Dual role of heme oxygenase in epithelial cell injury: Contrasting effects of short-term and long-term exposure to oxidant stress

Journal of Laboratory and Clinical Medicine

Volumn 128, Issue 3, 1996, Pages 290-296

  Da Silva, Jean Louis ^a   Morishita, Tomoyuki ^b   Escalante, Bruno ^b   Staudinger, Robert ^b   Drummond, George ^b   Goligorsky, Michael S ^b   Lutton, John D ^b   Abraham, Nader G ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0030230925     PISSN: 00222143     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2143(96)90030-X     Document Type: Article

References (38)

1. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32 kDA stress protein induced in human skin fibroblasts by UV radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 1989;86:99-103.
2. Abraham NG, Lavorvsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen E, et al. Transfection of the human heme oxygenase into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci USA 1995;92:6798-802.
3. Stocker O, Yammamato Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987;235:1043-7.
4. 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 1993;290:819-25.
5. Abraham NG, Lin JH-C, Schwartzman ML, Levere RD, Shibahara S. The physiological significance of heme oxygenase. Int Biochem 1988;20:543-58.
6. Kappas MD, Maines A. Metals as regulators of heme metabolism. Science 1976;192:60-2.
7. Shibahara S, Muller RM, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 1987;262: 12889-92.
8. Mitani K, Fujita H, Sassa S, Kappas A. Heat shock induction of heme oxygenase mRNA in human Hep3B hepatoma cells. Biochem Biophys Res Commun 1989;165:437-41.
9. Nascimento AL, Luscher P, Tyrell RM. Ultraviolet A (320-380 nm) radiation causes an alteration in the binding of a specific protein/protein complex to a short region of the promoter of the human oxygenase 1 gene. Nucleic Acids Res 1993;21:1103-9.
10. Alam J, Zhining D. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J Biol Chem 1992;267:21894-900.
11. Balla G, Vercelloti GM, Muller-Eberhard U, Eaton J, Jacob HS. Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab Invest 1991;64:648-55.
12. Kappas A, Drummond GS. Control of heme and cytochrome P450 metabolism by inorganic metals, organometals and synthetic metalloporphyrins. Environ Health Perspect 1984;57:301-6.
13. Stout DL, Becker FF. Heme enzyme patterns in genetically and chemically induced mouse liver tumors. Cancer Res 1986;46:2756-9.
14. Matsuura Y, Watanabe H, Fukuda T, Yoshida T, Kiroiwa Y. A sustained increase of microsomal heme oxygenase activity following treatment of rats with bacillus Calmette-Guerin and Corynebacterium parvum: its possible relation to the decrease of cytochrome P450 content. J Pharmacobiodyn 1985;8:668-78.
15. Shibagara S, Yoshizawa M, Suzuki H, Takeda K, Meguro K, Edno K. Functional analysis of cDNAs for two types of human heme oxygenase and evidence for their separate regulation. J Biochem 1993;113:214-8.
16. Nath KA, Balla G, Vercelloti 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 1992;90: 267-70.
17. Stocker R. Induction of haem oxygenase as defence against oxidative stress. Free Radic Res Commun 1990;9:101-12.
18. Taketani S, Kohno H, Yohinaga T, Tokunaga R. The human 32-kDa stress protein induced by exposure to arsenite and cadmium ions is heme oxygenase. FEBS Lett 1989;245:173-6.
19. Paller MS, Jacob HS. Cytochrome P450 mediates tissue-damaging hydroxyl radical formation during reoxygenation of the kidney. Proc Natl Acad Sci USA 1994;91:7002-6.
20. Abraham NG, Drummond G, Lutton JD, Kappas A. The significance and physiological role of heme oxygenase. Cellular Physics and Biochemistry (in press).
21. McCoubrey WK Jr, Weing JF, Maines MD. Human heme oxygenase-2: characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of a polyadenylation signal. Arch Biochem Biophys 1992;295:13-20.
22. Goligorsky MS, Morgan MA, Lyibsky S, Gross R, Adams D, Spitz D. Establishment of a hydrogen peroxide resistant variant of renal tubular epithelial cells: role of calcium-independent phospholipase A2 in cell damage. Arch Biochem Biophys 1992;295:13-20.
23. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem 1969; 244:6388-94.
24. Lutton JD, da Silva J-L, Moqattash S, Brown AC, Abraham NG. Differential induction of heme oxygenase in the hepatocarcinoma cell line (Hep3b) by environmental agents. J Cell Biochem 1992;49:259-65.
25. Lowry OH, Rosenbrough NF, Farr AG, Randal RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
26. Chomczynski R, Sacchi N. Single-step method of RNA isolation by acid guanidium isothiocyanate-phenol-chlorform extraction. Anal Biochem 1987;162:156-9.
27. Yoshida T, Biro P, Cohen T, Muller RM, Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur J Biochem 1988;171:457-61.
28. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science 1993;259:381-4.
29. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, et al. Ferritin: a cytoprotective antioxidant Strategen of endothelium. J Biol Chem 1992;267:18148-53.
30. Klausner RD, Rouault TA, Harford JB. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 1993;72: 19-28.
31. Guy GR, Cairns J, Ng SB, Tan YH. Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 1993;268:2141-8.
32. Vile GF, Tyrell RM. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J Biol Chem 1993; 268:14678-81.
33. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, et al. Ferritin: a cytoprotective antioxidant strategen of endothelium. J Biol Chem 1992;267:18148-53.
34. Kutty G, Hayden B, Osawa Y, Wiggert B, Chader GJ, Kutty RK. Heme oxygenase: expression in human retina and modulation by stress agents in a human retinoblastoma cell model system. Curr Eye Res 1992;11:153-60.
35. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercelloti JM. Endothelial cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 1993;90:9285-9.
36. Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol inhibiting plasma and low density lipoprotein lipid peroxidation. J Biol Chem 1994;269:16712-9.
37. Vile GF, Basu-Modak S, Waltner C, Tyrrell RM. Heme oxygenase-1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci USA 1994;91:2607-20.
38. Morishita T, Peresleny T, Noiri E, Staudinger R, Abraham NG, Goligorsky MS. Dual role of heme oxygenase in epithelial cell injury: contrasting effects of acute and chronic oxidant stress. J Am Soc Nephrol 1994;5:904.