Activation of macrophage peroxisome proliferator-activated receptor-γ by diclofenac results in the induction of cyclooxygenase-2 protein and the synthesis of anti-inflammatory cytokines

Molecular and Cellular Biochemistry

Volumn 327, Issue 1-2, 2009, Pages 101-110

  Ayoub, Samir S ^a   Botting, Regina M ^a   Joshi, Amrish N ^a   Seed, Michael P ^a   Colville Nash, Paul R ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Cyclooxygenase 2; Diclofenac; J774.2; Lipopolysaccharide; Paracetamol; Peroxisome proliferator activated receptor

Indexed keywords

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CYCLOOXYGENASE 2; CYTOKINES; DICLOFENAC; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED BALB C; PPAR GAMMA; RATS; RATS, WISTAR; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS);

EID: 67349116019     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-009-0048-y     Document Type: Article

References (50)

1. Xie WL, Chipman JG, Robertson DL, Erikson RL, Simmons DL (1991) Expression of a mitogen-responsive gene encoding prostaglandin synthase is regulated by mRNA splicing. Proc Natl Acad Sci USA 88:2692-2696. doi: 10.1073/pnas.88.7.2692
2. Tomlinson A, Appleton I, Moore AR, Gilroy DW, Willis D, Mitchell JA, Willoughby DA (1994) Cyclo-oxygenase and nitric oxide synthase isoforms in rat carrageenin-induced pleurisy. Br J Pharmacol 113:693-698
3. Jones DA, Carlton DP, McIntyre TM, Zimmerman GA, Prescott SM (1993) Molecular cloning of human prostaglandin endoperoxide synthase type II and demonstration of expression in response to cytokines. J Biol Chem 268:9049-9054
4. Hamasaki Y, Kitzler J, Hardman R, Nettesheim P, Eling TE (1993) Phorbol ester and epidermal growth factor enhance the expression of two inducible prostaglandin H synthase genes in rat tracheal epithelial cells. Arch Biochem Biophys 304:226-234. doi: 10.1006/abbi.1993.1343
5. O'Sullivan MG, Chilton FH, Huggins EM Jr, McCall CE (1992) Lipopolysaccharide priming of alveolar macrophages for enhanced synthesis of prostanoids involves induction of a novel prostaglandin H synthase. J Biol Chem 267:14547-14550
6. Simon LS, Weaver AL, Graham DY, Kivitz AJ, Lipsky PE, Hubbard RC, Isakson PC, Verburg KM, Yu SS, Zhao WW, Geis GS (1999) Anti-inflammatory and upper gastrointestinal effects of celecoxib in rheumatoid arthritis: a randomized controlled trial. JAMA 282:1921-1928. doi: 10.1001/ jama.282.20.1921
7. Johnson M, Seaton T (2003) Comparing celecoxib with traditional nonsteroidal anti-inflammatory drugs. J Fam Pract 52:96-98
8. Higgs EA, Moncada S, Vane JR (1978) Inflammatory effects of prostacyclin (PGI2) and 6-oxo-PGF1alpha in the rat paw. Prostaglandins 16:153-162. doi: 10.1016/0090-6980(78)90018-7
9. Zhang Y, DeWitt DL, McNeely TB, Wahl SM, Wahl LM (1997) Secretory leukocyte protease inhibitor suppresses the production of monocyte prostaglandin H synthase-2, prostaglandin E2, and matrix metalloproteinases. J Clin Invest 99:894-900. doi: 10.1172/JCI119254
10. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA (1999) Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 5:698-701. doi: 10.1038/9550
11. Ledwith BJ, Pauley CJ, Wagner LK, Rokos CL, Alberts DW, Manam S (1997) Induction of cyclooxygenase-2 expression by peroxisome proliferators and non-tetradecanoylphorbol 12, 13-myristate-type tumor promoters in immortalized mouse liver cells. J Biol Chem 272:3707-3714. doi: 10.1074/ jbc.272.6.3707
12. Callejas NA, Castrillo A, Bosca L, Martin-Sanz P (1999) Inhibition of prostaglandin synthesis up-regulates cyclooxygenase-2 induced by lipopolysaccharide and peroxisomal proliferators. J Pharmacol Exp Ther 288:1235-1241
13. Pontsler AV, St Hilaire A, Marathe GK, Zimmerman GA, McIntyre TM (2002) Cyclooxygenase-2 is induced in monocytes by peroxisome proliferator activated receptor gamma and oxidized alkyl phospholipids from oxidized low density lipoprotein. J Biol Chem 277:13029-13036. doi: 10.1074/ jbc.M109546200
14. Green S (1995) PPAR: A mediator of peroxisome proliferator action. Mutat Res 333:101-109. doi: 10.1016/0027-5107(95)00136-0
15. Keller H, Dreyer C, Medin J, Mahfoudi A, Ozato K, Wahli W (1993) Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. Proc Natl Acad Sci USA 90:2160-2164. doi: 10.1073/ pnas.90.6.2160
16. Simmons DL, Botting RM, Robertson PM, Madsen ML, Vane JR (1999) Induction of an acetaminophen-sensitive cyclooxygenase with reduced sensitivity to nonsteroid antiinflammatory drugs. Proc Natl Acad Sci USA 96:3275-3280. doi: 10.1073/pnas.96.6.3275
17. Ralph P, Nakoinz I (1977) Antibody-dependent killing of erythrocyte and tumor targets by macrophage-related cell lines: Enhancement by PPD and LPS. J Immunol 119:950-954
18. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. doi: 10.1016/0003-2697(76)90527-3
19. Wright HM, Clish CB, Mikami T, Hauser S, Yanagi K, Hiramatsu R, Serhan CN, Spiegelman BM (2000) A synthetic antagonist for the peroxisome proliferator-activated receptor gamma inhibits adipocyte differentiation. J Biol Chem 275:1873-1877. doi: 10.1074/jbc.275.3.1873
20. Bendixen AC, Shevde NK, Dienger KM, Willson TM, Funk CD, Pike JW (2001) IL-4 inhibits osteoclast formation through a direct action on osteoclast precursors via peroxisome proliferator-activated receptor gamma 1. Proc Natl Acad Sci USA 98:2443-2448. doi: 10.1073/pnas.041493198
21. Forman BM, Tontonoz P, Chen J, Brun RP, Spiegelman BM, Evans RM (1995) 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 83:803-812. doi: 10.1016/ 0092-8674(95)90193-0
22. Blackwell NM, Sembi P, Newson JS, Lawrence T, Gilroy DW, Kabouridis PS (2004) Reduced infiltration and increased apoptosis of leukocytes at sites of inflammation by systemic administration of a membrane-permeable IkappaBalpha repressor. Arthritis Rheum 50:2675-2684. doi: 10.1002/ art.20467
23. Foxworthy PS, Perry DN, Eacho PI (1993) Induction of peroxisomal beta-oxidation by nonsteroidal anti-inflammatory drugs. Toxicol Appl Pharmacol 118:271-274. doi: 10.1006/taap.1993.1033
24. Rekka E, Ayalogu EO, Lewis DF, Gibson GG, Ioannides C (1994) Induction of hepatic microsomal CYP4A activity and of peroxisomal beta-oxidation by two non-steroidal anti-inflammatory drugs. Arch Toxicol 68:73-78. doi: 10.1007/s002040050037
25. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM, Kliewer SA (1997) Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 272:3406-3410. doi: 10.1074/jbc.272.6.3406
26. Paik JH, Ju JH, Lee JY, Boudreau MD, Hwang DH (2000) Two opposing effects of non-steroidal anti-inflammatory drugs on the expression of the inducible cyclooxygenase. Mediation through different signaling pathways. J Biol Chem 275:28173-28179
27. Adamson DJ, Frew D, Tatoud R, Wolf CR, Palmer CN (2002) Diclofenac antagonizes peroxisome proliferator-activated receptor-gamma signaling. Mol Pharmacol 61:7-12. doi: 10.1124/mol.61.1.7
28. Chinetti G, Griglio S, Antonucci M, Torra IP, Delerive P, Majd Z, Fruchart JC, Chapman J, Najib J, Staels B (1998) Activation of proliferator-activated receptors alpha and gamma induces apoptosis of human monocyte-derived macrophages. J Biol Chem 273:25573-25580. doi: 10.1074/jbc.273.40.25573
29. Elstner E, Muller C, Koshizuka K, Williamson EA, Park D, Asou H, Shintaku P, Said JW, Heber D, Koeffler HP (1998) Ligands for peroxisome proliferator-activated receptor gamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc Natl Acad Sci USA 95:8806-8811. doi: 10.1073/ pnas.95.15.8806
30. Bishop-Bailey D, Hla T (1999) Endothelial cell apoptosis induced by the peroxisome proliferator-activated receptor (PPAR) ligand 15-deoxy-Delta12, 14-prostaglandin J2. J Biol Chem 274:17042-17048. doi: 10.1074/jbc.274.24.17042
31. Small RE (1989) Diclofenac sodium. Clin Pharm 8:545-558
32. Hinz B, Dormann H, Brune K (2006) More pronounced inhibition of cyclooxygenase-2 increase in blood pressure and reduction of heart rate by treatment with diclofenac compared with celecoxib and rofecoxib. Arthritis Rheum (Munch) 54:282-291. doi: 10.1002/art.21540
33. Tegeder I, Lotsch J, Krebs S, Muth-Selbach U, Brune K, Geisslinger G (1999) Comparison of inhibitory effects of meloxicam and diclofenac on human thromboxane biosynthesis after single dose and at steady state. Clin Pharmacol Ther 65:533-544. doi: 10.1016/S0009-9236(99)70073-1
34. Simmons DL, Regina BM, Hla T (2004) Cyclooxygenase isoenzymes: The biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56:387-437. doi: 10.1124/pr.56.3.3
35. Gilroy DW, Colville-Nash PR, McMaster S, Sawatzky DA, Willoughby DA, Lawrence T (2003) Inducible cyclooxygenase-derived 15-deoxy(Delta)12-14PGJ2 brings about acute inflammatory resolution in rat pleurisy by inducing neutrophil and macrophage apoptosis. FASEB J 17:2269-2271
36. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE 2, and PAF. J Clin Invest 101:890-898. doi: 10.1172/JCI1112
37. Maggi LB Jr, Sadeghi H, Weigand C, Scarim AL, Heitmeier MR, Corbett JA (2000) Anti-inflammatory actions of 15-deoxy-delta 12, 14-prostaglandin J2 and troglitazone: Evidence for heat shock-dependent and -independent inhibition of cytokine-induced inducible nitric oxide synthase expression. Diabetes 49:346-355. doi: 10.2337/diabetes.49.3.346
38. Cuzzocrea S, Wayman NS, Mazzon E, Dugo L, Di Paola R, Serraino I, Britti D, Chatterjee PK, Caputi AP, Thiemermann C (2000) The cyclopentenone prostaglandin 15-deoxy-Delta(12, 14)-prostaglandin J(2) attenuates the development of acute and chronic inflammation. Mol Pharmacol 61:997-1007. doi: 10.1124/mol.61.5.997
39. Diab A, Deng C, Smith JD, Hussain RZ, Phanavanh B, Lovett-Racke AE, Drew PD, Racke MK (2002) Peroxisome proliferator-activated receptor-gamma agonist 15-deoxy-Delta(12, 14)-prostaglandin J(2) ameliorates experimental autoimmune encephalomyelitis. J Immunol 168:2508-2515
40. Alleva DG, Johnson EB, Lio FM, Boehme SA, Conlon PJ, Crowe PD (2002) Regulation of murine macrophage proinflammatory and anti-inflammatory cytokines by ligands for peroxisome proliferator-activated receptor-gamma: Counter-regulatory activity by IFN-gamma. J Leukoc Biol 71:677-685
41. Kim Y, Ratziu V, Choi SG, Lalazar A, Theiss G, Dang Q, Kim SJ, Friedman SL (1998) Transcriptional activation of transforming growth factor beta1 and its receptors by the Kruppel-like factor Zf9/core promoter-binding protein and Sp1. Potential mechanisms for autocrine fibrogenesis in response to injury. J Biol Chem 273:33750-33758. doi: 10.1074/ jbc.273.50.33750
42. Ruscetti FW, Palladino MA (1991) Transforming growth factor-beta and the immune system. Prog Growth Factor Res 3:159-175. doi: 10.1016/ S0955-2235(05)80006-7
43. Liu M, Yang SC, Sharma S, Luo J, Cui X, Peebles KA, Huang M, Sato M, Ramirez RD, Shay JW, Minna JD, Dubinett SM (2007) EGFR signaling is required for TGF-beta 1 mediated COX-2 induction in human bronchial epithelial cells. Am J Respir Cell Mol Biol 37:578-588. doi: 10.1165/ rcmb.2007-0100OC
44. Mitchell JA, Akarasereenont P, Thiemermann C, Flower RJ, Vane JR (1993) Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc Natl Acad Sci USA 90:11693-11697. doi: 10.1073/pnas.90.24.11693
45. Flower RJ, Vane JR (1972) Inhibition of prostaglandin synthetase in brain explains the anti-pyretic activity of paracetamol (4-acetamidophenol). Nature 240:410-411. doi: 10.1038/240410a0
46. Chandrasekharan NV, Dai H, Roos KL, Evanson NK, Tomsik J, Elton TS, Simmons DL (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: Cloning, structure, and expression. Proc Natl Acad Sci USA 99:13926-13931. doi: 10.1073/ pnas.162468699
47. Ayoub SS, Botting RM, Goorha S, Colville-Nash PR, Willoughby DA, Ballou LR (2004) Acetaminophen-induced hypothermia in mice is mediated by a prostaglandin endoperoxide synthase 1 gene-derived protein. Proc Natl Acad Sci USA 101:11165-11169. doi: 10.1073/pnas.0404185101
48. Ayoub SS, Colville-Nash PR, Willoughby DA, Botting RM (2006) The involvement of a cyclooxygenase 1 gene-derived protein in the antinociceptive action of paracetamol in mice. Eur J Pharmacol 538:57-65. doi: 10.1016/j.ejphar.2006.03.061
49. Qin N, Zhang SP, Reitz TL, Mei JM, Flores CM (2005) Cloning, expression, and functional characterization of human cyclooxygenase-1 splicing variants: Evidence for intron 1 retention. J Pharmacol Exp Ther 315:1298-1305. doi: 10.1124/jpet.105.090944
50. Nemeth JF, Hochgesang GP Jr, Marnett LJ, Caprioli RM (2001) Characterization of the glycosylation sites in cyclooxygenase-2 using mass spectrometry. Biochemistry 40:3109-3116. doi: 10.1021/bi002313c