Nitric oxide mediates the lipopolysaccharide dependent upregulation of the heme oxygenase-1 gene expression in cultured rat Kupffer cells

Journal of Hepatology

Volumn 30, Issue 1, 1999, Pages 61-69

  Immenschuh, Stephan ^a   Tan, Melly ^a   Ramadori, Giuliano ^a  

^a Zentrum Neurologische Med Georg A   (Germany)

Author keywords

Heme oxygenase 1; Kupffer cells; Lipopolysaccharide; Nitric oxide

Indexed keywords

BILIVERDIN; HEME OXYGENASE; LIPOPOLYSACCHARIDE; NITRIC OXIDE;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME LOCALIZATION; ENZYME SUBSTRATE; GENE EXPRESSION REGULATION; GENETIC REGULATION; IMMUNOCYTOCHEMISTRY; KUPFFER CELL; LIVER SINUSOID; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SEPTIC SHOCK;

EID: 0032921697     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-8278(99)80008-7     Document Type: Article

References (51)

1. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA. 61:1968;748-755.
2. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 37:1997;517-554.
3. Tenhunen R, Marver HS, Schmid R. The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin. J Lab Clin Med. 75:1970;410-417.
4. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA. 86:1989;99-103.
5. Mitani K, Fujita H, Fukuda Y, Kappas A, Sassa S. The role of inorganic metals and metalloporphyrins in the induction of haem oxygenase and heat-shock protein 70 in human hepatoma cells. Biochem J. 290:1993;819-825.
6. Shibahara S, Müller R, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem. 262:1987;12889-12892.
7. Muraosa Y, Shibahara S. Identification of a cis-regulatory element and putative trans-acting factors responsible for 12-O-tetra-decanoylphorbol-13-acetate (TPA)-mediated induction of heme oxygenase expression in myelomonocytic cell lines. Mol Cell Biol. 13:1993;7881-7991.
8. Choi AMK, Tucker RW, Carlson SG, Wiegand G, Holbrook NJ. Calcium mediates expression of stress-response genes in prostaglandin A2-induced growth arrest. FASEB J. 8:1994;1048-1054.
9. Durante W, Christodoulides N, Cheng K, Peyton KJ, Sunahara RK, Schafer AI. cAMP induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle. Am J Physiol. 273:1997;H317-H323.
10. Immenschuh S, Kietzmann T, Hinke V, Wiederhold M, Katz N, Muller-Eberhard U. The rat heme oxygenase-1 gene is transcriptionally induced via the protein kinase A signaling pathway in rat hepatocyte cultures. Mol Pharmacol. 53:1998;483-491.
11. Applegate LA, Luscher P, Tyrrell RM. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res. 51:1991;974-978.
12. Choi AMK, Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol. 15:1996;9-19.
13. Poss KD, Tonegawa S. Heme oxygenase is required for mammalian iron reutilization. Proc Natl Acad Sci USA. 94:1997;10925-10930.
14. Decker K. Biologically active products of stimulated liver macrophages (Kupffer cells). Eur J Biochem. 192:1990;245-261.
15. Bouwens L. Structural and functional aspects of Kupffer cells. Rev Biol Cell. 16:1988;69-94.
16. Nolan JP. Intestinal endotoxins as mediators of hepatic injury: an idea whose time has come again. Hepatology. 10:1989;887-891.
17. Bissell DM, Hammaker L, Schmid R. Hemoglobin and erythrocyte catabolism in rat liver: the separate roles of parenchymal and sinusoidal cells. Blood. 40:1972;812-822.
18. Goda N, Suzuki K, Naito M, Takeoka S, Tsuchida E, Ishimura Y, et al. Distribution of heme oxygenase isoforms in rat liver. Topographic basis for carbon monoxide-mediated microvascular relaxation. J Clin Invest. 101:1998;604-612.
19. Praaning-van Dalen D, Brouwer A, Knook D. Clearance capacity of rat liver Kupffer, endothelial, and parenchymal cells. Gastroenterology. 81:1981;1036-1044.
20. Bremer C, Bradford BU, Hunt KJ, Knecht KT, Connor HD, Mason RP, et al. Role of Kupffer cells in the pathogenesis of hepatic reperfusion injury. Am J Physiol. 267:1994;G630-G636.
21. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med. 2:1996;87-90.
22. Otterbein L, Sylvester SL, Choi AMK. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J Respir Cell Mol Biol. 13:1995;595-601.
23. Vogt BA, Alam J, Croatt AJ, Vercellotti GM, Nath KA. Acquired resistance to acute oxidative stress; possible role of heme oxygenase and ferritin. Lab Invest. 72:1995;474-483.
24. Yet S-E, Pellacani A, Patterson C, Tan L, Folta SC, Foster L, et al. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J Biol Chem. 272:1997;4295-4301.
25. Knook DL, Sleyster EC. Separation of Kupffer and endothelial cells of the rat liver by centrifugal elutriation. Exp Cell Res. 99:1976;444-449.
26. Armbrust T, Nordmann B, Kreiβig M, Ramadori G. CIQ synthesis by tissue mononuclear phagocytes from normal and from damaged rat liver: up-regulation by dexamcthasone, down-regulation by interferon gamma, and lipopolysaccharide. Hepatology. 26:1997;98-106.
27. Immenschuh S, Iwahara S-I, Satoh H, Nell C, Katz N, Muller-Eberhard U. Expression of the mRNA of heme-binding protein 23 is coordinated with that of heme oxygenase-1 by heme and heavy metals in primary rat hepatocytes and hepatoma cells. Biochemistry. 34:1995;13407-13411.
28. Armbrust T, Ramadori G. Functional characterization of two different Kupffer cell populations of normal liver. J Hepatol. 25:1996;518-528.
29. Shibahara S, Müller R, Taguchi H, Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci. 82:1985;7865-7869.
30. Dyjkstra CD, Döpp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies. Immunology. 54:1985;589-599.
31. Stuehr DJ, Marletta MA. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc Natl Acad Sci USA. 82:1985;7738-7742.
32. Bauer I, Wanner GA, Rensing H, Alte C, Miescher E, Wolf B, et al. Expression pattern of heme oxygenase isoenzymes 1 and 2 in normal and stress-exposed rat liver. Hepatology. 27:1998;829-838.
33. Keyse SM, Applegate LA, Tromvoukis Y, Tyrrell RM. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol Cell Biol. 10:1990;4967-4969.
34. Kietzmann T, Immenschuh S, Katz N, Jungermann K, Muller-Eberhard U. Modulation of hemopexin gene expression by physiological oxygen tensions in primary rat hepatocytes. Biochem Biophys Res Comm. 213:1995;397-403.
35. Granick S, Sinclair P, Sassa S, Grieninger G. Effects by heme, insulin, and serum albumin on heme and protein synthesis in chick embryo liver cells cultured in a chemically defined medium, and a spectrofluorometric assay for porphyrin composition. J Biol Chem. 250:1975;9215-9225.
36. Kurata S-I, Matsumoto M, Yamashita U. Concomitant transcriptional activation of nitric oxide synthase and heme oxygenase genes during nitric oxide-mediated macrophage cytostasis. J Biochem. 120:1996;49-52.
37. Kurata S-I, Matsumoto M, Tsuji Y, Nakajima H. Lipopolysaccharide activates transcription of the heme oxygenase gene in mouse Ml cells through oxidative activation of nuclear factor κB. Eur J Biochem. 239:1996;566-571.
38. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AMK. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am J Respir Cell Mol Biol. 13:1995;387-398.
39. Ulevitch RJ, Tobias PS. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu Rev Immunol. 13:1995;437-457.
40. Sweet MJ, Hume DA. Endotoxin signal transduction in macrophages. J Leukoc Biol. 60:1996;8-26.
41. Foresti R, Clark JE, Green CJ, Motterlini R. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 in endothelial cells. J Biol Chem. 272:1997;18411-18417.
42. Takahashi K, Hara E, Suzuki H, Sasano H, Shibahara S. Expression of heme oxygenase isozyme mRNAs in the human brain and induction of heme oxygenase-1 by nitric oxide donors. J Neurochem. 67:1996;482-489.
43. Hartsfield C, Alam J, Cook J, Choi AMK. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitrite oxide. Am J Physiol. 273:1997;L980-L988.
44. Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI. Nitric oxide induces heme oxygenase-1 gene expression in vascular smooth muscle cells. Cire Res. 80:1997;557-564.
45. Willis D, Tomlinson A, Frederick R, Paul-Clark MJ, Willoughby DA. Modulation of heme oxygenase activity in rat brain and spleen by inhibitors and donors of nitric oxide. Biochem Biophys Res Comm. 214:1995;1152-1156.
46. Nath KA, Balla G, Vercellotti GM, Balla J, Jacob HS, Levitt MD, et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest. 90:1992;267-270.
47. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen ME, et al. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci USA. 92:1995;6798-6802.
48. Vile GF, Tyrrell RM. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci USA. 91:1994;2607-2610.
49. Otterbein L, Chin YB, Otterbein SL, Lowe VC, Fessler HE, Choi AMK. Mechanism of hemoglobin-induced protection against endotoxemia in rats: a ferritin-independent pathway. Am J Physiol. 272:1997;L268-L275.
50. Fincato G, Polentarutti N, Sica A, Mantovani A, Colotta F. Expression of a heat-inducible gene of the HSP70 family in human myelomonocytic cells: regulation by bacterial products and cytokines. Blood. 77:1991;579-586.
51. Cable EE, Pepe JA, Karamtsios NC, Lambrecht RW, Bonkovsky HL. Differential effects of metalloporphyrins on messenger RNA levels of δ-aminolevulinate synthase and heme oxygenase. J Clin Invest. 94:1994;649-654.