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,§,§
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*
Division of Gastrointestinal Pathology,
Department of Pathology, and
Center for Experimental Therapeutics and Reperfusion Injury, Brigham and Women’s Hospital, Harvard Medical School, and
§
The Harvard Digestive Diseases Center, Boston, MA 02115
Modeling Salmonella-epithelial cell interaction in vitro has led to the realization that epithelial cells are crucial in orchestrating neutrophil (PMN) responses, in part by stimulating basolateral release of epithelial chemokines, including IL-8. However, such basolaterally released chemokines, while likely important in orchestration of PMN movement across the subepithelial matrix, are unlikely to be responsible for the final step of transepithelial migration of PMN and entry into the apical compartment. We now show that S. typhimurium attachment to T84 cell apical epithelial membranes induces polarized apical secretion of a pathogen-elicited epithelial chemoattractant (PEEC) bioactivity. Experiments employing semipurified PEEC indicate that it is released in a polarized apical fashion and is sufficient to explain the observed final step of transepithelial migration of PMN induced by Salmonella-apical membrane interaction. By preliminary physical characterization and profiles of PMN activation, PEEC appears to be a novel PMN chemotactic bioactivity. This 1- to 3-kDa nominal molecular mass chemokine-like bioactivity directly stimulates PMN via a pertussis toxin-sensitive receptor and elicits a Ca2+ signal. While these latter features are shared by most other chemokines, analysis of PEEC-elicited PMN activation reveals that, unlike these other agonists, PEEC, even at saturating concentrations, elicits chemotactic activity in the absence of stimulation of superoxide production and/or release of primary and/or secondary granules. These data suggest that the apically released PEEC activity appears to represent a novel epithelial-derived chemoattractant that directs PMN movement across epithelial monolayers.
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C. K. Schmitt, J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien Absence of All Components of the Flagellar Export and Synthesis Machinery Differentially Alters Virulence of Salmonella enterica Serovar Typhimurium in Models of Typhoid Fever, Survival in Macrophages, Tissue Culture Invasiveness, and Calf Enterocolitis Infect. Immun., September 1, 2001; 69(9): 5619 - 5625. [Abstract] [Full Text] [PDF]
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D. L. Jaye, H. A. Edens, L. Mazzucchelli, and C. A. Parkos Novel G Protein-Coupled Responses in Leukocytes Elicited by a Chemotactic Bacteriophage Displaying a Cell Type-Selective Binding Peptide J. Immunol., June 15, 2001; 166(12): 7250 - 7259. [Abstract] [Full Text] [PDF]
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T. A. Reaves, S. P. Colgan, P. Selvaraj, M. M. Pochet, S. Walsh, A. Nusrat, T. W. Liang, J. L. Madara, and C. A. Parkos Neutrophil transepithelial migration: regulation at the apical epithelial surface by Fc-mediated events Am J Physiol Gastrointest Liver Physiol, April 1, 2001; 280(4): G746 - G754. [Abstract] [Full Text] [PDF]
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 P. Kaiser, L. Rothwell, E. E. Galyov, P. A. Barrow, J. Burnside, and P. Wigley Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum Microbiology, December 1, 2000; 146(12): 3217 - 3226. [Abstract] [Full Text] [PDF]
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T. W. Liang, R. A. DeMarco, R. J. Mrsny, A. Gurney, A. Gray, J. Hooley, H. L. Aaron, A. Huang, T. Klassen, D. B. Tumas, et al. Characterization of huJAM: evidence for involvement in cell-cell contact and tight junction regulation Am J Physiol Cell Physiol, December 1, 2000; 279(6): C1733 - C1743. [Abstract] [Full Text] [PDF]
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C. A. Lee, M. Silva, A. M. Siber, A. J. Kelly, E. Galyov, and B. A. McCormick A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration PNAS, October 24, 2000; 97(22): 12283 - 12288. [Abstract] [Full Text] [PDF]
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V. Hofman, V. Ricci, A. Galmiche, P. Brest, P. Auberger, B. Rossi, P. Boquet, and P. Hofman Effect of Helicobacter pylori on Polymorphonuclear Leukocyte Migration across Polarized T84 Epithelial Cell Monolayers: Role of Vacuolating Toxin VacA and cag Pathogenicity Island Infect. Immun., September 1, 2000; 68(9): 5225 - 5233. [Abstract] [Full Text] [PDF]
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D Haller, C Bode, W P Hammes, A M A Pfeifer, E J Schiffrin, and S Blum Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures Gut, July 1, 2000; 47(1): 79 - 87. [Abstract] [Full Text] [PDF]
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A. G. Frick, T. D. Joseph, L. Pang, A. M. Rabe, J. W. St. Geme III, and D. C. Look Haemophilus influenzae Stimulates ICAM-1 Expression on Respiratory Epithelial Cells J. Immunol., April 15, 2000; 164(8): 4185 - 4196. [Abstract] [Full Text] [PDF]
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 M.-H. Coconnier, V. Liévin, M. Lorrot, and A. L. Servin Antagonistic Activity of Lactobacillus acidophilus LB against Intracellular Salmonella enterica Serovar Typhimurium Infecting Human Enterocyte-Like Caco-2/TC-7 Cells Appl. Envir. Microbiol., March 1, 2000; 66(3): 1152 - 1157. [Abstract] [Full Text]
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S. D. Li, D. Kersulyte, I. J. D. Lindley, B. Neelam, D. E. Berg, and J. E. Crabtree Multiple Genes in the Left Half of the cag Pathogenicity Island of Helicobacter pylori Are Required for Tyrosine Kinase-Dependent Transcription of Interleukin-8 in Gastric Epithelial Cells Infect. Immun., August 1, 1999; 67(8): 3893 - 3899. [Abstract] [Full Text] [PDF]
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 K. H. Darwin and V. L. Miller Molecular Basis of the Interaction of Salmonella with the Intestinal Mucosa Clin. Microbiol. Rev., July 1, 1999; 12(3): 405 - 428. [Abstract] [Full Text] [PDF]
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A. T. Gewirtz, A. M. Siber, J. L. Madara, and B. A. McCormick Orchestration of Neutrophil Movement by Intestinal Epithelial Cells in Response to Salmonella typhimurium Can Be Uncoupled from Bacterial Internalization Infect. Immun., February 1, 1999; 67(2): 608 - 617. [Abstract] [Full Text] [PDF]
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B. A. McCormick, A. M. Siber, and A. T. Maurelli Requirement of the Shigella flexneri Virulence Plasmid in the Ability To Induce Trafficking of Neutrophils across Polarized Monolayers of the Intestinal Epithelium Infect. Immun., September 1, 1998; 66(9): 4237 - 4243. [Abstract] [Full Text] [PDF]
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