Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron

FASEB Journal

Volumn 13, Issue 13, 1999, Pages 1800-1809

  Suttner, Denise M ^a   Dennery, Phyllis A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bilirubin; Carbon monoxide; Doxycycline; Heme; Hyperoxia

Indexed keywords

BILE PIGMENT; BILIRUBIN; CARBON DIOXIDE; CARBON MONOXIDE; COMPLEMENTARY DNA; CYCLIC GMP; DOXYCYCLINE; GUANYLATE CYCLASE; HEME OXYGENASE; IRON; OXYGEN; TETRACYCLINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME REGULATION; GENE EXPRESSION; HAMSTER; HYPEROXIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALIA; CRICETINAE;

EID: 0032827423     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.13.1800     Document Type: Article

References (63)

1. Applegate, L. A., Luscher, P., and Tyrrell, R. M. (1991) Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res. 51, 974-978
2. Abraham, N. G., Lin, J. H., Schwartzman, M. L., Levere, R. D., and Shibahara, S. (1988) The physiological significance of heme oxygenase. Int. J. Biochem. 20, 543-558
3. Yee, E. L., Pitt, B. R., Billiar, T. R., and Kim, Y. M. (1996) Effect of nitric oxide on heme metabolism in pulmonary artery endothelial cells. Am. J. Physiol. 271, L512-L518
4. Zayasu, K., Sekizawa, K., Okinaga, S., Yamaya, M., Ohrui, T., and Sasaki, H. (1997) Increased carbon monoxide in exhaled air of asthmatic patients. Am. J. Respir. Crit. Care 156, 1140-1143
5. Abraham, N. G., Lavrovsky, Y., Schwartzman, M. L., Stoltz, R. A., Levere, R. D., Gerritsen, M. E., Shibahara, S., and Kappas, A. (1995) 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, 6798-6802
6. Dennery, P. A., Wong, H. E., Sridhar, K. J., Rodgers, P. A., Sim, J. E., and Spitz, D. R. (1996) Differences in basal and hyperoxiaassociated HO expression in oxidant-resistant hamster fibroblasts. Am. J. Physiol. 271, L672-L679
7. Dennery, P., Sridhar, K., Lee, C., Wong, H., Shokoohi, V., Rodgers, P., and Spitz, D. (1997) Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J. Biol. Chem. 272, 14937-14942
8. Vile, G. F., Basu-Modak, S., Waltner, C., and Tyrrell, R. M. (1994) Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. USA 91, 2607-2610
9. Otterbein, L., Sylvester, S. L., and Choi, A. M. (1995) Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am. J. Respir. Cell. Mol. Biol. 13, 595-601
10. Rizzardini, M., Terao, M., Falciani, F., and Cantoni, L. (1993) Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene. Biochem. J. 343-347
11. Yet, S. F., Pellacani, A., Patterson, C., Tan, L., Folta, S. C., Foster, L., Lee, W. S., Hsieh, C. M., and Perrella, M. A. (1997) Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J. Biol. Chem. 272, 4295-4301
12. Lin, J. H., Villalon, P., Martasek, P., and Abraham, N. G. (1990) Regulation of heme oxygenase gene expression by cobalt in rat liver and kidney. Eur J. Biochem. 192, 577-582
13. Ewing, J. F., Haber, S. N., and Maines, M. D. (1992) Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J. Neurochem. 58, 1140-1149
14. Gutteridge, J. M., Rowley, D. A., and Halliwell, B. (1981) Superoxide-dependent formation of hydroxyl radicals in the presence of iron salts. Detection of 'free' iron in biological systems by using bleomycin-dependent degradation of DNA. Biochem. J. 199, 263-265
15. Contag, C. H., Spillman, S. D., Contag, P. R., Oshiro, M., Eames, B., Dennery, P. A., Stevenson, D. K., and Benaron, D. A. (1997) Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem. Photobiol. 66, 523-531
16. Vreman, H. J., and Stevenson, D. K. (1988) Heme oxygenase activity as measured by carbon monoxide production. Anal. Biochem. 168, 31-38
17. Bradford, M. M. (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
18. Wilks, A., Black, S. M., Miller, W. L., and Ortiz de Montellano, P. R. (1995) Expression and characterization of truncated human heme oxygenase (hHO-1) and a fusion protein of hHO-1 with human cytochrome P450 reductase. Biochemistry 34, 4421-4427
19. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
20. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354
21. Koh, J. Y., and Choi, D. W. (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Methods 20, 83-90
22. Wright, J. R., Colby, H. D., and Miles, P. R. (1981) Cytosolic factors which affect microsomal lipid peroxidation in lung and liver. Arch. Biochem. Biophys. 206, 296-304
23. Rahman, I., Bel, A., Mulier, B., Lawson, M. F., Harrison, D. J., Macnee, W., and Smith, C. A. (1996) Transcriptional regulation of gamma-glutamylcysteine synthetase-heavy subunit by oxidants in human alveolar epithelial cells. Biochem. Biophys. Res. Commun. 229, 832-837
24. Fuhrop, J. H., and Smith, K. M. (1975) Hemes: determination as pyridine hemochromes. In Porphyrins and Metalloporphyrins (Smith, K. M., ed) pp. 804-807, Elsevier, New York
25. Evans, P. J., and Halliwell, B. (1994) Measurement of iron and copper in biological systems: bleomycin and copper-phenanthrolene assays. Methods Enzymol. 233, 82-92
26. McDonagh, A. F., Agati, G., and Lightner, D. A. (1998) Induction of wavelength-dependent photochemistry in bilirubins by serum albumin. Monatsh. Chem. 129, 649-660
27. Christodoulides, N., Durante, W., Kroll, M. H., and Schafer, A. I. (1995) Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation 91, 2306-2309
28. Lee, P. J., Alam, J., Wiegand, G. W., and Choi, A. M. (1996) Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc. Natl. Acad. Sci. USA 93, 10393-10398
29. Wang, Y., and Becker, D. (1997) Antisense targeting of basic fibroblast growth factor and fibroblast growth factor receptor-1 in human melanomas blocks intratumoral angiogenesis and tumor growth. Nat. Med. 3, 887-893
30. Hsu, P. I., Chow, N. H., Lai, K. H., Yang, H. B., Chan, S. H., Lin, X. Z., Cheng, J. S., Huang, J. S., Ger, L. P., Huang, S. M., Yen, M. Y., and Yang, Y. F. (1997) Implications of serum basic fibroblast growth factor levels in chronic liver diseases and hepatocellular carcinoma. Anticancer Res. 17, 2803-2809
31. de Jong, J. S., van Diest, P. J., van der Valk, P., and Baak, J. P. (1998) Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. II: Correlations with proliferation and angiogenesis. J. Pathol. 184, 53-57
32. Levine, R., Williams, J., Stadtman, E., and Shacter, E. (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233, 346-357
33. Schacter, E., Williams, J. A., Lim, M., and Levine, R. L. (1994) Differential susceptibility of plasma proteins to oxidative modification: examination by Western blot immunoassay. Free Rad. Biol. Med. 17, 429-437
34. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazzer, A. N., and Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiologic importance. Science 235, 1043-1046
35. Balla, G., Jacob, H. S., Balla, J., Rosenberg, M., Nath, K., Apple, F., Eaton, J. W., and Vercellotti, G. M. (1992) Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267, 18148-18153
36. Eisenstein, R. S., and Munro, H. N. (1990) Translational regulation of ferritin synthesis by iron. Enzyme 44, 42-58
37. Gutteridge, J. M., Rowley, D. A., and Halliwell, B. (1982) Superoxide-dependent formation of hydroxyl radicals and lipid peroxidation in the presence of iron salts. Detection of 'catalytic' iron and anti-oxidant activity in extracellular fluids. Biochem. J. 206, 605-609
38. da Silva, J. L., Morishita, T., Escalante, B., Staudinger, R., Drummond, G., Goligorsky, M. S., Lutton, J. D., and Abraham, N. G. (1996) Dual role of heme oxygenase in epithelial cell injury: contrasting effects of short-term and long-term exposure to oxidant stress. J. Lab. Clin. Med. 128, 290-296
39. Suttner, D. M., Sridhar, K. J., Lee, C. S., Tamura, T., Hansen, T. N., and Dennery, P. A. (1999) Overexpression of heme oxygenase-1 increases resistance to oxygen toxicity in rat fetal lung cells. Am. J. Physiol. 276, 463-470
40. Gladstone, I. M., Jr., and Levine, R. L. (1994) Oxidation of proteins in neonatal lungs. Pediatrics 93, 764-768
41. Varsila, E., Pesonen, E., and Andersson, S. (1995) Early protein oxidation in the neonatal lung is related to development of chronic lung disease. Acta Paediatr. 84, 1296-1299
42. Rahman, I., Clerch, L. B., and Massaro, D. (1991) Rat lung antioxidant enzyme induction by ozone. Am. J. Physiol. L412-L418
43. Willis, D. (1995) Expression and modulatory effects of heme oxygenase in acute inflammation in the rat. Inflammation Res. 44 (Suppl. 2), S218-S220
44. Madden, S. L., Galella, E. A., Riley, D., Bertelsen, A. H., and Beaudry, G. A. (1996) Induction of cell growth regulatory genes by P53. Cancer Res. 56, 5384-5390
45. Gansauge, S., Gansauge, F., Cause, H., Poch, B., Schoenberg, M. H., and Beger, H. G. (1997) The induction of apoptosis in proliferating human fibroblasts by oxygen radicals is associated with a p53- and p21WAF1CIP1 induction. FEBS Lett. 404, 6-10
46. Liebler, J. M., Picou, M. A., Qu, Z., Powers, M. R., and Rosenbaum, J. T. (1997) Altered immunohistochemical localization of basic fibroblast growth factor after bleomycin-induced lung injury. Growth Factors 14, 25-38
47. Vaillant, P., Menard, O., Vignaud, J. M., Martinet, N., and Martinet, Y. (1996) The role of cytokines in human lung fibrosis. Manaldi Arch. Chest Dis. 51, 145-152
48. Inoue, Y., King, T. E., Jr., Tinkle, S. S., Dockstader, K., and Newman, L. S. (1996) Human mast cell basic fibroblast growth factor in pulmonary fibrotic disorders. Am. J. Pathol. 149, 2037-2054
49. Vile, G. F., and Tyrrell, R. M. (1993) Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J. Biol. Chem. 268, 14678-14681
50. Ferreira, G. C. (1995) Ferrochelatase binds the iron-responsive element present in the erythroid 5-aminolevulinate synthase mRNA. Biochem. Biophys. Res. Commun. 214, 875-878
51. Bloch, K. D., Filippov, G., Sanchez, L. S., Nakane, M., and de la Monte, S. M. (1997) Pulmonary soluble guanylate cyclase, a nitric oxide receptor, is increased during the perinatal period. Am. J. Physiol. 272, L400-L406
52. Ignarro, L. J., Ballot, B., and Wood, K. S. (1984) Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. J. Biol. Chem. 259, 6201-6207
53. Patel, M. J., Wypij, D. M., Rose, D. A., Rimele, T. J., and Wiseman, J. S. (1995) Secretion of cyclic GMP by cultured epithelial and fibroblast cell lines in response to nitric oxide. J. Pharmacol. Exp. Ther. 273, 16-25
54. Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V., and Snyder, S. H. (1993) Carbon monoxide: a putative neural messenger. Science 259, 381-384
55. Vigne, P., Feolde, E., Ladoux, A., Duval, D., and Frelin, C. (1995) Contributions of NO synthase and heme oxygenase to cGMP formation by cytokine and hemin treated brain capillary endothelial cells. Biochem. Biophys. Res. Commun. 214, 1-5
56. Coceani, F., Kelsey, L., and Seidlitz, E. (1996) Carbon monoxide-induced relaxation of the ductus arteriosus in the lamb: evidence against the prime role of guanylyl cyclase. Br. J. Pharmacol. 118, 1689-1696
57. Nutter, L. M., Sierra, E. E., and Ngo, E. O. (1994) Heme oxygenase does not protect human cells against oxidant stress. J. Lab. Clin. Med. 123, 506-514
58. Gutteridge, J. M., Mumby, S., Quinlan, G. J., Chung, K. F., and Evans, T. W. (1996) Pro-oxidant iron is present in human pulmonary epithelial lining fluid: implications for oxidative stress in the lung. Biochem. Biophys. Res. Commun. 220, 1024-1027
59. Gutteridge, J. M., Mumby, S., Koizumi, M., and Taniguchi, N. (1996) 'Free' iron in neonatal plasma activates aconitase: evidence for biologically reactive iron. Biochem. Biophys. Res. Commun. 229, 806-809
60. Gutteridge, J. M., Quinlan, G. J., and Evans, T. W. (1994) Transient iron overload with bleomycin detectable iron in the plasma of patients with adult respiratory distress syndrome. Thorax 49, 707-710
61. Ryan, T. P., Krzesicki, R. F., Blakeman, D. P., Chin, J. E., Griffin, R. L., Richards, I. M., Aust, S. D., and Petry, T. W. (1997) Pulmonary ferritin: differential effects of hyperoxic lung injury on subunit mRNA levels. Free Rad. Biol. Med. 22, 901-908
62. Reif, D. W. (1992) Ferritin as a source of iron for oxidative damage. Free Rad. Biol. Med. 12, 417-427
63. 2+)-ATPase against iron-induced inhibition. Eur. J. Pharmacol. 290, 133-139