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 GN Garcia, Viswanathan Natarajan

Research output: Contribution to journalArticle

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Abstract

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). S1P(1), S1P(3), S1P(4), S1P(5), and weak S1P(2) 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/G(i) 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.

Original languageEnglish (US)
Pages (from-to)30227-30235
Number of pages9
JournalJournal of Biological Chemistry
Volume277
Issue number33
StatePublished - Aug 16 2002
Externally publishedYes

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Phospholipase D
Interleukin-8
Epithelial Cells
Chemical activation
Phosphatidic Acids
Lysosphingolipid Receptors
1-Butanol
Pertussis Toxin
sphingosine 1-phosphate
rho-Associated Kinases
Sphingolipids
Chemotactic Factors
Dactinomycin
Tetradecanoylphorbol Acetate
Luciferases
Transcription
Protein Kinase C
Neutrophils

ASJC Scopus subject areas

  • Biochemistry

Cite this

Cummings, R. J., Parinandi, N. L., Zaiman, A., Wang, L., Usatyuk, P. V., Garcia, J. GN., & Natarajan, V. (2002). Phospholipase D activation by sphingosine 1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells. Journal of Biological Chemistry, 277(33), 30227-30235.

Phospholipase D activation by sphingosine 1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells. / Cummings, Rhett J.; Parinandi, Narasimham L.; Zaiman, Ari; Wang, Lixin; Usatyuk, Peter V.; Garcia, Joe GN; Natarajan, Viswanathan.

In: Journal of Biological Chemistry, Vol. 277, No. 33, 16.08.2002, p. 30227-30235.

Research output: Contribution to journalArticle

Cummings, RJ, Parinandi, NL, Zaiman, A, Wang, L, Usatyuk, PV, Garcia, JGN & Natarajan, V 2002, 'Phospholipase D activation by sphingosine 1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells.', Journal of Biological Chemistry, vol. 277, no. 33, pp. 30227-30235.
Cummings, Rhett J. ; Parinandi, Narasimham L. ; Zaiman, Ari ; Wang, Lixin ; Usatyuk, Peter V. ; Garcia, Joe GN ; Natarajan, Viswanathan. / Phospholipase D activation by sphingosine 1-phosphate regulates interleukin-8 secretion in human bronchial epithelial cells. In: Journal of Biological Chemistry. 2002 ; Vol. 277, No. 33. pp. 30227-30235.
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abstract = "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). S1P(1), S1P(3), S1P(4), S1P(5), and weak S1P(2) 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/G(i) 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.",
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