Development of vascular biology over the past 10 years: Heme oxygenase-1 in cardiovascular homeostasis

Journal of Endovascular Therapy

Volumn 11, Issue SUPPL. 2, 2004, Pages

  Ohta, Kunio ^a   Yachie, Akihiro ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Antioxidants; Antiproliferative mechanisms; Atherosclerosis; Carbon monoxide; Heme oxygenase 1; Hemostasis; Inflammation; Lymphocyte migration; Platelet aggregation; T cells; Thrombus; Vascular endothelial growth factor; Vascular smooth muscle cells

Indexed keywords

ANTIOXIDANT; CARBON DIOXIDE; CYTOKINE; HEME OXYGENASE 1; LOW DENSITY LIPOPROTEIN; VASODILATOR AGENT;

APOPTOSIS; ATHEROGENESIS; BLOOD VESSEL TONE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CELL DEATH; CELL PROLIFERATION; CYTOKINE RELEASE; ENDOTHELIUM CELL; GENE EXPRESSION; HISTORY OF MEDICINE; HOMEOSTASIS; HUMAN; LEUKOCYTE MIGRATION; MITOGENESIS; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; TISSUE INJURY;

EID: 12144273503     PISSN: 15266028     EISSN: None     Source Type: Journal    
DOI: 10.1583/04-1330.1     Document Type: Review

References (76)

1. Ross R, Glomset JA. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science. 1973;180:1332-1339.
2. Jeney V, Balla J, Yachie A, et al. Pro-oxidant and cytotoxic effects of circulating heme. Blood. 2002;100:879-887.
3. Motterlini R, Clark JE, Foresti R, et al. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res. 2002;90:E17-E24.
4. Balla J, Vercellotti GM, Nath K, et al. Haem, haem oxygenase and ferritin in vascular endothelial cell injury. Nephrol Dial Transplant. 2003;18(Suppl 5):v8-v12.
5. Ohta K, Yachie A. Role of heme oxygenase-1 in cardiovascular diseases: a novel target for molecular intervention? J Endovasc Ther. 2001;8:444-446.
6. Shibahara S, Yoshida T, Kikuchi G. Induction of heme oxygenase by hemin in cultured pig alveolar macrophages. Arch Biochem Biophys. 1978;188:243-250.
7. Murphy BJ, Laderoute KR, Short SM, et al. The identification of heme oxygenase as a major hypoxic stress protein in Chinese hamster ovary cells. Br J Cancer. 1991;64:69-73.
8. Ewing JF, Maines MD. Rapid induction of heme oxygenase 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc Natl Acad Sci USA. 1991;88:5364-5368.
9. Taketani S, Kohno H, Yoshinaga T, et al. Induction of heme oxygenase in rat hepatoma cells by exposure to heavy metals and hyperthermia. Biochem Int. 1988;17:665-672.
10. Siow RC, Ishii T, Sato H, et al. Induction of the antioxidant stress proteins heme oxygenase-1 and MSP23 by stress agents and oxidised LDL in cultured vascular smooth muscle cells. FEBS Lett. 1995;368:239-242.
11. Rizzardini M, Terao M, Falciani F, et al. Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene. Biochem J. 1993;290:343-347.
12. Kutty RK, Nagineni CN, Kutty G, et al. Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor-beta. J Cell Physiol. 1994;159:371-378.
13. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem. 1997;247:725-732.
14. Yachie A, Niida Y, Wada T, et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103:129-135.
15. Kawashima A, Oda Y, Yachie A, et al. Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol. 2002;33:125-130.
16. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA. 1997;94:10919-10924.
17. Ohta K, Yachie A, Fujimoto K, et al. Tubular injury as a cardinal pathologic feature in human heme oxygenase-1 deficiency. Am J Kidney Dis. 2000;35:863-870.
18. Yang Y, Ohta K, Shimizu M, et al. Selective protection of renal tubular epithelial cells by heme oxygenase (HO)-1 during stress-induced injury. Kidney Int. 2003;64:1302-1309.
19. Morita T, Perrella MA, Lee ME, et al. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA. 1995;92:1475-1479.
20. Christodoulides N, Durante W, Kroll MH, et al. Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation. 1995;91:2306-2309.
21. Peyton KJ, Reyna SV, Chapman GB, et al. Heme oxygenase-1-derived carbon monoxide is an autocrine inhibitor of vascular smooth muscle cell growth. Blood. 2002;99:4443-4448.
22. Togane Y, Morita T, Suematsu M, et al. Protective roles of endogenous carbon monoxide in neointimal development elicited by arterial injury. Am J Physiol Heart Circ Physiol. 2000;278:H623-H632.
23. Durante W, Peyton KJ, Schafer AI. Platelet-derived growth factor stimulates heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1999;19:2666-2672.
24. Morita T, Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest. 1995;96:2676-2682.
25. Duckers HJ, Boehm M, True AL, et al. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med. 2001;7:693-698.
26. Chauveau C, Bouchet D, Roussel JC, et al. Gene transfer of heme oxygenase-1 and carbon monoxide delivery inhibit chronic rejection. Am J Transplant. 2002;2:581-592.
27. Minamino T, Christou H, Hsieh CM, et al. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci USA. 2001;98:8798-8803.
28. Pae HO, Oh GS, Choi BM, et al. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. J Immunol. 2004;172:4744-4751.
29. Song R, Mahidhara RS, Zhou Z, et al. Carbon monoxide inhibits T lymphocyte proliferation via caspase-dependent pathway. J Immunol. 2004;172:1220-1226.
30. Morita T, Mitsialis SA, Koike H, et al. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem. 1997;272:32804-32809.
31. Li Volti G, Wang J, Traganos F, et al. Differential effect of heme oxygenase-1 in endothelial and smooth muscle cell cycle progression. Biochem Biophys Res Commun. 2002;296:1077-1082.
32. Zhang X, Bedard EL, Potter R, et al. Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury. Am J Physiol Lung Cell Mol Physiol. 2002;283:L815-L829.
33. Abraham NG, Kushida T, McClung J, et al. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res. 2003; 93:507-514.
34. Deramaudt BM, Braunstein S, Remy P, et al. Gene transfer of human heme oxygenase into coronary endothelial cells potentially promotes angiogenesis. J Cell Biochem. 1998;68:121-127.
35. Bussolati B, Ahmed A, Pemberton H, et al. Bifunctional role for VEGF-induced heme oxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood. 2004;103:761-766.
36. Dulak J, Jozkowicz A, Foresti R, et al. Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal. 2002;4:229-240.
37. Wagner CT, Durante W, Christodoulides N, et al. Hemodynamic forces induce the expression of heme oxygenase in cultured vascular smooth muscle cells. J Clin Invest. 1997;100: 589-596.
38. Sato K, Balla J, Otterbein L, et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J Immunol. 2001;166:4185-4194.
39. Lindenblatt N, Bordel R, Schareck W, et al. Vascular heme oxygenase-1 induction suppresses microvascular thrombus formation in vivo. Arterioscler Thromb Vasc Biol. 2004;24:601-606.
40. Otterbein LE, Bach FH, Alam J, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000;6:422-428.
41. Kushida T, Li Volti G, Quan S, et al. Role of human heme oxygenase-1 in attenuating TNF-alpha-mediated inflammation injury in endothelial cells. J Cell Biochem. 2002;87:377-385.
42. Ishikawa K, Navab M, Leitinger N, et al. Induction of heme oxygenase-1 inhibits the monocvte transmigration induced by mildly oxidized LDL J Clin Invest. 1997;100:1209-1216.
43. Hayashi S, Takamiya R, Yamaguchi T, et al. Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res. 1999;85:663-671.
44. Soares MP, Seldon MP, Gregoire IP, et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol. 2004;172:3553-3563.
45. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA. 1997;94:10925-10930.
46. Soares MP, Lin Y, Anrather J, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med. 1998;4:1073-1077.
47. Zhang X, Shan P, Otterbein LE, et al. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem. 2003;278:1248-1258.
48. Yet SF, Perrella MA, Layne MD, et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest. 1999;103:R23-R29.
49. Tulis DA, Durante W, Liu X, et al. Adenovirus-mediated heme oxygenase-1 gene delivery inhibits injury-induced vascular neointima formation. Circulation. 2001;104:2710-2715.
50. Tulis DA, Durante W, Peyton KJ, et al. Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries. Atherosclerosis. 2001;155:113-122.
51. Brouard S, Otterbein LE, Anrather J, et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 2000;192:1015-1026.
52. Liu XM, Chapman GB, Peyton KJ, et al. Carbon monoxide inhibits apoptosis in vascular smooth muscle cells. Cardiovasc Res. 2002;55: 396-405.
53. Yachie A, Toma T, Mizuno K, et al. Heme oxygenase-1 production by peripheral blood monocytes during acute inflammatory illnesses of children. Exp Biol Med (Maywood). 2003; 228:550-556.
54. Liu XM, Chapman GB, Wang H, et al. Adenovirus-mediated heme oxygenase-1 gene expression stimulates apoptosis in vascular smooth muscle cells. Circulation. 2002;105:79-84.
55. Maruhashi K, Kasahara Y, Ohta K, et al. Paradoxical enhancement of oxidative cell injury by overexpression of heme oxygenase-1 in an anchorage-dependent cell ECV304. J Cell Biochem. 2004;93:552.
56. Naik JS, Walker BR. Heme oxygenase-mediated vasodilation involves vascular smooth mus-cle cell hyperpolarization. Am J Physiol Heart Circ Physiol. 2003;285:H220-H228.
57. Durante W, Kroll MH, Christodoulides N, et al. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res. 1997;80:557-564.
58. Hartsfield CL, Alam J, Cook JL, et al. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol. 1997;273:L980-L988.
59. Imai T, Morita T, Shindo T, et al. Vascular smooth muscle cell-directed overexpression of heme oxygenase-1 elevates blood pressure through attenuation of nitric oxide-induced vasodilation in mice. Circ Res. 2001;89:55-62.
60. Wang LJ, Lee TS, Lee FY, et al. Expression of heme oxygenase-1 in atherosclerotic lesions. Am J Pathol. 1998;152:711-720.
61. Nakahashi TK, Hoshina K, Tsao PS, et al. Flow loading induces macrophage antioxidative gene expression in experimental aneurysms. Arterioscler Thromb Vasc Biol. 2002;22:2017-2022.
62. Yet SF, Layne MD, Liu X, et al. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003;17:1759-1761.
63. Ishikawa K, Sugawara D, Wang XP, et al. Heme oxygenase-1 inhibits atherosclerotic lesion formation in LDL-receptor knockout mice. Circ Res. 2001;88:506-512.
64. Otterbein LE, Zuckerbraun BS, Haga M, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med. 2003;9:183-190.
65. Yamashita K, McDaid J, Ollinger R, et al. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J. 2004;18:765-767.
66. Philippidis P, Mason JC, Evans BJ, et al. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ Res. 2004;94:119-126.
67. Exner M, Schillinger M, Minar E, et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty. J Endovasc Ther. 2001;8:433-440.
68. Chen YH, Chau LY, Lin MW, et al. Heme oxygenase-1 gene promotor microsatellite polymorphism is associated with angiographic restenosis after coronary stenting. Eur Heart J. 2004;25:39-47.
69. Schillinger M, Exner M, Minar E, et al. Heme oxygenase-1 genotype and restenosis after balloon angioplasty: a novel vascular protective factor. J Am Coll Cardiol. 2004;43:950-957.
70. Kaneda H, Ohno M, Taguchi J, et al. Heme oxygenase-1 gene promoter polymorphism is associated with coronary artery disease in Japanese patients with coronary risk factors. Arterioscler Thromb Vasc Biol. 2002;22:1680-1685.
71. Ono K, Goto Y, Takagi S, et al. A promoter variant of the heme oxygenase-1 gene may reduce the incidence of ischemic heart disease in Japanese. Atherosclerosis. 2004;173:315-319.
72. Endler G, Exner M, Schillinger M, et al. A microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with increased bilirubin and HDL levels but not with coronary artery disease. Thromb Haemost. 2004;91:155-161.
73. Hirai H, Kubo H, Yamaya M, et al. Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines. Blood. 2003;102:1619-1621.
74. Visner GA, Lu F, Zhou H, et al. Rapamycin induces heme oxygenase-1 in human pulmonary vascular cells: implications in the antiproliferative response to rapamycin. Circulation. 2003; 107:911-916.
75. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8:240-246.
76. Tang YL, Tang Y, Zhang YC, et al. Protection from ischemic heart injury by a vigilant heme oxygenase-1 plasmid system. Hypertension. 2004;43:746-751.