Resistance to hyperoxia with heme oxygenase-1 disruption: Role of iron

Free Radical Biology and Medicine

Volumn 34, Issue 1, 2003, Pages 124-133

  Dennery, Phyllis A ^a   Visner, Gary ^b   Weng, Yi Hao ^a   Nguyen, Xuandai ^a   Lu, Fuhua ^b   Zander, Dani ^c   Yang, Guang ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Free radicals; Knockout; Lung; NADPH cytochrome c P450 reductase; pPeroxidase; Reactive iron

Indexed keywords

CYTOCHROME; HEME; HEME OXYGENASE 1; HYDROGEN PEROXIDE; IRON; OXIDOREDUCTASE; PEROXIDASE; PROTOPORPHYRIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; GRAFT REJECTION; HYPEROXIA; HYPOXIA; INFLAMMATION; IRON METABOLISM; KNOCKOUT MOUSE; LUNG INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; HEME OXYGENASE (DECYCLIZING); HYPEROXIA; IRON; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SUBSTRATE SPECIFICITY;

EID: 12244304860     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(02)01295-9     Document Type: Article

References (47)

1. Keyse, S. M.; Applegate, L. A.; Tromvoukis, Y.; Tyrrell, R. M. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol. Cell. Biol. 10:4967-4969.
2. Abraham N.G., Lavrovsky Y., Schwartzman M.L., Stoltz R.A., Levere R.D., Gerritsen M.E., Shibahara S., Kappas A. 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.
3. Dennery P., Sridhar K., Lee C., Wong H., Shokoohi V., Rodgers P., Spitz D. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J. Biol. Chem. 272:1997;14937-14942.
4. Gutteridge J.M., Rowley D.A., Halliwell B. 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. 199:1981;263-265.
5. Suttner D.M., Dennery P.A. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J. 13:1999;1800-1808.
6. Dennery P.A., Yang G., Tatarov A., Lee C.S., Shegog M.L., Spitz D.R., Poss K.D. Lung oxidative injury in the absence of heme oxygenase-2 in mice. J. Clin. Invest. 101:1998;1001-1011.
7. Welty, S. E.; Rogers, L. K.; Tom, D. J.; McNaughton, K. J.; Geske, R. S.; DeMayo, F. J.; Smith, C. V. Hyperoxic lung injury is potentiated by SP-C promoter driven expression of an HO-1 transgene in mice. Am. Rev. Respir. Crit. Care Med. 159:A218 (abstract); 1999.
8. Weng Y.H., Tatarov A., Bartos B.P., Contag C.H., Dennery P.A. HO-1 expression in type II pneumocytes after transpulmonary gene delivery. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:2000;L1273-L1279.
9. Poss K.D., Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. USA. 94:1997;10919-10924.
10. Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103:1999;129-135.
11. Otterbein L.E., Mantell L.L., Choi A.M. Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol. 276:1999;L688-L694.
12. Yang F., Coalson J.J., Bobb H.H., Carter J.D., Banu J., Ghio A.J. Resistance of hypotransferrinemic mice to hyperoxia-induced lung injury. Am. J. Physiol. 277:1999;L1214-L1223.
13. Ryan T.P., Krzesicki R.F., Blakeman D.P., Chin J.E., Griffin R.L., Richards I.M., Aust S.D., Petry T.W. Pulmonary ferritin differential effects of hyperoxic lung injury on subunit mRNA levels. Free Radic. Biol. Med. 22:1997;901-908.
14. Griendling K.K., Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept. 91:2000;21-27.
15. Poss K.D., Thomas M.J., Ebralidze A.K., O'Dell T.J., Tonegawa S. Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron. 15:1995;867-873.
16. Kreiser D., Nguyen X., Wong R., Seidman D., Stevenson D., Quan S., Abraham N., Dennery P.A. Heme oxygenase-1 modulates fetal growth in the rat. Lab. Invest. 82:2002;687-692.
17. Vreman H.J., Rodgers P.A., Gale R., Stevenson D.K. Carbon monoxide excretion as an index of bilirubin production in rhesus monkeys. J. Med. Primatol. 18:1989;449-460.
18. Wilks A., Ortiz de Montellano P.R. Rat liver heme oxygenase. High level expression of a truncated soluble form and nature of the meso-hydroxylating species. J. Biol. Chem. 268:1993;22357-22362.
19. Smith M.A., Kutty R.K., Richey P.L., Yan S.D., Stern D., Chader G.J., Wiggert B., Petersen R.B., Perry G. Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am. J. Pathol. 145:1994;42-47.
20. Dennery P.A., Wong H.E., Sridhar K.J., Rodgers P.A., Sim J.E., Spitz D.R. Differences in basal and hyperoxia-associated HO expression in oxidant-resistant hamster fibroblasts. Am. J. Physiol. 271:1996;L672-L679.
21. Wright J.R., Colby H.D., Miles P.R. Cytosolic factors which affect microsomal lipid peroxidation in lung and liver. Arch. Biochem. Biophys. 206:1981;296-304.
22. Schacter E., Williams J.A., Lim M., Levine R.L. Differential susceptibility of plasma proteins to oxidative modification examination by western blot immunoassay. Free Radic. Biol. Med. 17:1994;429-437.
23. Lowry O., Rosebrough H., Farr A., Randall R. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:1951;265-272.
24. Lawrence R.A., Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71:1976;952-958.
25. 2 by catalase. J. Biol. Chem. 195:1952;133-140.
26. Aebi H. Catalase in vitro. Methods Enzymol. 105:1984;121-126.
27. Spitz D.R., Oberley L.W. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal. Biochem. 179:1989;8-18.
28. Dennery P.A., Rodgers P.A., Lum M.A., Jennings B.C., Shokoohi V. Hyperoxic regulation of lung heme oxygenase in neonatal rats. Pediatr. Res. 40:1996;815-821.
29. van Deursen C.T., van Dieijen-Visser M.P., Koudstaal J., Brombacher P.J. Determination of tissue iron and ferritin in liver pathology comparison of histochemical and biochemical results. J. Clin. Chem. Clin. Biochem. 27:1989;345-349.
30. Evans P.J., Halliwell B. Measurement of iron and copper in biological systems bleomycin and copper-phenanthroline assays. Methods Enzymol. 233:1994;82-92.
31. Griendling K.K., Minieri C.A., Ollerenshaw J.D., Alexander R.W. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74:1994;1141-1148.
32. Clerch L.B., Massaro D. Tolerance of rats to hyperoxia. Lung antioxidant enzyme gene expression. J. Clin. Invest. 91:1993;499-508.
33. 2 in angiotensin II-induced vascular hypertrophy. Hypertension. 32:1998;488-495.
34. Schipper H.M., Bernier L., Mehindate K., Frankel D. Mitochondrial iron sequestration in dopamine-challenged astroglia role of heme oxygenase-1 and the permeability transition pore. J. Neurochem. 72:1999;1802-1811.
35. Inoue S., Suzuki M., Nagashima Y., Suzuki S., Hashiba T., Tsuburai T., Ikehara K., Matsuse T., Ishigatsubo Y. Transfer of heme oxygenase 1 cDNA by a replication-deficient adenovirus enhances interleukin 10 production from alveolar macrophages that attenuates lipopolysaccharide-induced acute lung injury in mice. Hum. Gene Ther. 12:2001;967-979.
36. Ho Y.S., Magnenat J.L., Bronson R.T., Cao J., Gargano M., Sugawara M., Funk C.D. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J. Biol. Chem. 272:1997;16644-16651.
37. 2-resistant fibroblasts. Arch. Biochem. Biophys. 292:1992;221-227.
38. Frankel D., Mehindate K., Schipper H.M. Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively challenged astroglia. J. Cell. Physiol. 185:2000;80-86.
39. Miller R.A., Britigan B.E. Protease-cleaved iron-transferrin augments oxidant-mediated endothelial cell injury via hydroxyl radical formation. J. Clin. Invest. 95:1995;2491-2500.
40. Ushio-Fukai M., Zafari A.M., Fukui T., Ishizaka N., Griendling K.K. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J. Biol. Chem. 271:1996;23317-23321.
41. Emerson M.R., LeVine S.M. Heme oxygenase-1 and NADPH cytochrome P450 reductase expression in experimental allergic encephalomyelitis an expanded view of the stress response. J. Neurochem. 75:2000;2555-2562.
42. Johnston C.J., Wright T.W., Reed C.K., Finkelstein J.N. Comparison of adult and newborn pulmonary cytokine mRNA expression after hyperoxia. Exp. Lung Res. 23:1997;537-552.
43. Minamino T., Christou H., Hsieh C.M., Liu Y., Dhawan V., Abraham N.G., Perrella M.A., Mitsialis S.A., Kourembanas S. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc. Natl. Acad. Sci. USA. 98:2001;8798-8803.
44. Crowley M.R. Oxygen-induced pulmonary vasodilation is mediated by adenosine triphosphate in newborn lambs. J. Cardiovasc. Pharmacol. 30:1997;102-109.
45. Fineman J.R., Wong J., Soifer S.J. Hyperoxia and alkalosis produce pulmonary vasodilation independent of endothelium-derived nitric oxide in newborn lambs. Pediatr. Res. 33:1993;341-346.
46. Berg J.T., White J.E., Tsan M.F. Response of alveolar macrophage-depleted rats to hyperoxia. Exp. Lung Res. 21:1995;175-185.
47. Kinnula V.L., Chang L.Y., Ho Y.S., Crapo J.D. Hydrogen peroxide release from alveolar macrophages and alveolar type II cells during adaptation to hyperoxia in vivo. Exp. Lung Res. 18:1992;655-673.