 5 J. Biol. Chem., October 18, 2002; 277(43): 40456 - 40461. [Abstract] [Full Text] [PDF]
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S. J. McSorley, B. D. Ehst, Y. Yu, and A. T. Gewirtz Bacterial Flagellin Is an Effective Adjuvant for CD4+ T Cells In Vivo J. Immunol., October 1, 2002; 169(7): 3914 - 3919. [Abstract] [Full Text] [PDF]
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S. B. Mizel and J. A. Snipes Gram-negative Flagellin-induced Self-tolerance Is Associated with a Block in Interleukin-1 Receptor-associated Kinase Release from Toll-like Receptor 5 J. Biol. Chem., June 14, 2002; 277(25): 22414 - 22420. [Abstract] [Full Text] [PDF]
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J. Hellman, J. D. Roberts Jr., M. M. Tehan, J. E. Allaire, and H. S. Warren Bacterial Peptidoglycan-associated Lipoprotein Is Released into the Bloodstream in Gram-negative Sepsis and Causes Inflammation and Death in Mice J. Biol. Chem., April 12, 2002; 277(16): 14274 - 14280. [Abstract] [Full Text] [PDF]
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L. Liaudet, K. G. K. Murthy, J. G. Mabley, P. Pacher, F. G. Soriano, A. L. Salzman, and C. Szabo Comparison of Inflammation, Organ Damage, and Oxidant Stress Induced by Salmonella enterica Serovar Muenchen Flagellin and Serovar Enteritidis Lipopolysaccharide Infect. Immun., January 1, 2002; 70(1): 192 - 198. [Abstract] [Full Text] [PDF]
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 J. F. Toso, V. J. Gill, P. Hwu, F. M. Marincola, N. P. Restifo, D. J. Schwartzentruber, R. M. Sherry, S. L. Topalian, J. C. Yang, F. Stock, et al. Phase I Study of the Intravenous Administration of Attenuated Salmonella typhimurium to Patients With Metastatic Melanoma J. Clin. Oncol., January 1, 2002; 20(1): 142 - 152. [Abstract] [Full Text] [PDF]
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T. D. Eaves-Pyles, H. R. Wong, K. Odoms, and R. B. Pyles Salmonella Flagellin-Dependent Proinflammatory Responses Are Localized to the Conserved Amino and Carboxyl Regions of the Protein J. Immunol., December 15, 2001; 167(12): 7009 - 7016. [Abstract] [Full Text] [PDF]
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F. Sierro, B. Dubois, A. Coste, D. Kaiserlian, J.-P. Kraehenbuhl, and J.-C. Sirard Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells PNAS, November 20, 2001; 98(24): 13722 - 13727. [Abstract] [Full Text] [PDF]
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 S. O. Kim, K. Ono, and J. Han Apoptosis by pan-caspase inhibitors in lipopolysaccharide-activated macrophages Am J Physiol Lung Cell Mol Physiol, November 1, 2001; 281(5): L1095 - L1105. [Abstract] [Full Text] [PDF]
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Y. S. Lopez-Boado, C. L. Wilson, and W. C. Parks Regulation of Matrilysin Expression in Airway Epithelial Cells by Pseudomonas aeruginosa Flagellin J. Biol. Chem., October 26, 2001; 276(44): 41417 - 41423. [Abstract] [Full Text] [PDF]
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