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Originally published In Press as doi:10.1074/jbc.M111078200 on May 30, 2002

J. Biol. Chem., Vol. 277, Issue 33, 30227-30235, August 16, 2002
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Phospholipase D Activation by Sphingosine 1-Phosphate Regulates Interleukin-8 Secretion in Human Bronchial Epithelial Cells*

Rhett J. Cummings, Narasimham L. Parinandi, Ari Zaiman, Lixin Wang, Peter V. Usatyuk, Joe G. N. Garcia, and Viswanathan NatarajanDagger

From the Department of Medicine, Division of Pulmonary and Critical Care Medicine, The Johns Hopkins University, Baltimore, Maryland 21224

Sphingosine 1-phosphate (S1P), a potent bioactive sphingolipid, has been implicated in many critical cellular events, including a regulatory role in the pathogenesis of airway inflammation. We investigated the participation of S1P as an inflammatory mediator by assessing interleukin-8 (IL-8) secretion and phospholipase D (PLD) activation in human bronchial epithelial cells (Beas-2B). S1P1, S1P3, S1P4, S1P5, and weak S1P2 receptors were detected in Beas-2B and primary human bronchial epithelial cells. S1P stimulated a rapid activation of PLD, which was nearly abolished by pertussis toxin (PTX) treatment, consistent with S1P receptor/Gi protein coupling. S1P also markedly induced Beas-2B secretion of IL-8, a powerful neutrophil chemoattractant and activator, in a PTX-sensitive manner. This S1P-mediated response was dependent on transcription as indicated by a strong induction of IL-8 promoter-mediated luciferase activity in transfected Beas-2B cells and a complete inhibition by actinomycin D. Beas-2B exposure to 1-butanol, which converts the PLD-generated phosphatidic acid (PA) to phosphatidylbutanol by a transphosphatidylation reaction, significantly attenuated the S1P-induced IL-8 secretion, indicating the involvement of PLD-derived PA in the signaling pathway. Inhibition of 12-O-tetradecanoyl-phorbol-13-acetate-stimulated IL-8 production by 1-butanol further strengthened this observation. Blocking protein kinase C and Rho kinase also attenuated S1P-induced IL-8 secretion. Our data suggest that PLD-derived PA, protein kinase C, and Rho are important signaling components in S1P-mediated IL-8 secretion by human bronchial epithelial cells.

* This work was supported by National Institutes of Health Grants HL47671 and HL71152 (to V. N.).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.

Dagger To whom correspondence should be addressed: The Johns Hopkins Asthma and Allergy Center, Division of Pulmonary and Critical Care Medicine, 5501 Hopkins Bayview Circle, Baltimore, MD 21224. Tel.: 410-550-7748; Fax: 410-550-2612; E-mail: vnatara1@jhmi.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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