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PMID: 8643498 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Elevated interleukin 6 is induced by prostaglandin E2 in a murine model of inflammation: possible role of cyclooxygenase-2.

Hinson RM, Williams JA, Shacter E

Abstract

Injection of mineral oils such as pristane into the peritoneal cavities of BALB/c mice results in a chronic peritonitis associated with high tissue levels of interleukin 6 (IL-6). Here we show that increased prostaglandin E2 (PGE2) synthesis causes induction of IL-6 and that expression of an inducible cyclooxygenase, Cox-2, may mediate this process. Levels of both PGE2 and IL-6 are elevated in inflammatory exudates from pristane-treated mice compared with lavage samples from untreated mice. The Cox-2 gene is induced in the peritoneal macrophage fraction isolated from the mice. A cause and effect relationship between increased macrophage PGE2 and IL-6 production is shown in vitro. When peritoneal macrophages are activated with an inflammatory stimulus (polymerized albumin), the Cox-2 gene is induced and secretion of PGE2 and IL-6 increases, with elevated PGE2 appearing before IL-6. Cotreatment with 1 microM indomethacin inhibits PGE2 production by the cells and reduces the induction of IL-6 mRNA but has no effect on Cox-2 mRNA, consistent with the fact that the drug inhibits catalytic activity of the cyclooxygenase but does not affect expression of the gene. Addition of exogenous PGE2 to macrophages induces IL-6 protein and mRNA synthesis, indicating that the eicosanoid stimulates IL-6 production at the level of gene expression. PGE2-stimulated IL-6 production is unaffected by addition of indomethacin. Taken together with the earlier finding that indomethacin diminishes the elevation of IL-6 in pristane-treated mice, the results show that PGE2 can induce IL-6 production in vivo and implicate expression of the Cox-2 gene in the regulation of this cytokine.

MeSH Terms
Animals Cyclooxygenase 2 Dinoprostone/biosynthesis,pharmacology Disease Models, Animal Female Gene Expression In Vitro Techniques Inflammation/enzymology,etiology,immunology Interleukin-6/biosynthesis,genetics Isoenzymes/genetics,metabolism Kinetics Macrophages, Peritoneal/immunology,metabolism Mice Mice, Inbred BALB C Peritonitis/enzymology,etiology,immunology Prostaglandin-Endoperoxide Synthases/genetics,metabolism RNA, Messenger/genetics,metabolism Terpenes/toxicity
Chemicals
Interleukin-6 Isoenzymes RNA, Messenger Terpenes pristane Cyclooxygenase 2 Prostaglandin-Endoperoxide Synthases Dinoprostone
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hinson R M
Departmment of Pediatrics, Uniformed Services University of the Health Sciences, Bethesda, MD 20814 USA.
Williams J A
Shacter E
References (58)
58 references, click to expand
  1. High circulating concentrations of interleukin-6 in active Crohn's disease but not ulcerative colitis.
    Gut. 1991 Dec;32(12):1531-4 PMID: 1773961
  2. Expression and selective inhibition of constitutive and inducible forms of cyclooxygenase.
    Adv Prostaglandin Thromboxane Leukot Res. 1995;23:125-7 PMID: 7794421
  3. Perspectives on the origins of multiple myeloma and plasmacytomas in mice.
    Hematol Oncol Clin North Am. 1992 Apr;6(2):211-23 PMID: 1582969
  4. Studies on the pathogenesis of plasma cell tumors. I. Effect of cortisol on development of plasma cell tumors.
    Cancer Res. 1966 Apr;26(4):596-9 PMID: 5934894
  5. Corticosteroids inhibit prostaglandin production by rheumatiod synovia.
    Nature. 1975 Dec 25;258(5537):737-9 PMID: 1207758
  6. The requirement of an adherent cell substratum for the growth of developing plasmacytoma cells in vivo.
    J Exp Med. 1976 Dec 1;144(6):1554-67 PMID: 1003103
  7. Genetics of susceptibility to pristane-induced plasmacytomas in BALB/cAn: reduced susceptibility in BALB/cJ with a brief description of pristane-induced arthritis.
    J Immunol. 1981 Oct;127(4):1591-5 PMID: 7276572
  8. A radioimmunoassay for the unstable pulmonary metabolites of prostaglandin E1 and E2: an indirect index of their in vivo disposition and pharmacokinetics.
    J Pharmacol Exp Ther. 1982 Feb;220(2):229-35 PMID: 6948952
  9. Rapid extraction of arachidonic acid metabolites from biological samples using octadecylsilyl silica.
    Methods Enzymol. 1982;86:467-77 PMID: 6290844
  10. Indomethacin inhibition of glutathione S-transferases.
    Biochem Biophys Res Commun. 1983 May 16;112(3):980-5 PMID: 6847692
  11. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays.
    J Immunol Methods. 1983 Dec 16;65(1-2):55-63 PMID: 6606682
  12. Inhibition of plasmacytoma development in BALB/c mice by indomethacin.
    J Exp Med. 1985 May 1;161(5):996-1012 PMID: 3989472
  13. Modes of action of aspirin-like drugs.
    Proc Natl Acad Sci U S A. 1985 Nov;82(21):7227-31 PMID: 2997778
  14. A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro.
    Science. 1986 Aug 1;233(4763):566-9 PMID: 3726549
  15. Serum-free medium for growth factor-dependent and -independent plasmacytomas and hybridomas.
    J Immunol Methods. 1987 May 20;99(2):259-70 PMID: 3584996
  16. Elevated levels of the 26K human hybridoma growth factor (interleukin 6) in cerebrospinal fluid of patients with acute infection of the central nervous system.
    Clin Exp Immunol. 1988 Feb;71(2):320-3 PMID: 3349651
  17. Synthesis of interleukin 6 (interferon-beta 2/B cell stimulatory factor 2) in human fibroblasts is triggered by an increase in intracellular cyclic AMP.
    J Biol Chem. 1988 May 5;263(13):6177-82 PMID: 2452159
  18. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides.
    Arthritis Rheum. 1988 Jun;31(6):784-8 PMID: 3260102
  19. Molecular regulation of B lymphocyte response.
    Annu Rev Immunol. 1988;6:485-512 PMID: 3289574
  20. Activated neutrophils induce prolonged DNA damage in neighboring cells.
    Carcinogenesis. 1988 Dec;9(12):2297-304 PMID: 2847879
  21. Functional discrimination between interleukin 6 and interleukin 1.
    Eur J Immunol. 1988 Oct;18(10):1535-40 PMID: 3263920
  22. Inhibition by cyclo-oxygenase inhibitors of interleukin-6 production by human peripheral blood mononuclear cells.
    Int J Immunopharmacol. 1991;13(8):1137-46 PMID: 1814850
  23. Excessive production of interleukin 6/B cell stimulatory factor-2 in rheumatoid arthritis.
    Eur J Immunol. 1988 Nov;18(11):1797-801 PMID: 2462501
  24. The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome.
    J Exp Med. 1989 Jan 1;169(1):333-8 PMID: 2783334
  25. Endotoxemia elicits increased circulating beta 2-IFN/IL-6 in man.
    J Immunol. 1989 Apr 1;142(7):2321-4 PMID: 2784459
  26. Identification of a cyclooxygenase-related gene and its potential role in prostaglandin formation.
    Biochem Biophys Res Commun. 1989 Nov 15;164(3):1358-65 PMID: 2480117
  27. Serum levels of interleukin 6, a potent myeloma cell growth factor, as a reflect of disease severity in plasma cell dyscrasias.
    J Clin Invest. 1989 Dec;84(6):2008-11 PMID: 2592570
  28. Independent induction of interleukin 6 and prostaglandin E2 by interleukin 1 in human articular chondrocytes.
    Biochem Biophys Res Commun. 1990 Feb 14;166(3):1163-70 PMID: 2407240
  29. Interleukin-6: an overview.
    Annu Rev Immunol. 1990;8:253-78 PMID: 2188664
  30. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF).
    FASEB J. 1990 Aug;4(11):2860-7 PMID: 2199284
  31. LPS-stimulated bovine aortic endothelial cells produce IL-1 and IL-6 like activities.
    Agents Actions. 1990 Jun;30(3-4):403-11 PMID: 2386111
  32. Mouse plasmacytoma growth in vivo: enhancement by interleukin 6 (IL-6) and inhibition by antibodies directed against IL-6 or its receptor.
    J Exp Med. 1990 Sep 1;172(3):997-1000 PMID: 2388041
  33. Pathophysiology of cytokines.
    Leuk Res. 1990;14(8):675-7 PMID: 2201818
  34. The induction and suppression of prostaglandin H2 synthase (cyclooxygenase) in human monocytes.
    J Biol Chem. 1990 Oct 5;265(28):16737-40 PMID: 2120205
  35. Interleukin 6 in infection and cancer.
    Proc Soc Exp Biol Med. 1990 Nov;195(2):183-91 PMID: 2236101
  36. Experimental endotoxemia in humans: analysis of cytokine release and coagulation, fibrinolytic, and complement pathways.
    Blood. 1990 Dec 15;76(12):2520-6 PMID: 2124934
  37. Inhibition of the myeloperoxidase-H2O2-Cl- system of neutrophils by indomethacin and other non-steroidal anti-inflammatory drugs.
    Biochem Pharmacol. 1991 Mar 15-Apr 1;41(6-7):975-84 PMID: 1848981
  38. Monocyte zinc and in vitro prostaglandin E2 and interleukin-1 beta production by cultured peripheral blood monocytes in patients with Crohn's disease.
    Dig Dis Sci. 1991 May;36(5):627-33 PMID: 2022165
  39. Interleukin-6 is the central tumor growth factor in vitro and in vivo in multiple myeloma.
    Eur Cytokine Netw. 1990 Oct-Nov;1(4):193-201 PMID: 2104241
  40. Interleukin-6 and its relation to inflammation and disease.
    Clin Immunol Immunopathol. 1992 Jan;62(1 Pt 2):S60-5 PMID: 1728989
  41. In vivo cyclooxygenase expression in synovial tissues of patients with rheumatoid arthritis and osteoarthritis and rats with adjuvant and streptococcal cell wall arthritis.
    J Clin Invest. 1992 Jan;89(1):97-108 PMID: 1729286
  42. Elevation of interleukin-6 in response to a chronic inflammatory stimulus in mice: inhibition by indomethacin.
    Blood. 1992 Jul 1;80(1):194-202 PMID: 1611085
  43. Human cyclooxygenase-2 cDNA.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7384-8 PMID: 1380156
  44. Selective expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide.
    J Biol Chem. 1992 Dec 25;267(36):25934-8 PMID: 1464605
  45. Modulation of tumor necrosis factor-alpha, interleukin-1 beta, interleukin-6, interleukin-8, and granulocyte/macrophage colony-stimulating factor expression in human monocytes by an endogenous anxiogenic benzodiazepine ligand, triakontatetraneuropeptide: evidence for a role of prostaglandins.
    Mol Pharmacol. 1993 Jan;43(1):64-9 PMID: 8380885
  46. Differential inhibition of prostaglandin endoperoxide synthase (cyclooxygenase) isozymes by aspirin and other non-steroidal anti-inflammatory drugs.
    J Biol Chem. 1993 Mar 25;268(9):6610-4 PMID: 8454631
  47. Prostaglandin E2 downregulates Kupffer cell production of IL-1 and IL-6 during hepatic regeneration.
    Am J Physiol. 1993 Apr;264(4 Pt 1):G601-8 PMID: 8476047
  48. Interleukin-6 in biology and medicine.
    Adv Immunol. 1993;54:1-78 PMID: 8379461
  49. Stimulation of interleukin-6 and prostaglandin E2 secretion from peritoneal macrophages by polymers of albumin.
    Blood. 1993 Nov 1;82(9):2853-64 PMID: 8219233
  50. Cyclooxygenase-1 and -2 expression in rheumatoid synovial tissues. Effects of interleukin-1 beta, phorbol ester, and corticosteroids.
    J Clin Invest. 1994 Mar;93(3):1095-101 PMID: 8132748
  51. NS-398, a new anti-inflammatory agent, selectively inhibits prostaglandin G/H synthase/cyclooxygenase (COX-2) activity in vitro.
    Prostaglandins. 1994 Jan;47(1):55-9 PMID: 8140262
  52. Selective inhibition of inducible cyclooxygenase 2 in vivo is antiinflammatory and nonulcerogenic.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3228-32 PMID: 8159730
  53. Production of tumor necrosis factor, interleukin-6 and prostaglandin E2 by LPS-stimulated rat bone marrow macrophages after thermal injury: effect of indomethacin.
    Inflammation. 1994 Apr;18(2):175-85 PMID: 8070901
  54. Evidence for the involvement of interleukin 10 in the differential deactivation of murine peritoneal macrophages by prostaglandin E2.
    J Exp Med. 1994 Dec 1;180(6):2365-70 PMID: 7525853
  55. Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12013-7 PMID: 7991575
  56. Interactions between cytokines and eicosanoids: a study using human peritoneal macrophages.
    Immunol Lett. 1994 Jul;41(2-3):255-60 PMID: 8002047
  57. Prostanoid enhancement of interleukin-6 production by rat peritoneal mast cells.
    J Immunol. 1995 May 1;154(9):4759-67 PMID: 7536779
  58. A collection of mRNA species that are inducible in the RAW 264.7 mouse macrophage cell line by gamma interferon and other agents.
    Mol Cell Biol. 1992 Apr;12(4):1535-45 PMID: 1372386
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1996-05-14
Pages
4885-90
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC39374
Subset
IM
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