Heme oxygenase: Who needs it?

Proceedings of the Society for Experimental Biology and Medicine

Volumn 222, Issue 3, 1999, Pages 299-305

  Galbraith, Richard ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; HEME; HEME OXYGENASE; IRON;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; BILIRUBIN METABOLISM; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; RAT;

ANIMALIA;

EID: 0032704339     PISSN: 00379727     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1525-1373.1999.d01-147.x     Document Type: Conference Paper

References (106)

1. Virchow R. Die pathologischen pigments. Arch Pathol Anat 1:379-486, 1847.
2. Mann FC, Sheard C, Bollman JL et al. The formation of bile pigment from hemoglobin. Am J Physiol 76:306-315, 1926.
3. London IM, West K, Shemin D et al. On the origin of bile pigment in normal man. J Biol Chem 184:351-358, 1950.
4. Sjorstrand T. Endogenous formation of carbon monoxide in man under normal and pathological conditions. Scand J Clin Lab Invest 1:201-214, 1949.
5. Coburn RF, Williams WJ, White P et al. Production of carbon monoxide from hemoglobin in vivo. J Clin Invest 46:346-356, 1967.
6. Drabkin DL. The hemophagous organ of the placenta and in vivo studies of endogenous carbon monoxide production. Ann N Y Acad Sci 174:49-63, 1970.
7. Landaw SA, Callahan EW Jr., Schmid R. Catabolism of heme in vivo: Comparison of the simultaneous production of bilirubin and carbon monoxide. J Clin Invest 49:914-925, 1970.
8. White P. Carbon monoxide production and heme catabolism. Ann N Y Acad Sci 174:23-31, 1970.
9. Wise CD, Drabkin DL. Degradation of haemoglobin and hemin to biliverdin by a new cell-free system obtained from the hemophagous organ of dog placenta. Fed Proc 23:323, 1964.
10. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase: Characterization of the enzyme. J Biol Chem 244:6388-6394, 1969.
11. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of hemoglobin to bilirubin. Proc Natl Acad Sci U S A 61:748-755, 1968.
12. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of hemoglobin to bilirubin. Trans Assoc Am Phys 82:363-371, 1969.
13. Tenhunen R, Marver HS, Primstone NR et al. Enzymatic degradation of heme: Oxysensitive cleavage requiring cytochrome P-450. Biochemistry 11:1716-1720, 1972.
14. Maines MD, Kappas A. Cobalt induction of hepatic heme oxygenase, with evidence that cytochrome P-450 is not essential for this enzyme activity. Proc Natl Acad Sci U S A 71:4293-4297, 1974.
15. Maines MD, Kappas A. Cobalt stimulation of heme degradation in the liver: Dissociation of microsomal oxidation of heme from cytochrome P-450. J Biol Chem 250:4171-1177, 1975.
16. Yoshida T, Takahashi S, Kikuchi G. Partial purification and reconstitution of the heme oxygenase system from pig spleen microsomes. J Biochem (Tokyo) 75:1187-1191, 1974.
17. Maines MD. Heme oxygenase: Function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2:2557-2568, 1988.
18. Berk PD, Howe RB, Bloomer JR et al. Studies on bilirubin kinetics in normal adults. J Clin Invest 48:2176-2190, 1979.
19. Cavallui-Stahl E, Johnson GI, Lundh BA. A new method for the determination of microsomal heme oxygenases based on the quantitation of carbon monoxide formation. Scand J Clin Lab 38:69-76, 1978.
20. Vreman HJ, Stevenson D. Heme oxygenase activity as measured by carbon monoxide activity. Anal Biochem 168:31-38, 1998.
21. Tenhunen R. Method for microassay of microsomal heme oxygenase activity. Anal Biochem 45:600-607, 1972.
22. Sierra E, Nutter LA. Microassay for heme oxygenase activity using thin-layer chromotography. Anal Biochem 200:27-30, 1992.
23. Ryter S, Kvam E, Richman L et al. A chromatographic assay for heme oxygenase activity in cultured human cells: Application to artificial heme oxygenase overexpression. Free Radic Biol Med 24:959-971, 1998.
24. Ryter S, Kvam E, Tyrrell RM. Heme oxygenase activity determination by high-performance liquid chromatography. Oxidants Antioxidants 300:322-336, 1999.
25. Williams JF. Induction of tolerance in mice and rats to the effect of endotoxin to decrease the hepatic microsomal mixed-function oxidase system: Evidence for a possible macrophage-derived factor in the endotoxin effect. Int J Immunopharmacol 7:501-509, 1985.
26. McCoubrey WK Jr., Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247:725-732, 1997.
27. Cruse I, Maines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 263:3348-3353, 1988.
28. Maines MD. Characterization and regulation of heme oxygenase isozymes at the molecular level. In: Maines MD, Ed. Heme Oxygenase: Clinical Applications and Functions. Boca Raton, FL: CRC Press, pp109-144, 1999.
29. Muller RM, Taguchi H, Shibahara S. Nucleotide sequence and organization of the rat heme oxygenase gene. J Biol Chem 262:6795-6802, 1987.
30. Masuya Y, Hioki K, Tokunaga R et al. Involvement of the tyrosine phosphorylation pathway in induction of human heme oxygenase-1 by hemin, sodium arsenite, and cadmium chloride. J Biochem (Tokyo) 124:628-633, 1998.
31. Hartsfield CL, Alam J, Choi AM. Transcriptional regulation of the heme oxygenase 1 gene by pyrrolidine dithiocarbamate. FASEB J 12:1675-1682, 1998.
32. Camhi SL, Alam J, Wiegand GW et al. Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: Role of reactive oxygen intermediates and AP-1. Am J Respir Cell Mol Biol 18:226-234, 1998.
33. Oguro T, Hayashi M, Nakajo S, Numazawa S, Yoshida T. The expression of heme oxygenase-1 gene responded to oxidative stress produced by phorone, a glutathione depletor, in the rat liver; the relevance to activation of c-jun n-terminal kinase. J Pharmacol Exp Ther 287:773-778, 1998.
34. Immenschuh S, Kietzmann T, Hinke V et al. The rat heme oxygenase-1 gene is transcriptionally induced via the protein kinase a signaling pathway in rat hepatocyte cultures. Mol Pharmacol 53:483-491, 1998.
35. Elbirt KK, Whitmarsh AJ, Davis RJ et al. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. J Biol Chem 273:8922-8931, 1998.
36. Immenschuh S, Tan M, Ramadori G. Nitric oxide mediates the lipopolysaccharide-dependent upregulation of the heme oxygenase-1 gene expression in cultured rat Kupffer cells. J Hepatol 30:61-69, 1999.
37. Turcanu V, Dhouib M, Poindron P. Heme oxygenase inhibits nitric oxide synthase by degrading heme: A negative feedback regulation mechanism for nitric oxide production. Transplant Proc 30:4184-4185, 1998.
38. Schuller DJ, Wilks A, de Montellano PR et al. Crystallization of recombinant human heme oxygenase-1. Protein Sci 7:1836-1838, 1998.
39. Gibbs L, Willis D, Morgan MJ. The identification and expression of heme oxygenase-2 alternative transcripts in the mouse. Gene 221:171-177, 1998.
40. McCoubrey W, Huang TJ, Maines MD. Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 272:12568-12574, 1997.
41. Marks GS, Brian JF, Nakatsu K et al. Does carbon monoxide have a physiological function? Trends Pharmacol Sci 12:185-188, 1991.
42. Verma A, Hirsch DJ, Glatt CE et al. Carbon monoxide: A putative neural messenger. Science 259:381-384, 1993.
43. Maines MD. Carbon monoxide: An emerging regulator of cGMP in the brain. Mol Cell Neurosci 4:389-397, 1993.
44. Furchgott RF, Jothianandin S. Endothelium-dependent and -independent vasodilation involving cGMP: Relaxation induced by nitric oxide, carbon monoxide, and light. Blood Vessels 28:52-61, 1991.
45. Grundemar L, Johansson M-B, Ekelund M et al. Haem oxygenase activity in blood vessel homogenates as measured by carbon monoxide production. Acta Physiol Scand 153:203-204, 1995.
46. Kozma F, Johnson R, Chang F, et al. Contribution of endogenous carbon monoxide to regulation of diameter in resistance vessels. Am J Physiol 276:R1087-R1094, 1999.
47. Sammut IA, Foresti R, Clark JE et al. Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. Br J Pharmacol 125:1437-1444, 1998.
48. Motterlini R, Gonzales A, Foresti R et al. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ Res 83:568-577, 1998.
49. dos Santos EA, Yamaguishi GA, Heimann JC. Effect of the heme/ heme oxygenase pathway on the relationship between salt consumption and blood pressure. J Hypertens 16:1965-1969, 1998.
50. Thom SR, Fisher D, Xu YA et al. Role of nitric oxide-derived oxidants in vascular injury from carbon monoxide in the rat. Am J Physiol 276:H984-H992, 1999.
51. Silva CCS, Almeida VA, Haibara AS et al. Role of carbon monoxide in 1-glutamate-induced cardiovascular responses in nucleus tractus solitarius of conscious rats. Brain Res 824:147-152, 1999.
52. Pannen BH, Bauer M. Differential regulation of hepatic arterial and portal venous vascular resistance by nitric oxide and carbon monoxide in rats. Life Sci 62:2025-2033, 1998.
53. Pannen BH, Kohler N, Bauer M et al. Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J Clin Invest 102:1220-1228, 1998.
54. Goda N, Suzuki K, Naito M et al. Distribution of heme oxygenase isoforms in rat liver. J Clin Invest 101:604-612, 1998.
55. Durante W, Schafer A. Carbon monoxide and vascular cell function (review). Int J Mol Med 2:255-262, 1998.
56. Montecot C, Seylaz J, Pinard E. Carbon monoxide regulates cerebral blood flow in epileptic seizures but not in hypercapnia. Neuroreport 9:2341-2346, 1998.
57. Rich A, Farrugia G, Rae JL. Stimulation of a potassium current in rabbit corneal epithelium by carbon monoxide. Am J Physiol 267:C435-C442, 1994.
58. Maines MD, Eke BC, Weber CM et al. Corticosterone has a permissive effect on expression of heme oxygenase-1 in CA1-CA3 neurons of hippocampus in thermal-stressed rats. J Neurochem 64:1769-1779, 1995.
59. Stevens C, Wang Y. Reversal of long-term potentiation by inhibitors of haem oxygenase. Nature 364:147-149, 1993.
60. Zhuo M, Laitinen JT, Li X-C et al. On the respective roles of nitric oxide and carbon monoxide in long-term potentiation in the hippocampus. Learning Memory 5:467-480, 1998.
61. Zhuo M, Hu Y, Schulz C et al. Role of guanyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635-639, 1994.
62. Pozzoli G, Mancuso C, Mirtella A et al. Carbon monoxide as a novel neuroendocrine modulator: Inhibition of stimulated corticotropin-releasing hormone release from acute rat hypothalamic explants. Endocrinology 135:2314-2317, 1994.
63. Snyder SH, Jaffrey SR, Zakhary R. Nitric oxide and carbon monoxide: Parallel roles as neural messengers. Brain Res Rev 26:167-175, 1998.
64. Farrugia G, Miller SM, Rich A et al. Distribution of heme oxygenase and effects of exogenous carbon monoxide in canine jejunum. Am J Physiol 274:G350-G358, 1998.
65. Miller SM, Farrugia G, Schmalz PF et al. Heme oxygenase-2 is present in interstitial cell networks of the mouse small intestine. Gastroenterology 114:239-244, 1998.
66. Hu Y, Yang M, Ma N et al. Contribution of carbon monoxide-producing cells in the gastric mucosa of rat and monkey. Histochem Cell Biol 109:369-373, 1998.
67. Odrcich MJ, Graham CH, Kimura KA et al. Heme oxygenase and nitric oxide synthase in the placenta of the guinea pig during gestation. Placenta 19:509-516, 1998.
68. Acevedo CH, Ahmed A. Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy. J Clin Invest 101:949-955, 1998.
69. Hu Y, Ma N, Yang M et al. Expression and distribution of heme oxygenase-2 mRNA and protein in rat kidney. J Histochem Cytochem 46:249-256, 1998.
70. Henningsson R, Alm P, Ekstrom P et al. Heme oxygenase and carbon monoxide: Regulatory roles in islet hormone release. A biochemical, immunohistochemical, and confocal microscopic study. Diabetes 48:66-76, 1999.
71. Horvath I, Donnelly LE, Kiss A et al. Raised levels of exhaled carbon monoxide are associated with an increased expression of heme oxygenase-1 in airway macrophages in asthma: A new marker of oxidative stress. Thorax 53:668-672, 1998.
72. Horvath I, Loukides S, Wodehouse T et al. Increased levels of exhaled carbon monoxide in bronchiectasis. Thorax 53:867-870, 1998.
73. Turcanu V, Dhouib M, Gendrault J-L et al. Carbon monoxide induces murine thymocyte apoptosis by a free radical-mediated mechanism. Cell Biol Toxicol 14:47-54, 1998.
74. Vreman HJ, Wong RJ, Sanesi CA et al. Simultaneous production of carbon monoxide and thiobarbituric acid reactive substances in rat tissue preparations by an iron-ascorbate system. Can J Physiol Pharmacol 76:1057-1065, 1999.
75. Stocker R, Yamamoto Y, McDonagh AF et al. Bilirubin is an antioxidant of possible physiologic importance. Science 235:1043-1046, 1987.
76. Applegate LA, Noel A, Vile G et al. Two genes contribute to different extents to the heme oxygenase enzyme activity measured in cultured human skin fibroblasts and keratinocytes: Implications for protection against oxidant stress. Photochem Photobiol 61:285-291, 1995.
77. Rizzardini M, Carelli M, Cabello Porras MR et al. Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: Synergism by glutathione depletion and protection by N-acetylcysteine. Biochem J 304:477-483, 1994.
78. Ito K, Ikeda S, Shibata T et al. Immunohistochemical analysis of heme oxygenase-1 in rat liver after ischemia. Biochem Mol Biol Int 43:551-556, 1997.
79. Mosley K, Wembridge DE, Cattell V et al. Heme oxygenase is induced in nephrotoxic nephritis and hemin, a stimulator of heme oxygenase synthesis, ameliorates disease. Kidney Int 53:672-678, 1998.
80. Dennery PA, Sridhar KJ, Lee SC et al. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. J Biol Chem 272:14937-14942, 1997.
81. Minetti M, Mallozz C, Di Stasi AM et al. Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma. Arch Biochem Biophys 352:165-174, 1998.
82. Borger DR, Essig DA. Induction of HSP 32 gene in hypoxic cardiomyocytes is attenuated by treatment in N-acetyl-1-cysteine. Am J Physiol 274:H965-H973, 1998.
83. Wang L, Lee T-S, Lee F-Y et al. Expression of heme oxygenase-1 in atherosclerotic lesions. Am J Pathol 152:711-720, 1998.
84. Terry CM, Clikeman JA, Hoidan JR et al. Effect of tumor necrosis factor-α and interleukin-1α on heme oxygenase-1 expression in human endothelial cells. Am J Physiol 274:H883-H891, 1998.
85. Dwyer BE, Lu S-Y, Laitinen JT et al. Protective properties of tin- and manganese-centered porphyrins against hydrogen peroxide-mediated injury in rat astroglial cells. J Neurochem 71:2497-2504, 1998.
86. Matsuoka Y, Kitamura Y, Okazaki M et al. Induction of heme oxygenase-1 and major histocompatibility complex antigens in transient forebrain ischemia. J Cereb Blood Flow Metab 18:824-832, 1998.
87. Takeda A, Onodera H, Sugimoto A et al. Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia. Brain Res 666:120-124, 1994.
88. Takizawa S, Hirabayashi H, Matsushima K et al. Induction of heme oxygenase protein protects neurons in cortex and striatum, but not in hippocampus, against transient forebrain ischemia. J Cereb Blood Flow Metab 18:559-569, 1998.
89. Dore S, Takahashi M, Ferris C et al. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A 96:2445-2450, 1999.
90. Suttner DM, Sridhar K, Lee CS et al. Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells. Am J Physiol 276:L443-L451, 1999.
91. Otterbein LE, Kolls JK, Nantell LL et al. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest 103:1047-1054, 1999.
92. Panahian N, Yoshiura M, Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72:1187-1203, 1999.
93. Soares MP, Lin Y, Anrather J et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 4:1073-1077, 1998.
94. Yet S-F, Perrella MA, Layne MD et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest 103:R23-R29, 1999.
95. Yachie A, Niida Y, Wada T et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 103:129-135, 1999.
96. Mireles LC, Lum MA, Dennery PA. Antioxidant and cytotoxic effects of bilirubin on neonatal erythrocytes. Pediatr Res 45:355-362, 1999.
97. Lin F, Girotti A. Hemin-enhanced resistance of human leukemia cells to oxidative killing: Antisense determination of ferritin involvement. Arch Biochem Biophys 352:51-58, 1998.
98. Applegate LA, Scaletta C, Panizzon R et al. Evidence that ferritin is UV inducible in human skin: Part of a putative defense mechanism. J Invest Dermatol 111:159-163, 1998.
99. Eisenstein RS, Blemings KP. Iron regulatory proteins, iron responsive elements, and iron homeostasis. J Nutr 128:2295-2298, 1998.
100. Pantopoulos K, Hentze MW. Activation of iron regulatory protein-1 by oxidative stress in vitro. Proc Natl Acad Sci U S A 95:10559-10563, 1998.
101. Fogg S, Agarwal A, Nick HS et al. Iron regulates hyperoxia-dependent human heme oxygenase-1 gene expression in pulmonary endothelial cells. Am J Respir Cell Mol Biol 20:797-804, 1999.
102. Dennery PA, Spitz DR, Yang G et al. Oxygen toxicity and iron accumulation in the lungs of mice lacking heme oxygenase-2. J Clin Invest 101:1001-1011, 1998.
103. Braun V. Regulation of iron uptake minimizes iron-mediated oxidative stress. J Biosci 23:483-489, 1998.
104. Malorni W, Testa U, Rainaldi G et al. Oxidative stress leads to a rapid alteration of transferrin receptor intravesicular trafficking. Exp Cell Res 241:102-116, 1998.
105. 2+-mediated Fenton reactions has possible biological implications. J Biol Chem 274:962-971, 1998.
106. Baxter PJ, Garton K, Kharasch ED. Mechanistic aspects of carbon monoxide formation from volatile anesthetics. Anesthesiology 89:929-941, 1998.