Enhanced expression of haem oxygenase-1 by nitric oxide and antiinflammatory drugs in NIH 3T3 fibroblasts

British Journal of Pharmacology

Volumn 130, Issue 1, 2000, Pages 57-64

  Alcaraz, Maria José ^b   Habib, Aïda ^a   Lebret, Marilyne ^a   Créminon, Christophe ^c   Lévy Toledano, Sylviane ^a   Maclouf, Jacques ^a  

^a INSERM   (France)

^b UNIVERSITY OF VALENCIA   (Spain)

^c Institut National de la Recherche Agronomique   (France)

Author keywords

Cyclo oxygenase 2; Haem oxygenase; Lipopolysaccharide; NIH 3T3 fibroblasts; Nitric oxide; Non steroidal antiinflammatory drugs; Reactive oxygen intermediates

Indexed keywords

5 (4 FLUOROPHENYL) 1 [(4 METHYLSULFONYL)PHENYL] 3 TRIFLUOROMETHYLPYRAZOLE; ANTIINFLAMMATORY AGENT; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; FLURBIPROFEN; HEME OXYGENASE; INDOMETACIN; LIPOPOLYSACCHARIDE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; PROTOPORPHYRIN ZINC; SPERMINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CELL STRAIN 3T3; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; ENZYME ACTIVITY; ENZYME INDUCTION; INFLAMMATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROSTAGLANDIN SYNTHESIS;

EID: 0002167892     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0703281     Document Type: Article

References (47)

1. ABRAHAM, N.G., LIN, J.H., SCHWARTZMAN, M.L., LEVERE, R.D. & SHIBAHARA, S. (1988). The physiological significance of heme oxygenase. Int. J. Biochem., 20, 543-558.
2. CAMHI, S.L., ALAM. J., OTTERBEIN, L., SYLVESTER, S.L. & CHOI, A.M. (1995). Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am. J. Respir. Cell Mol. Biol., 13, 387-398.
3. CAMHI, S.L., ALAM, J., WIEGAND, G.W., CHIN, B.Y. & CHOI, A.M. (1998). Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: role of reactive oxygen intermediates and AP-1. Am. J. Respir. Cell Mol. Biol., 18, 226-234.
4. COLVILLE-NASH, P.R., QURESHI, S.S., WILLIS, D. & WILLOUGHBY, D.A. (1998). Inhibition of inducible nitric oxide synthase by peroxisome proliferator-activated receptor agonists: correlation with induction of heme oxygenase 1. J. Immunol., 161, 978-984.
5. CRÉMINON, C., HABIB, A., MACLOUF, J., PRADELLES, P., GRASSI, J. & FROBERT, Y. (1995). Differential measurement of constitutive (Cox-1) and inducible (Cox-2) cyclooxygenase expression in human umbilical vein endothelial cells using specific immunometric enzyme immunoassays. Biochim. Biophys. Acta, 1254, 341-348.
6. DENNERY, PA., SRIDHAR, K.J., LEE, C.S., WONG, H.E., SHOKOOHI, V., RODGERS, P.A. & SPITZ, D.R. (1997). Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J. Biol. Chem., 272, 14937-14942.
7. DERAMAUDT, B.M., BRAUNSTEIN, S., REMY, P. & ABRAHAM, N.G. (1998). Gene transfer of human heme oxygenase into coronary endothelial cells potentially promotes angiogenesis. J. Cell Biochem., 68, 121-127.
8. DURANTE, W., KROLL, M.H., CHRISTODOULIDES, N., PEYTON, K.J. & SCHAFER, A.I. (1997). Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ. Res., 80, 557-564.
9. FORESTI, R., CLARK, J.E., GREEN, C.J. & MOTTERLINI, R. (1997). Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of Superoxide and peroxynitrite anions. J. Biol. Chem., 272, 18411-18417.
10. FREI, B., STOCKER, R. & AMES, B.N. (1988). Antioxidant defenses and lipid peroxidation in human blood plasma. Proc. Natl. Acad. Sci. U.S.A., 85, 9748-9752.
11. 2 synthase (cyclooxygenase) in human monocytes. J. Biol. Chem., 265, 16737-16740.
12. 15N) in biological fluids. Anal. Biochem., 126, 131-138.
13. HABIB, A., BERNARD, C., LEBRET, M., CRÉMINON, C., ESPOSITO, B., TEDGUI, A. & MACLOUF, J. (1997). Regulation of the expression of cyclooxygenase-2 by nitric oxide in rat peritoneal macrophages. J. Immunol., 158, 3845-3851.
14. HAIDER, A., FERRERI, N.R. & ABRAHAM, N.G. (1999). The regulatory role of home oxygenase on the cyclooxygenase pathway. FASEB J., 13 (Part II), A781.
15. HARTSFIELD, C.L., ALAM, J., COOK, J.L. & CHOI, A.M.K. (1997). Regulation of home oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am. J. Physiol., 273, L980-L988.
16. HERSCHMAN, H., GILBERT, R., REDDY, S. & XIE, W. (1997). Coordinate regulation of the inducible forms of prostaglandin synthase and nitric oxide synthase in fibroblasts and macrophages. In Eicosanoids and other bioactive lipids in cancer, inflammation, and radiation injury. ed. Honn, K.V., pp. 177-182. New York: Plenum Press.
17. HLA, T. & NEILSON, K. (1992). Human cyclooxygenase-2 cDNA. Proc. Natl. Acad. Sci. U.S.A., 89, 7384-7388.
18. 2 isomerase activity by PDGF: involvement of nitric oxide. Arch. Biochem. Biophys., 312, 240 243.
19. KLM, Y.M., BERGONIA, H.A., MÜLLER, C., PITT, B.R., WATKINS, W.D. & LANCASTER, J.R.J. (1995). Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem., 270, 5710-5713.
20. KNOWLES, R.G. & MONCADA, S. (1994). Nitric oxide synthases in mammals. Biochem. J., 298, 249-258.
21. KRÖNCKE, K.-D., FEHSEL, K. & KOLB-BACHOFEN, V. (1997). Nitric oxide: cytotoxicity versus cytoprotection How, why, when and where? Nitric Oxide: Biol. Chem., 1, 107-120.
22. KUJUBU, D.A., REDDY, S.T., FLETCHER, B.S. & HERSCHMAN, H.R. (1993). Expression of the protein product of the prostaglandin synthase-2 TIS10 gene in mitogen stimulated Swiss 3T3 cells. J. Biol. Chem., 268, 5425-5430.
23. KURATA, S.-I., MATSUMOTO, M., TSUJI, Y. & NAKAJIMA, H. (1996). Lipopolysaccharide activates transcription of the heme oxygenase gene in mouse M1 cells through oxidative activation of nuclear factor kB. Eur. J. Biochem., 239, 566-571.
24. LANIADO-SCHWARTZMAN, M., ABRAHAM, N.G., CONNERS, M., DUNN, M.W., LEVERE, R.D. & KAPPAS, A. (1997). Home oxygenase induction with attenuation of experimentally induced corneal inflammation. Biochem. Pharmacol., 53, 1069-1075.
25. MCCOUBREY, W.K., HUAG, T.J. & MAINES, M.D. (1997). Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem., 247, 725-732.
26. MEADE, E.A., MCINTYRE, T.M., ZIMMERMAN, G.A. & PRESCOTT, S.M. (1999). Peroxisome proliferators enhance cyclooxygenase-2 expression in epithelial cells. J. Biol. Chem., 274, 8328-8334.
27. MONCADA, S. & HIGGS, A. (1993). The L-arginine-nitric oxide pathway. N. Engl. J. Med., 329, 2002-2012.
28. MOSLEY, K., WEMBRIDGE, D.E., CATTELL, V. & COOK, H.T. (1998). Heme oxygenase is induced in nephrotoxic nephritis and hemin, a stimulator of heme oxygenase synthesis, ameliorates disease. Kidney Int., 53, 672-678.
29. MOTTERLINI, R., GONZALES, A., FORESTI, R., CLARK, J.E., GREEN, C.J. & WINSLOW, R.M. (1998). Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ. Res., 83, 568-577.
30. NAKAGAMI, T., TOYOMURA, K., KINOSHITA. T. & MORISAWA, S. (1993). A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochim. Biophys. Acta, 1158, 189-193.
31. NUMAZAWA, S., YAMADA, H., FURUSHO, A., NAKAHARA, T., OGURO, T. & YOSHIDA, T. (1997). Cooperative induction of c-fos and heme oxygenase gene products under oxidative stress in human fibroblastic cells. Exp. Cell Res., 237, 434-444.
32. OTTERBEIN, L.E., KOLLS, J.K., MANTELL, L.L., COOK, J.L., ALAM, J. & CHOI, A.M. (1999). Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J. Clin. Invest., 103, 1047-1054.
33. POSS, K.D. & TONEGAWA, S. (1997a). Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. U.S.A., 94, 10919-10924.
34. POSS, K.D. & TONEGAWA, S. (1997b). Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U.S.A., 94, 10925-10930.
35. PRADELLES, P., GRASSI, J. & MACLOUF, J. (1985). Enzyme immunoassay of eicosanoids using acetylcholine esterase as label: an alternative to radioimmunoassay. Anal. Chem., 57, 1170-1173.
36. REDDY, S.T. & HERSCHMAN, H.R. (1994). Ligand-induced prostaglandin synthesis requires expression of the TTS10/PGS-2 prostaglandin synthase gene in murine fibrohlasts and macrophages. J. Biol. Chem., 269, 15473-15480.
37. SEIBERT, K., ZHANG. Y., LEAHY, K., HAUSER, S., MASFERRER, J., PERKINS, W., LEE, L. & ISAKSON, P. ( 1994). Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc. Natl. Acad. Sci. U.S.A., 91, 12013-12017.
38. SHIBAHARA, S., MULLER, R.M. & TAGUCHI, H. (1987). Transcriptional control of rat heme oxygenase by heat shock. J. Biol. Chem., 262, 12889-12892.
39. SOARES, M.P., LIN, Y., ANRATHER, J., CSIZMADIA, E., TAKIGAMI. K., SATO, K., GREY, S.T., COLVIN, R.B., CHOI, A.M., POSS, K.D. & BACH, F.H. (1998). Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nature Med., 4, 1073-1077.
40. STEINHAUSER, M.L., KUNKEL, S.L., HOGABOAM, C.M., EVANOFF, H., STRIETER, R.M. & LUKACS, N.W. (1998). Macrophage/ fibroblast coculture induces macrophage inflammatory protein-1 alpha production mediated by intercellular adhesion molecule-1 and oxygen radicals. J. Leukoc. Biol., 64, 636-641.
41. STOCKER, R. & PETERHANS, E. (1989). Antioxidant properties of conjugated bilirubin and biliverdin: biologically relevant scavenging of hypochlorous acid. Free Rad. Res. Comms., 6, 57-66.
42. TERRY, C.M., CLIKEMAN, J.A., HOIDAL, J.R. & CALLAHAN, K.S. (1998). Effect of tumor necrosis factor-α and interleukin-1α on heme oxygenase-1 expression in human endothelial cells. Am. J. Physiol., 274, H883-H891.
43. 2 negatively modulates interleukin-1 induced heme oxygenase-1 mRNA. Biochem. Biophys. Res. Commun., 212, 617-623.
44. WAGENER, F.A.D.T.G., FELDMAN, E., DE WITTE, T. & ABRAHAM, N.G. (1997). Heme induces the expression of adhesion molecules ICAM-1, VCAM-1, and E selectin in vascular endothelial cells. Proc. Soc. Exp. Biol. Med., 216, 456-463.
45. WILLIS, D., MOORE, A.R., FREDERICK, R. & WILLOUGHBY, D.A. (1996). Heme oxygenase: a novel target for the modulation of the inflammatory response. Nature Med., 2, 87-90.
46. WILLIS, D., TOMLINSON, A., FREDERICK, R., PAUL, C.M. & WILLOUGHBY, D.A. (1995). Modulation of heme oxygenase activity in rat brain and spleen by inhibitors and donors of nitric oxide. Biochem. Biophys. Res. Commun., 214, 1152-1156.
47. ZHANG, S.Z., LIPSKI, M.M., TRUMP, B.F. & HSU, I.C. (1990). Neutral red (NR) assay for cell viability and xenobiotic-induced cytotoxicity in primary cultures of human and rat hepatocytes. Cell Biol. Toxicol., 6, 219-234.