Home LiteratureArticle Details
PMID: 20826566 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Dexamethasone enhances ATP-induced inflammatory responses in endothelial cells.

The Journal of pharmacology and experimental therapeutics ·Vol. 335 ·No. 3 ·2010-12-00 ·Pages 693-702

Ding Y, Gao ZG, Jacobson KA, Suffredini AF

Abstract

The purinergic nucleotide ATP is released from stressed cells and is implicated in vascular inflammation. Glucocorticoids are essential to stress responses and are used therapeutically, yet little information is available that describes the effects of glucocorticoids on ATP-induced inflammation. In a human microvascular endothelial cell line, extracellular ATP-induced interleukin (IL)-6 secretion in a dose- and time-dependent manner. When cells were pretreated with dexamethasone, a prototypic glucocorticoid, ATP-induced IL-6 production was enhanced in a time- and dose-dependent manner. Mifepristone, a glucocorticoid receptor antagonist, blocked these effects. ATP-induced IL-6 release was significantly inhibited by a phospholipase C inhibitor [1-[6-[((17β)-3-methoxyestra-1,3,5[10]-trien-17-yl)amino]hexyl]-1H-pyrrole-2,5-dione (U73122)] (63.2 ± 3%, p < 0.001) and abolished by a p38 mitogen-activated protein kinase inhibitor [4-(4-fluorophenyl)-2-(4-methylsulfinylphenyl)-5-(4-pyridyl)-1H-imidazole (SB 203580)] (88 ± 1%, p < 0.001). Cells treated with dexamethasone induced mRNA expression of the purinergic P2Y(2) receptor (P2Y(2)R) 1.8- ± 0.1-fold and, when stimulated with ATP, enhanced Ca(2+) release and augmented IL-6 mRNA expression. Silencing of the P2Y(2)R by its small interfering RNA decreased ATP-induced IL-6 production by 81 ± 1% (p < 0.001). Dexamethasone enhanced the transcription rate of P2Y(2)R mRNA and induced a dose-related increase in the activity of the P2Y(2)R promoter. Furthermore, dexamethasone-enhanced ATP induction of adhesion molecule transcription and augmented the release of IL-8. Dexamethasone leads to an unanticipated enhancement of endothelial inflammatory mediator production by extracellular ATP via a P2Y(2)R-dependent mechanism. These data define a novel positive feedback loop of glucocorticoids and ATP-induced endothelial inflammation.

MeSH Terms
Adenosine Triphosphate/pharmacology Calcium Signaling/drug effects Cell Adhesion Molecules/genetics Cell Line Chemokine CCL2/metabolism Cytokines/genetics,metabolism DNA-Binding Proteins Dexamethasone/pharmacology Dose-Response Relationship, Drug Endothelial Cells/drug effects,metabolism Gene Expression/drug effects Gene Expression Profiling Humans Inflammation Mediators/metabolism Interleukin-6/genetics,metabolism Intracellular Signaling Peptides and Proteins/genetics Kinetics Lipopolysaccharides/pharmacology Mifepristone/pharmacology Nuclear Proteins/genetics Nucleotides/pharmacology Purinergic P2 Receptor Antagonists/pharmacology RNA, Small Interfering/genetics Receptors, Glucocorticoid/antagonists & inhibitors,metabolism Receptors, Purinergic P2Y2/genetics,metabolism Signal Transduction/drug effects,physiology Suramin/pharmacology Tumor Necrosis Factor alpha-Induced Protein 3 Type C Phospholipases/antagonists & inhibitors,metabolism Up-Regulation/genetics p38 Mitogen-Activated Protein Kinases/antagonists & inhibitors,metabolism
Chemicals
CCL2 protein, human Cell Adhesion Molecules Chemokine CCL2 Cytokines DNA-Binding Proteins IL6 protein, human Inflammation Mediators Interleukin-6 Intracellular Signaling Peptides and Proteins Lipopolysaccharides Nuclear Proteins Nucleotides Purinergic P2 Receptor Antagonists RNA, Small Interfering Receptors, Glucocorticoid Receptors, Purinergic P2Y2 Mifepristone Suramin Dexamethasone Adenosine Triphosphate p38 Mitogen-Activated Protein Kinases Type C Phospholipases TNFAIP3 protein, human Tumor Necrosis Factor alpha-Induced Protein 3
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ding Yi
Critical Care Medicine Department, Clinical Center and Molecular Recognition Section, Laboratory of Bioorganic Chemistry, National Institutes of Health, Bethesda, Maryland 20892-1662, USA.
Gao Zhan-Guo
Jacobson Kenneth A
Suffredini Anthony F
References (44)
44 references, click to expand
  1. Alterations in high-energy phosphates in hemorrhagic shock as related to tissue and organ function.
    Surgery. 1976 Jun;79(6):666-8 PMID: 1273752
  2. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy.
    Pharmacol Rev. 2006 Sep;58(3):281-341 PMID: 16968944
  3. The effects of steroids during sepsis depend on dose and severity of illness: an updated meta-analysis.
    Clin Microbiol Infect. 2009 Apr;15(4):308-18 PMID: 19416302
  4. Uridine nucleotide selectivity of three phospholipase C-activating P2 receptors: identification of a UDP-selective, a UTP-selective, and an ATP- and UTP-specific receptor.
    Mol Pharmacol. 1996 Aug;50(2):224-9 PMID: 8700127
  5. Glucocorticoid therapy alters hormonal and cytokine responses to endotoxin in man.
    J Immunol. 1993 Mar 1;150(5):1999-2006 PMID: 8436830
  6. Rapid inhibition of ATP-induced currents by corticosterone in rat dorsal root ganglion neurons.
    Pharmacology. 2008;82(2):164-70 PMID: 18679041
  7. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors.
    Science. 2006 Dec 15;314(5806):1792-5 PMID: 17170310
  8. Role of microvascular endothelial cells in inflammation.
    J Invest Dermatol. 1993 Jan;100(1):111S-115S PMID: 8423379
  9. Human endothelium as a source of multifunctional cytokines: molecular regulation and possible role in human disease.
    J Interferon Cytokine Res. 1999 Feb;19(2):91-104 PMID: 10090394
  10. P2 receptors in cardiovascular regulation and disease.
    Purinergic Signal. 2008 Mar;4(1):1-20 PMID: 18368530
  11. P2Y2 receptor transcription is increased by NF-kappa B and stimulates cyclooxygenase-2 expression and PGE2 released by intestinal epithelial cells.
    J Immunol. 2009 Oct 1;183(7):4521-9 PMID: 19734210
  12. Nongenomic effects of aldosterone on intracellular calcium in porcine endothelial cells.
    Am J Physiol. 1997 Apr;272(4 Pt 1):E616-20 PMID: 9142882
  13. Adenosine triphosphate is released during injurious mechanical ventilation and contributes to lung edema.
    J Trauma. 2003 Aug;55(2):290-7 PMID: 12913640
  14. Extracellular ATP signaling and P2X nucleotide receptors in monolayers of primary human vascular endothelial cells.
    Am J Physiol Cell Physiol. 2002 Feb;282(2):C289-301 PMID: 11788340
  15. ATPgammaS enhances the production of inflammatory mediators by a human dermal endothelial cell line via purinergic receptor signaling.
    J Invest Dermatol. 2006 May;126(5):1017-27 PMID: 16410784
  16. Minireview: Neuro-immuno-endocrine modulation of the hypothalamic-pituitary-adrenal (HPA) axis by gp130 signaling molecules.
    Endocrinology. 2002 May;143(5):1571-4 PMID: 11956136
  17. Endothelial injury, alarmins, and allograft rejection.
    Crit Rev Immunol. 2008;28(3):229-48 PMID: 19024347
  18. Inhibition of ATP-induced calcium influx in HT4 cells by glucocorticoids: involvement of protein kinase A.
    Acta Pharmacol Sin. 2005 Feb;26(2):199-204 PMID: 15663899
  19. A3 and P2Y2 receptors control the recruitment of neutrophils to the lungs in a mouse model of sepsis.
    Shock. 2008 Aug;30(2):173-7 PMID: 18091570
  20. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells.
    FASEB J. 2002 Jan;16(1):61-71 PMID: 11772937
  21. Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase.
    PLoS One. 2008 Jul 09;3(7):e2599 PMID: 18612415
  22. Induction of the P2z/P2X7 nucleotide receptor and associated phospholipase D activity by lipopolysaccharide and IFN-gamma in the human THP-1 monocytic cell line.
    J Immunol. 1996 Dec 15;157(12):5627-37 PMID: 8955215
  23. Glucocorticoids and cardiovascular disease.
    Eur J Endocrinol. 2007 Nov;157(5):545-59 PMID: 17984234
  24. Human plasma ATP concentration.
    Clin Chem. 2007 Feb;53(2):318-25 PMID: 17185366
  25. Association between mitochondrial dysfunction and severity and outcome of septic shock.
    Lancet. 2002 Jul 20;360(9328):219-23 PMID: 12133657
  26. A20 inhibits NF-kappaB activation by dual ubiquitin-editing functions.
    Trends Biochem Sci. 2005 Jan;30(1):1-4 PMID: 15653317
  27. Increased susceptibility of purinergic receptor-deficient mice to lung infection with Pseudomonas aeruginosa.
    Am J Physiol Lung Cell Mol Physiol. 2005 Nov;289(5):L890-5 PMID: 16024720
  28. Plasma changes in endotoxin and anaphylactic shock (ATP, ADP and Creatine phosphorus).
    Ann Clin Lab Sci. 1979 Mar-Apr;9(2):121-32 PMID: 453786
  29. Characterization of the signalling pathways involved in ATP and basic fibroblast growth factor-induced astrogliosis.
    Br J Pharmacol. 1997 Aug;121(8):1692-9 PMID: 9283705
  30. Adenosine-triphosphate in trauma-related and elective hypothermia.
    J Trauma. 1999 Oct;47(4):673-83 PMID: 10528601
  31. Tetracycline suppresses ATP gamma S-induced CXCL8 and CXCL1 production by the human dermal microvascular endothelial cell-1 (HMEC-1) cell line and primary human dermal microvascular endothelial cells.
    Exp Dermatol. 2008 Sep;17(9):752-60 PMID: 18341570
  32. Down-regulation of P2U-purinergic nucleotide receptor messenger RNA expression during in vitro differentiation of human myeloid leukocytes by phorbol esters or inflammatory activators.
    Mol Pharmacol. 1997 Jan;51(1):97-108 PMID: 9016351
  33. Extracellular ATP in the immune system: more than just a "danger signal".
    Sci Signal. 2009 Feb 03;2(56):pe6 PMID: 19193605
  34. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation.
    Pharmacol Ther. 2006 Nov;112(2):358-404 PMID: 16784779
  35. Mechanisms of endothelial dysfunction, injury, and death.
    Annu Rev Pathol. 2009;4:71-95 PMID: 18754744
  36. P2 receptors meet the immune system.
    Trends Pharmacol Sci. 2001 Jan;22(1):5-7 PMID: 11261415
  37. Epinephrine inhibits tumor necrosis factor-alpha and potentiates interleukin 10 production during human endotoxemia.
    J Clin Invest. 1996 Feb 1;97(3):713-9 PMID: 8609227
  38. Rapid non-genomic inhibition of ATP-induced Cl- secretion by dexamethasone in human bronchial epithelium.
    J Physiol. 2002 Dec 15;545(3):869-78 PMID: 12482892
  39. Modulation of nucleotide pyrophosphatase in plasmacytoma cells.
    Biochem Biophys Res Commun. 1991 Mar 15;175(2):637-44 PMID: 1850250
  40. Development of a novel transgenic rat overexpressing the P2Y(2) nucleotide receptor using a lentiviral vector.
    J Vasc Res. 2009;46(5):447-58 PMID: 19155635
  41. The caspase-1 inflammasome: a pilot of innate immune responses.
    Cell Host Microbe. 2008 Sep 11;4(3):198-208 PMID: 18779046
  42. Nucleotide receptors: an emerging family of regulatory molecules in blood cells.
    Blood. 2001 Feb 1;97(3):587-600 PMID: 11157473
  43. Transient up-regulation of P2Y2 nucleotide receptor mRNA expression is an immediate early gene response in activated thymocytes.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):831-6 PMID: 9023342
  44. Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family.
    Biochim Biophys Acta. 2003 May 20;1638(1):1-19 PMID: 12757929
Article Info
Journal
The Journal of pharmacology and experimental therapeutics
Abbr.
J Pharmacol Exp Ther
ISSN
1521-0103
Published
2010-12-00
Epub
2010-00-08
Pages
693-702
Language
English
Region
United States
NLM ID
0376362
PMCID
PMC2993554
Subset
IM
Grants
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com