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Originally published In Press as doi:10.1074/jbc.M007703200 on March 8, 2001

J. Biol. Chem., Vol. 276, Issue 22, 19267-19275, June 1, 2001
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Cystic Fibrosis Pathogens Activate Ca2+-dependent Mitogen-activated Protein Kinase Signaling Pathways in Airway Epithelial Cells*

Adam J. Ratner, Ruth Bryan, Adam Weber, Stephen Nguyen, Derrick Barnes, Allyson Pitt, Shari Gelber, Ambrose CheungDagger , and Alice Prince§

From the College of Physicians & Surgeons, Columbia University, New York, New York 10032 and the Dagger  Department of Microbiology, Dartmouth Medical School, Hanover, New Hampshire 03755

Much of the pulmonary disease in cystic fibrosis is associated with polymorphonuclear leukocyte-dominated airway inflammation caused by bacterial infection. Respiratory epithelial cells express the polymorphonuclear chemokine interleukin-8 (IL-8) in response to ligation of asialylated glycolipid receptors, which are increased on damaged or regenerating cells and those with cystic fibrosis transmembrane conductance regulator mutations. Because both Pseudomonas aeruginosa and Staphylococcus aureus, the most common pathogens in cystic fibrosis, bind asialylated glycolipid receptors such as asialoGM1, we postulated that diverse bacteria can activate a common epithelial signaling pathway to elicit IL-8 expression. P. aeruginosa PAO1 but not pil mutants and S. aureus RN6390 but not the agr mutant RN6911 stimulated increases in [Ca2+]i in 1HAEo- airway epithelial cells. This response stimulated p38 and ERK1/2 mitogen-activated protein kinase (MAPK) signaling cascades resulting in NF-kappa B activation and IL-8 expression. Ligation of the asialoGM1 receptor or thapsigargin-elicited Ca2+ release activated this pathway, whereas P. aeruginosa lipopolysaccharide did not. The rapid kinetics of epithelial activation precluded bacterial invasion of the epithelium. Recognition of asialylated glycolipid receptors on airway epithelial cells provides a common pathway for Gram-positive and Gram-negative organisms to initiate an epithelial inflammatory response.

* This work was supported by National Institutes of Health Grants HL56194 and HL60293 and Cystic Fibrosis Foundation grants (to A. P. and A. J. R.) and by an American Academy of Pediatrics Resident research grant (to A. J. R.).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 correspondence should be addressed: Depts. of Pediatrics and Pharmacology, Columbia University, 650 W. 168th St., New York, NY 10032. Tel.: 212-305-4192; Fax: 212-305-2284; E-mail: asp7@columbia.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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