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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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K. G. K. Murthy, A. Deb, S. Goonesekera, C. Szabo, and A. L. Salzman Identification of Conserved Domains in Salmonella muenchen Flagellin That Are Essential for Its Ability to Activate TLR5 and to Induce an Inflammatory Response in Vitro J. Biol. Chem., February 13, 2004; 279(7): 5667 - 5675. [Abstract] [Full Text] [PDF]
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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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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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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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K. A. Reed, M. E. Hobert, C. E. Kolenda, K. A. Sands, M. Rathman, M. O'Connor, S. Lyons, A. T. Gewirtz, P. J. Sansonetti, and J. L. Madara The Salmonella typhimurium Flagellar Basal Body Protein FliE Is Required for Flagellin Production and to Induce a Proinflammatory Response in Epithelial Cells J. Biol. Chem., April 5, 2002; 277(15): 13346 - 13353. [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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