Haem oxygenase-1 prevents cell death by regulating cellular iron

Nature Cell Biology

Volumn 1, Issue 3, 1999, Pages 152-157

  Ferris, Christopher D ^a   Jaffrey, Samie R ^a   Sawa, Akira ^a   Takahashi, Masaaki ^a   Brady, Stephen D ^a   Barrow, Roxanne K ^a   Tysoe, Steven A ^b   Wolosker, Herman ^a   Barañano, David E ^a   Doré, Sylvain ^a   Poss, Kenneth D ^c   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SKIDMORE COLLEGE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; HEME OXYGENASE; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; HMOX1 PROTEIN, MOUSE; IRON; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; STAUROSPORINE;

ANIMAL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL LINE; CELL SURVIVAL; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; FIBROBLAST; GENE DELETION; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; MOLECULAR CLONING; MOUSE; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SKIN;

ANIMALS; APOPTOSIS; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CLONING, MOLECULAR; CULTURE MEDIA, SERUM-FREE; ETOPOSIDE; FIBROBLASTS; GENE DELETION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; IRON; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; RECOMBINANT PROTEINS; SKIN; STAUROSPORINE; TRANSFECTION;

EID: 0033161957     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/11072     Document Type: Article

References (40)

1. Lindquist, S. & Craig, E. A. The heat-shock proteins. Annu. Rev. Genet. 22, 631-677 (1988).
2. Lindquist, S. The heat-shock response. Annu. Rev. Biochem. 55, 1151-1191 (1986).
3. Hard, F. U. Molecular chaperones in cellular protein folding. Nature 381, 571-579 (1996).
4. Bukau, B. & Horwich, A. L. The Hsp60 and Hsp60 chaperone machines. Cell 92, 351-366 (1998).
5. Wu, C. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441-469 (1995).
6. Camhi, S. L., Alam, J., Otterbein, L., Sylvester, S. L. & Choi, A. M. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am. J. Resp. Cell Mol. Biol. 13, 387-398 (1995).
7. Choi, A. M. & Alam, J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Resp. Cell Mol. Biol. 15, 9-19 (1996).
8. Levinson, W., Oppermann, H. & Jackson, J. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim. Biophys. Acta 606, 170-180 (1980).
9. Keyse, S. M. & Tyrrell, R. M. 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, 99-103 (1989).
10. Maines, M. D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2, 2557-2568 (1988).
11. Maines, M. D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554 (1997).
12. Yoshinaga, T., Sassa, S. & Kappas, A. The occurrence of molecular interactions among NADPH-cytochrome c reductase, heme oxygenase, and biliverdin reductase in heme degradation. J. Biol. Chem. 257, 7786-7793 (1982).
13. Farinelli, S. E., Greene, L. A. & Friedman, W. J. Neuroprotective actions of dipyridamole on cultured CNS neurons. J. Neurosci. 18, 5112-5123 (1998).
14. Kroemer, G., Dallaporta, B. & Resche-Rigon, M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60, 619-642 (1998).
15. Green, D. R. & Reed, J. C. Mitochondria and apoptosis. Science 281, 1309-1312 (1998).
16. Ankarcrona, M. et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973 (1995).
17. Trakshel, G. M., Kutty, R. K. & Maines, M. D. Cadmium-mediated inhibition of testicular heme oxygenase activity: the role of NADPH-cytochrome c (P-450) reductase. Arch. Biochem. Biophys. 251, 175-187 (1986).
18. Poss, K. D. & Tonegawa, S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl Acad. Sci. USA 94, 10919-10924 (1997).
19. Mukhopadhyay, C. K., Mazumder, B., Lindley, P. F. & Fox, P. L. Identification of the prooxidant site of human ceruloplasmin: a model for oxidative damage by copper bound to protein surfaces. Proc. Natl Acad. Sci. USA 94, 11546-11551 (1997).
20. Ponka, P., Beaumont, C. & Richardson, D. R. Function and regulation of transferrin and ferritin. Semin. Hematol. 35, 35-54 (1998).
21. Eisenstein, R. S., Garcia-Mayol, D., Pettingell, W. & Munro, H. N. Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron. Proc. Natl Acad. Sci. USA 88, 688-692 (1991).
22. Zakhary, R. et al. Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc. Natl Acad. Sci. USA 93, 795-798 (1996).
23. McCord, J. M. Iron, free radicals, and oxidative injury. Semin. Hematol 35, 5-12 (1998).
24. Meneghini, R. Iron homeostasis, oxidative stress, and DNA damage. Free Rad. Biol. Med. 23, 783-792 (1997).
25. Gunshin, H. et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488 (1997).
26. Umbreit, J. N., Conrad, M. E., Moore, E. G. & Latour, L F. Iron absorption and cellular transport: the mobilferrin/paraferritin paradigm. Semin. Hematol. 35, 13-26 (1998).
27. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D. & Dancis, A. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271, 1552-1557 (1996).
28. Conrad, M. E. Introduction: iron overloading disorders and iron regulation. Semin. Hematol. 35, 1-4 (1998).
29. Bothwell, T. H., Charlton, R.W. & Motulsky, A.G. in The Metabolic and Molecular Basis of Inherited Disease (eds Scriver, C. R., Beaudet, A.L., Sly, W.S. & Valle, D.) 2237-2269 (McGraw-Hill, New York, 1995).
30. Tenhunen, R., Marver, H. S. & Schmid, R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl Acad. Sci. USA 61, 748-755 (1968).
31. Tenhunen, R., Marver, H. S. & Schmid, R. The enzymatic conversion of hemoglobin to bilirubin. Trans. Assoc. Am. Physicians 82, 363-371 (1909).
32. Baranano, D. et al. Identification and characterization of an iron transporting ATPase. Gastroenterol. 116, A1183 (1999).
33. Soares, M. P. et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nature Med. 4, 1073-1077 (1998).
34. Verma, A., Hirsch, D. J., Glatt, C E., Ronnett, G. V. & Snyder, S. H. Carbon monoxide: a putative neural messenger. Science 259, 381-384 (1993).
35. Zakhary, R. et al. Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide. Proc. Natl Acad. Sci. USA 94, 14848-14853 (1997).
36. Miller, S. M. et al. Heme oxygenase 2 is present in interstitial cell networks of the mouse small intestine. Gastroenterol. 114, 239-244 (1998).
37. Dennery, P. A. et al. Oxygen toxicity and iron accumulation in the lungs of mice lacking heme oxygenase-2. J. Clin. Invest. 101, 1001-1011 (1998).
38. McCoubrey, W. K. Jr, Huang, T. J. & Maines, M. D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 247, 725-732 (1997).
39. Bredt, D. S., Ferris, C D. & Snyder, S. H. Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 267, 10976-10981 (1992).
40. Hockenbery, D., Nunez, G., Milliman, C, Schreiber, R. D. & Korsmeyer, S. J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348, 334-336 (1990).