NO-mediated activation of heme oxygenase: Endogenous cytoprotection against oxidative stress to endothelium

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 270, Issue 1 39-1, 1996, Pages

  Motterlini, Roberto ^a,b   Foresti, Roberta ^a   Intaglietta, Marcos ^a   Winslow, Robert M ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b NORTHWICK PARK INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

bilirubin; nitric oxide donors; stress protein; vascular endothelial cells

Indexed keywords

HEME OXYGENASE; NITRIC OXIDE;

ANIMAL CELL; AORTA; ARTICLE; BLOOD PRESSURE REGULATION; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; COMPETITIVE INHIBITION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SWINE; VASCULAR ENDOTHELIUM;

EID: 0030065052     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.1996.270.1.h107     Document Type: Article

References (39)

1. Abraham, N. G., J. H. C. Lin, M. L. Schwartzman, R. D. Levere, and S. Shibahara. The physiological significance of heme oxygenase. Int. J. Biochem. 20: 543-558, 1988.
2. Adcock, I. M., C. R. Brown, O. Kwon, and P. J. Barnes. Oxidative stress induces NF kappa B DNA binding and inducible NOS mRNA in human epithelial cells. Biochem. Biophys. Res. Commun. 199: 1518-1524, 1994.
3. Balla, G., H. S. Jacob, J. Balla, M. Rosenberg, K. Nath, F. Apple, J. W. Eaton, and G. M. Vercellotti. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267: 18148-18153, 1992.
4. Balla, J., H. S. Jacob, G. Balla, K. Nath, J. W. Eaton, and G. M. Vercellotti. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc. Natl Acad. Sci. USA 90: 9285-9289, 1993.
5. G-monomethyl-L-arginine inhibits endotoxin-induced nitrite/nitrate biosynthesis while promoting hepatic damage. J. Leukocyte Biol. 48: 565-569, 1990.
6. Estrada, C., C. Gomez, C. Martin, S. Moncada and C. Gonzales. Nitric oxide mediates tumor necrosis factor-α cytotoxicity in endothelial cells. Biochem. Biophys. Res. Commun. 186: 475-482, 1992.
7. Ewing, J. F., V. S. Raju, and M. D. Maines. Induction of heart heme oxygenase-1 (HSP32) by hyperthermia: possible role in stress-mediated elevation of cyclic 3′:5′-guanosine monophosphate. J. Pharmarol Exp. Ther. 271: 408-414, 1994.
8. Geng, Y., A. Petersson, A. Wennmalm, and G. K. Hansson. Cytokine-induced expression of nitric oxide synthase results in nitrosylation of heme and nonheme iron proteins in vascular smooth muscle cells. Exp. Cell Res. 214: 418-428, 1994.
9. Halliwell, B., and M. C. Gutteridge. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186: 1-85, 1990.
10. Ioannidis, I., and H. De Groot. Cytotoxicity of nitric oxide in Fu5 rat hepatoma cells: evidence for co-operative action with hydrogen peroxide. Biochem. J. 296: 341-345, 1993.
11. Iyengar, R., D. J. Stuehr, and M. A. Marietta. Macrophage synthesis of nitrite, nitrate and N-nitrosamines: precursors and role of the respiratory burst. Proc. Natl. Acad. Sci. USA 84: 6369-6373, 1987.
12. Keyse, S. M., and R. M. Tyrrell. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblast by UVA radiation, hydrogen peroxide, and sodium arsemte. Proc. Natl. Acad. Sci USA 86: 99-103, 1989.
13. Keyse, S. M., and R. M. Tyrrell. Induction of the heme oxygenase gene in human skin fibroblast by hydrogen peroxide and UVA(365 nm) radiation: evidence for the involvement of the hydroxyl radical. Carcinogenesis 11: 787-791, 1989.
14. Khatsenko, O. G., S. S. Gross, A. B. Rifkind, and J. R. Vane. Nitric oxide is a mediator of the decrease in cytochrome P450-dependent metabolism caused by immunostimulants. Proc. Natl. Acad. Sci. USA 90: 11147-11151, 1993.
15. G-methyl-L-arginine inhibits tumor necrosis factor-induced hypotension: implications for the involvement of nitric oxide. Proc. Natl. Acad. Sci. USA 87: 3629-3632, 1990.
16. Lefer, D. J., K. Nakanishi, W. E. Johnston, and J. Vinten-Johansen. Antineutrophil and myocardial protecting actions of novel nitric oxide donors after acute myocardial ischemia and reperfusion in dogs. Circulation 88: 2337-2350, 1993.
17. Llesuy, S. F., and M. L. Tomaro. Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim. Biophys. Acta 1223: 9-14, 1994.
18. Lu, D., N. Maulik, I. I. Moraru, D. L. Kreutzer, and D. K. Das. Molecular adaptation of vascular endothelial cells to oxidative stress. Am. J. Physiol. 264 (Cell Physiol. 33): C715-C722, 1993.
19. Maines, M. D. Heme Oxygenase: Clinical Applications and Functions. Boca Raton, FL: CRC Press, 1992, p. 276
20. Maines, M. D., and A. Kappas. Metals as regulator of heme oxygenase. Science Wash. DC 198: 1215-1221, 1977.
21. Matheis, G., M. P. Sherman, G. D. Buckberg, D. M. Haybron, H. H. Young, and L. J. Ignarro. Role of L-arginine-nitric oxide pathway in myocardial reoxygenation injury. Am. J. Physiol. 262 (Heart Circ. Physiol. 31): H616-H620, 1992.
22. Mayer, B., F. Brunner, and K. Schmidt. Novel actions of methylene blue. Eur. Heart J. 14: 22-26, 1993.
23. Motterlini, R., R. Foresti, K. Vandegriff, M. Intaglietta, and R. M. Winslow. Oxidative-stress response in vascular endothelial cells exposed to acellular hemoglobin solutions. Am. J. Physiol. 269 (Heart Circ. Physiol. 38): H648-H655, 1995.
24. Neuzil, J., and R. Stocker. Bilirubin attenuates radical-mediated damage to serum albumin. FEBS Lett. 331: 281-284, 1993.
25. Neuzil, J., and R. Stocker. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J. Biol. Chem. 269: 16712-16719, 1994.
26. Nunoshiba, T., T. DeRojas-Walker, J. S. Wishnok, S. R. Tannenbaum, and B. Demple. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophage. Proc. Natl. Acad. Sci. USA 90: 9993-9997, 1993.
27. Oswald, I. P., I. Eltoum, T. A. Wynn, B. Schwartz, P. Caspar, D. Paulin, A. Sher, and S. L. James. Endothelial cells are activated by cytokine treatment to kill an intravascular parasite, Schistosoma mansoni, through the production of nitric oxide. Proc. Natl. Acad. Sci. USA 91: 999-1003, 1994.
28. Palmer, R. M. J., D. S. Ashton, and S. Moncada. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature Lond. 333: 664-666, 1988.
29. Peterson, G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83: 346-356, 1977.
30. Radomski, M. W., R. M. J. Palmer, and S. Moncada. Glucocorticoids inhibit the expression of an inducible, but not constitutive, nitric oxide synthase in vascular endothelial cells. Proc. Natl. Acad. Sci. USA 87: 10043-10047, 1990.
31. Rapoport, R. M., and F. Murad. Agonist induced endothelium-dependent relaxation in rat thoracic aorta may be mediated through cyclic GMP. Circ. Res. 52: 352-357, 1983.
32. Rees, D. D., R. M. J. Palmer, and S. Moncada. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc. Natl. Acad. Sci. USA 86: 3375-3378, 1989.
33. Rizzardini, M., M. Terao, F. Falciani, and L. Cantoni. Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem gene. Biochem. J. 290: 343-347, 1993.
34. Schluter, K. D., M. Weber, E. Schraven, and H. M. Piper. NO donor SIN-1 protects against reoxygenation-induced cardiomyocyte injury by a dual action. Am. J. Physiol. 267 (Heart Circ. Physiol 36): H1461-H1466, 1994.
35. Siegfried, M. R., J. Erhardt, T. Rider, X. L. Ma, and A. M. Lefer. Cardioprotection and attenuation of endothelial dysfunction by organic nitric oxide donors in myocardial ischemia reperfusion. J. Pharmacol. Exp. Ther. 260: 668-675, 1992.
36. Stocker, R., Y. Yamamoto, A. F. McDonagh, A. N. Glazer, and B. N. Ames. Bilirubin is an antioxidant of possible physiological importance. Science Wash. DC 235: 1043-1046, 1987.
37. Stuehr, D. J., and C. F. Nathan. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor cells. J. Exp. Med. 169: 1543-1555, 1989.
38. Tenhunen, R., H. S. Marver, and R. Schmid. The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin. J. Lab. Clin. Med. 75: 410-421, 1970.
39. Wink, D. A., I. Hanbauer, M. C. Krishna, W. DeGraff, J. Gamson, and J. B. Mitchell. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA 90: 9813-9817, 1993.