Phospholipase D Activation by Sphingosine 1-Phosphate Regulates Interleukin-8 Secretion in Human Bronchial Epithelial Cells*

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.

[1]  T. Palmer,et al.  Dual Regulation of EDG1/S1P1 Receptor Phosphorylation and Internalization by Protein Kinase C and G-protein-coupled Receptor Kinase 2* , 2002, The Journal of Biological Chemistry.

[2]  J. Exton Regulation of phospholipase D. , 1999, FEBS letters.

[3]  T. Hla,et al.  Lysophospholipids--Receptor Revelations , 2001, Science.

[4]  D. Im,et al.  Characterization of the human and mouse sphingosine 1-phosphate receptor, S1P5 (Edg-8): structure-activity relationship of sphingosine1-phosphate receptors. , 2001, Biochemistry.

[5]  B. Friedman,et al.  Selective Loss of Sphingosine 1-Phosphate Signaling with No Obvious Phenotypic Abnormality in Mice Lacking Its G Protein-coupled Receptor, LPB3/EDG-3* , 2001, The Journal of Biological Chemistry.

[6]  I. Komuro,et al.  Dual regulation of sphingosine 1-phosphate-induced phospholipase D activity through RhoA and protein kinase C-alpha in C2C12 myoblasts. , 2001, Cellular signalling.

[7]  J. Metcalf,et al.  Adenovirus Type 7 Induces Interleukin-8 Production via Activation of Extracellular Regulated Kinase 1/2 , 2001, Journal of Virology.

[8]  S. Roper,et al.  An essential role for the H218/AGR16/Edg‐5/LPB2 sphingosine 1‐phosphate receptor in neuronal excitability , 2001, The European journal of neuroscience.

[9]  A. Verin,et al.  Differential Regulation of Sphingosine-1-phosphate-and Vegf-induced Endothelial Cell Chemotaxis Involvement of G I ␣ 2 -linked Rho Kinase Activity We Compared Stimulus-coupling Pathways Involved in Bovine Pulmonary Artery (pa) and Lung Microvascular Endothelial Cell Migration Evoked by Sphingosine-1 , 2022 .

[10]  Yan Xu,et al.  Lysophospholipids increase interleukin-8 expression in ovarian cancer cells. , 2001, Gynecologic oncology.

[11]  S. Spiegel,et al.  Sphingosine 1‐phosphate modulates human airway smooth muscle cell functions that promote inflammation and airway remodeling in asthma , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[12]  K. Jakobs,et al.  Stimulation of intracellular sphingosine-1-phosphate production by G-protein-coupled sphingosine-1-phosphate receptors. , 2001, European journal of pharmacology.

[13]  Sylvia Wong,et al.  Nrg-1 Belongs to the Endothelial Differentiation Gene Family of G Protein-coupled Sphingosine-1-phosphate Receptors* , 2001, The Journal of Biological Chemistry.

[14]  O. Volpert,et al.  Sphingosine 1‐phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  J. Jaffrezou,et al.  Phosphatidylcholine-specific phospholipase C and phospholipase D are respectively implicated in mitogen-activated protein kinase and nuclear factor kappaB activation in tumour-necrosis-factor-alpha-treated immature acute-myeloid-leukaemia cells. , 2000, The Biochemical journal.

[16]  J. P. Hobson,et al.  Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. , 2000, The Journal of clinical investigation.

[17]  S. Pyne,et al.  Sphingosine 1-phosphate signalling in mammalian cells , 2000 .

[18]  K. Racké,et al.  Potential role of EDG receptors and lysophospholipids as their endogenous ligands in the respiratory tract. , 2000, Pulmonary pharmacology & therapeutics.

[19]  N. Suttorp,et al.  Rho proteins and the p38-MAPK pathway are important mediators for LPS-induced interleukin-8 expression in human endothelial cells. , 2000, Blood.

[20]  J. P. Hobson,et al.  Sphingosine-1-phosphate is a ligand for the G protein-coupled receptor EDG-6. , 2000, Blood.

[21]  S. Milstien,et al.  Functions of a new family of sphingosine-1-phosphate receptors. , 2000, Biochimica et biophysica acta.

[22]  C. H. Liu,et al.  Sphingosine‐1‐Phosphate Signaling via the EDG‐1 Family of G‐Protein‐Coupled Receptors , 2000, Annals of the New York Academy of Sciences.

[23]  R. Strieter,et al.  Chemokine signaling in inflammation , 2000, Critical care medicine.

[24]  S. Spiegel,et al.  Sphingosine-1-phosphate activates phospholipase D in human airway epithelial cells via a G protein-coupled receptor. , 2000, Archives of biochemistry and biophysics.

[25]  G. Fiucci,et al.  Phospholipase D: molecular and cell biology of a novel gene family. , 2000, The Biochemical journal.

[26]  T. Bleu,et al.  Sphingosine 1-Phosphate-induced Cell Proliferation, Survival, and Related Signaling Events Mediated by G Protein-coupled Receptors Edg3 and Edg5* , 2000, The Journal of Biological Chemistry.

[27]  T. Horie,et al.  Diesel exhaust particles activate p38 MAP kinase to produce interleukin 8 and RANTES by human bronchial epithelial cells and N-acetylcysteine attenuates p38 MAP kinase activation. , 2000, American journal of respiratory and critical care medicine.

[28]  J. Gamble,et al.  Activation of Sphingosine Kinase by Tumor Necrosis Factor-α Inhibits Apoptosis in Human Endothelial Cells* , 1999, The Journal of Biological Chemistry.

[29]  A. Barr,et al.  Differential Coupling of the Sphingosine 1-Phosphate Receptors Edg-1, Edg-3, and H218/Edg-5 to the Gi, Gq, and G12 Families of Heterotrimeric G Proteins* , 1999, The Journal of Biological Chemistry.

[30]  M. Frohman,et al.  Mammalian phospholipase D structure and regulation. , 1999, Biochimica et biophysica acta.

[31]  C. H. Liu,et al.  Sphingosine-1-phosphate: extracellular mediator or intracellular second messenger? , 1999, Biochemical pharmacology.

[32]  J. Moss,et al.  Effect of Rho and ADP-ribosylation Factor GTPases on Phospholipase D Activity in Intact Human Adenocarcinoma A549 Cells* , 1999, The Journal of Biological Chemistry.

[33]  M. Schroth,et al.  Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. , 1999, American journal of respiratory cell and molecular biology.

[34]  T. Out,et al.  Influx of Neutrophils into the Airway Lumen at 4 h after Segmental Allergen Challenge in Asthma , 1999, International Archives of Allergy and Immunology.

[35]  P. Casellas,et al.  Stimulation of peripheral cannabinoid receptor CB2 induces MCP‐1 and IL‐8 gene expression in human promyelocytic cell line HL60 , 1999, FEBS letters.

[36]  C. H. Liu,et al.  Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. , 1999, Molecular biology of the cell.

[37]  J. Nick,et al.  Selective activation and functional significance of p38alpha mitogen-activated protein kinase in lipopolysaccharide-stimulated neutrophils. , 1999, The Journal of clinical investigation.

[38]  T. Horie,et al.  Hyperosmolarity-induced interleukin-8 expression in human bronchial epithelial cells through p38 mitogen-activated protein kinase. , 1999, American journal of respiratory and critical care medicine.

[39]  J. Exton,et al.  Phospholipase D Mediates Matrix Metalloproteinase-9 Secretion in Phorbol Ester-stimulated Human Fibrosarcoma Cells* , 1999, The Journal of Biological Chemistry.

[40]  T. Wyatt,et al.  Protein kinase C activation is required for cigarette smoke-enhanced C5a-mediated release of interleukin-8 in human bronchial epithelial cells. , 1999, American journal of respiratory cell and molecular biology.

[41]  Lung-Chi Chen,et al.  Induction of interleukin‐8 by ozone is mediated by tyrosine kinase and protein kinase A, but not by protein kinase C , 1998, Journal of cellular physiology.

[42]  M. Lipp,et al.  EDG6, a novel G-protein-coupled receptor related to receptors for bioactive lysophospholipids, is specifically expressed in lymphoid tissue. , 1998, Genomics.

[43]  A. Gilman,et al.  p115 RhoGEF, a GTPase activating protein for Gα12 and Gα13 , 1998 .

[44]  C. H. Liu,et al.  Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. , 1998, Science.

[45]  R. Garofalo,et al.  A promoter recruitment mechanism for tumor necrosis factor-alpha-induced interleukin-8 transcription in type II pulmonary epithelial cells. Dependence on nuclear abundance of Rel A, NF-kappaB1, and c-Rel transcription factors. , 1998, The Journal of biological chemistry.

[46]  Y. Igarashi,et al.  Sphingosine 1-phosphate is a blood constituent released from activated platelets, possibly playing a variety of physiological and pathophysiological roles. , 1998, Acta biochimica Polonica.

[47]  O. Kozawa,et al.  Activation of mitogen‐activated protein kinase is involved in sphingosine 1‐phosphate‐stimulated interleukin‐6 synthesis in osteoblasts , 1997, FEBS letters.

[48]  M. Frohman,et al.  Measurement of phospholipase D activity. , 1997, Analytical biochemistry.

[49]  O. Kozawa,et al.  Thrombin regulates interleukin-6 synthesis through phosphatidylcholine hydrolysis by phospholipase D in osteoblasts. , 1997, Archives of biochemistry and biophysics.

[50]  Y. Igarashi,et al.  Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. , 1997, Journal of biochemistry.

[51]  S. Hammond,et al.  Characterization of Two Alternately Spliced Forms of Phospholipase D1 , 1997, The Journal of Biological Chemistry.

[52]  R. Strieter,et al.  Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome. , 1996, American journal of respiratory and critical care medicine.

[53]  H. Simon,et al.  Platelet-activating factor exerts mitogenic activity and stimulates expression of interleukin 6 and interleukin 8 in human lung fibroblasts via binding to its functional receptor , 1996, The Journal of experimental medicine.

[54]  P. Barnes,et al.  Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. , 1996, American journal of respiratory and critical care medicine.

[55]  A. Gomez-Muñoz,et al.  Interaction of Ceramides, Sphingosine, and Sphingosine 1-Phosphate in Regulating DNA Synthesis and Phospholipase D Activity (*) , 1995, The Journal of Biological Chemistry.

[56]  S. Spiegel,et al.  Sphingosine 1-phosphate rapidly activates the mitogen-activated protein kinase pathway by a G protein-dependent mechanism , 1995, The Journal of Biological Chemistry.

[57]  L. del Peso,et al.  Generation of phosphorylcholine as an essential event in the activation of Raf‐1 and MAP‐kinases in growth factors‐induced mitogenic stimulation , 1995, Journal of cellular biochemistry.

[58]  A. Kazlauskas,et al.  Activation of phospholipase C-gamma is necessary for stimulation of phospholipase D by platelet-derived growth factor. , 1994, The Journal of biological chemistry.

[59]  F. Mollinedo,et al.  Involvement of phospholipase D in the activation of transcription factor AP-1 in human T lymphoid Jurkat cells. , 1994, Journal of immunology.

[60]  V. Natarajan,et al.  Activation of endothelial cell phospholipase D by sphingosine and sphingosine-1-phosphate. , 1994, American journal of respiratory cell and molecular biology.

[61]  F. Meloni,et al.  Elevated IL-8 and MCP-1 in the bronchoalveolar lavage fluid of patients with idiopathic pulmonary fibrosis and pulmonary sarcoidosis. , 1994, American journal of respiratory and critical care medicine.

[62]  V. Natarajan,et al.  Agonist-induced activation of phospholipase D in bovine pulmonary artery endothelial cells: regulation by protein kinase C and calcium. , 1993, The Journal of laboratory and clinical medicine.

[63]  S. Spiegel,et al.  Sphingosine-1-phosphate, a metabolite of sphingosine, increases phosphatidic acid levels by phospholipase D activation. , 1992, The Journal of biological chemistry.

[64]  M. Baggiolini,et al.  Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. , 1989, The Journal of clinical investigation.