Heme oxygenase-1: Unleashing the protective properties of heme

Trends in Immunology

Volumn 24, Issue 8, 2003, Pages 449-455

  Otterbein, Leo E ^a   Soares, Miguel P ^b,c   Yamashita, Kenichiro ^b   Bach, Fritz H ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; HEME OXYGENASE 1; INTERLEUKIN 10; IRON BINDING PROTEIN; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN;

ALLOGRAFT; GENE ACTIVITY; GRAFT SURVIVAL; HUMAN; ISCHEMIA; NEUROPROTECTION; NONHUMAN; REPERFUSION INJURY; REVIEW; XENOGRAFT;

EID: 0043268709     PISSN: 14714906     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1471-4906(03)00181-9     Document Type: Review

References (60)

1. Brouard S., et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 192:2000;1015-1026.
2. Lee P.J., et al. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc. Natl. Acad. Sci. U. S. A. 93:1996;10393-10398.
3. Peyton K.J., et al. Heme oxygenase-1-derived carbon monoxide is an autocrine inhibitor of vascular smooth muscle cell growth. Blood. 99:2002;4443-4448.
4. Tobiasch E., et al. Heme oxygenase-1 protects pancreatic beta cells from apoptosis caused by various stimuli. J. Invest. Med. 49:2001;566-571.
5. Tenhunen R., et al. The enzymatic catabolism of hemoglobin stimulation of microsomal heme oxygenase by hemin. J. Lab. Clin. Med. 75:1970;410-421.
6. Soares M.P., et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat. Med. 4:1998;1073-1077.
7. Sato K., et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol. 166:2001;4185-4194.
8. Otterbein L.E., et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:2000;422-428.
9. Singleton J.W., Laster L. Biliverdin reductase of guinea pig liver. J. Biol. Chem. 240:1965;4780-4789.
10. O'Carra P., Colleran E. Properties and kinetics of biliverdin reductase. Biochem. J. 125:1971;110P.
11. Stocker R., et al. Bilirubin is an antioxidant of possible physiological importance. Science. 235:1987;1043-1046.
12. Baranano D.E., et al. Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. U. S. A. 99:2002;16093-16098.
13. Ferris C.D., et al. Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1:1999;152-157.
14. Balla G., et al. Ferritin: a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem. 267:1992;18148-18153.
15. Willis D., et al. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat. Med. 2:1996;87-90.
16. Nath K.A., et al. Induction of heme oxygenase is a rapid, protective response I in rhabdomyolysis in the rat. J. Clin. Invest. 90:1992;267-270.
17. Poss K.D., Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. U. S. A. 94:1997;10919-10924.
18. Yachie A., et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103:1999;129-135.
19. Minamino T., et al. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 98:2001;8798-8803.
20. Yet S.F., et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ. Res. 89:2001;168-173.
21. Fujita T., et al. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 7:2001;598-604.
22. Otterbein L.E., et al. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J. Clin. Invest. 103:1999;1047-1054.
23. Lee T.S., Chau L.Y. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8:2002;240-246.
24. Vile G.F., et al. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 91:1994;2607-2610.
25. Gray C.P., et al. Heavy chain ferritin activates regulatory T cells by induction of changes in dendritic cells. Blood. 99:2002;3326-3334.
26. Nakagami T., et al. A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochim. Biophys. Acta. 1158:1993;189-193.
27. Chiu H., et al. Differential induction of heme oxygenase-1 in macrophages and hepatocytes during acetaminophen-induced hepatotoxicity in the rat: effects of hemin and biliverdin. Toxicol. Appl. Pharmacol. 181:2002;106-115.
28. Otterbein L.E., et al. Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol. 276:1999;L688-L694.
29. Sarady J.K., et al. Carbon monoxide modulates endotoxin-induced production of granulocyte macrophage colony-stimulating factor in macrophages. Am. J. Respir. Cell Mol. Biol. 27:2002;739-745.
30. Koyamada N. Transient complement inhibition plus T-cell immunosuppression induces long-term survival of mouse-to-rat cardiac xenografts. Transplantation. 65:1998;1210-1215.
31. Soares M.P., et al. Heme oxygenase-1, a protective gene that prevents the rejection of transplanted organs. Immunol. Rev. 184:2001;275-285.
32. Soares M.P., et al. Accomodation. Immunol. Today. 20:1999;434-437.
33. Beutler B., et al. Identity of tumour necrosis factor and the macrophage-secreted factor cachectin. Nature. 316:1985;552-554.
34. Gerard C., et al. Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177:1993;547-550.
35. Brune B., Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32:1987;497-504.
36. Brouard S., et al. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-κB to protect endothelial cells from tumor necrosis factor-α-mediated apoptosis. J. Biol. Chem. 277:2002;17950-17961.
37. Petrache I., et al. Heme oxygenase-1 inhibits TNF-α-induced apoptosis in cultured fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:2000;L312-L319.
38. Gunther L., et al. Carbon monoxide protects pancreatic β-cells from apoptosis and improves islet function and survival after transplantation. Diabetes. 51:2002;994-999.
39. Bombeli T., et al. Endothelial cells undergoing apoptosis become pro-adhesive for non-activated platelets. Blood. 93:1999;3831-3838.
40. Otterbein L.E., et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat. Med. 9:2003;183-190.
41. Bouche D., et al. Inhibition of graft arteriosclerosis development in rat aortas following heme oxygenase-1 gene transfer. Transplant. Immunol. 9:2002;235-238.
42. Motterlini R., et al. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ. Res. 90:2002;E17-E24.
43. Dioum E.M., et al. NPAS2: a gas-responsive transcription factor. Science. 298:2002;2385-2387.
44. Stevenson T.H., et al. Kinetics of CO binding to the haem domain of murine inducible nitric oxide synthase: differential effects of haem domain ligands. Biochem. J. 358:2001;201-208.
45. Foresti R., et al. Role of heme oxygenase-1 in hypoxia-reoxygenation: requirement of substrate heme to promote cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 281:2001;H1976-H1984.
46. Clark J., et al. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am. J. Physiol. Heart Circ. Physiol. 278:2000;H643-H651.
47. Tessner T.G., et al. Prostaglandins prevent decreased epithelial cell proliferation associated with dextran sodium sulfate injury in mice. Gastroenterology. 115:1998;874-882.
48. DeBruyne L.A., et al. Gene transfer of immunomodulatory peptides correlates with heme oxygenase-1 induction and enhanced allograft survival. Transplantation. 69:2000;120-128.
49. Taylor J.L., et al. Lung-specific induction of heme oxygenase-1 and hyperoxic lung injury. Am. J. Physiol. 274:1998;L582-L590.
50. Otterbein L.E., et al. Mechanism of hemoglobin-induced protection against endotoxemia in rats: a ferritin-independent pathway. Am. J. Physiol. 272:1997;L268-L275.
51. Moore B.A., et al. Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology. 124:2003;377-391.
52. Kimpara T., et al. Microsatellite polymorphism in the human heme oxygenase-1 gene promotor and its application in association studies with Alzheimer and Parkinson disease. Hum. Genet. 100:1997;145-147.
53. Exner M., et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty. J. Endovasc. Ther. 8:2001;433-440.
54. Visner G.A., et al. Rapamycin induces heme oxygenase-1 in human pulmonary vascular cells: implications in the antiproliferative response to rapamycin. Circulation. 107:2003;911-916.
55. Mandrekar P., et al. Human monocyte IL-10 production is increased by acute ethanol treatment. Cytokine. 8:1996;567-577.
56. Szabo G., et al. Inhibition of superantigen-induced T cell proliferation and monocyte IL-1β, TNF-α, and IL-6 production by acute ethanol treatment. J. Leukocyte Biol. 58:1995;342-351.
57. Mukamal K.J., et al. Prior alcohol consumption and mortality following acute myocardial infarction. J. Am. Med. Assoc. 285:2001;1965-1970.
58. Lee T.S., et al. Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta 12,14-prostaglandin J2. J. Biol. Chem. 278:2003;19325-19330.
59. Redaelli C.A., et al. Extended preservation of rat liver graft by induction of heme oxygenase-1. Hepatology. 35:2002;1082-1089.
60. Motterlini R., et al. Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic. Biol. Med. 28:2000;1303-1312.