The heme oxygenase system: A regulator of second messenger gases

Annual Review of Pharmacology and Toxicology

Volumn 37, Issue , 1997, Pages 517-554

  Maines, Mahin D ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

carbon monoxide generation; CO regulation of cGMP dependent activities; heme degradation; heme oxygenase 1 and 2; regulation of nitric oxide activity

Indexed keywords

CARBON MONOXIDE; CYCLIC GMP; HEME OXYGENASE; NITRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; CARDIOVASCULAR SYSTEM; IMMUNE SYSTEM; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; REVIEW; SECOND MESSENGER;

ANIMALIA;

EID: 0030923630     PISSN: 00664251     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.pharmtox.37.1.517     Document Type: Review

References (213)

1. Maines MD. 1993. Carbon monoxide: An emerging regulator of cGMP in the brain. Mol. Cell. Neurosci. 4:389-97
2. Maines MD, Kappas A. 1974. Cobalt induction of hepatic heme oxygenase: with evidence that Cyt P450 is not essential for this enzyme activity. Proc. Natl. Acad. Sci. USA 71:4293-97
3. Maines MD, Chung A-S, Kutty RK. 1982. Inhibition of testicular HO activity by cadmium: a novel cellular response. J. Biol. Chem. 257:14116-21
4. Maines MD, Trakshel GM, Kutty RK. 1986. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: Only one molecular species of the enzyme is inducible. J. Biol. Chem. 261:411-19
5. Trakshel GM, Kutty RK, Maines MD. 1986. Purification and characterization of the major constitutive form of testicular heme oxygenase: the non-inducible isoform. J. Biol. Chem. 261:11131-37
6. Maines MD. 1984. New developments in the regulation of heme metabolism and their implications. CRC Crit. Rev. Toxicol. 12:241-314
7. Maines MD. 1992. Heme Oxygenase: In Clinical Applications and Functions. Boca Raton, FL: CRC Press. 266 pp.
8. Kutty RK, Maines MD. 1981. Purification and characterization of biliverdin reductase from the rat liver. J. Biol. Chem. 256:3956-62
9. McCoubrey WK Jr, Cooklis MA, Maines MD. 1995. The structure, organization and differential expression of the rat gene for biliverdin reductase. Gene 160:235-40
10. Stocker P, Yamamoto Y, McDonach AF, Glazer AN, Ames BN. 1987. Bilirubin is an antioxidant of possible physiological importance. Science 235:1043-47
11. Maines MD. 1996. Mice transgenic for heme oxygenase-1 show increased neuronal expression of the protein and decreased lipid peroxidation activity. In Molecular Chaperones and the Heat Shock Protein, ed. C Georgopoulos, S Lindquist, R Morimoto, p. 231. Cold Spring Harbor, NY: Cold Spring Harbor Lab.
12. Mori H, Otake T, Morimoto M, Ueba N, Kunita N, et al. 1991. In vitro anti-human immunodeficiency virus type-1 activity of biliverdin, a bile pigment. Jpn. J. Cancer Res. 82:755-57
13. Maines MD, Kappas A. 1975. Cobalt stimulation of heme degradation in the liver: Dissociation of microsomal oxidation of heme from cytochrome P-450. J. Biol Chem. 250:4171-77
14. Maines MD. 1988. Heme oxygenase: Function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2:2557-68
15. Tappel AL. 1961. Biocatalysts: lipoxidase and hematin compounds. In Autooxidation and Antioxidants, ed. WO Lundberg, 1:325-66. New York: Wiley
16. Nathan CF, Hibbs JB Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65-70
17. Ignarro LJ. 1993. NO-mediated vasorelaxation. Thrombosis Haemostasis 70:148-51
18. Moncada S. 1994. Nitric oxide. J. Hypertens. 12:S35-S39
19. Jaffrey SR, Snyder SH. 1995. Nitric oxide - a neural messenger. Annu. Rev. Cell. Dev. Biol. 11:417-40
20. Billiar TR. 1995. Nitric oxide: novel biology with clinical relevance. Ann. Surg. 221:339-49
21. Falk JE. 1964. Porphyrins and Metallaporphyrins. Amsterdam, The Netherlands: Elsevier
22. Ignarro LJ, Ballot B, Wood KS. 1984. Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. Biol. Chem. 259:6201-7
23. Stone JR, Marletta MA. 1994. Soluble guanylate cyclase from bovine lung: Activation of nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 33:5636-40
24. Burstyn J, Yu AE, Dierks EA. 1995. Studies of heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): characterization of Fe(II)SGC and Fe(II)sGC (CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme. Biochemistry 34:5896-903
25. Yang KX, Artz JD, Lock J, Sanchez C, Bennett BM, et al. 1996. Synthesis of novel organic nitrate esters - guanylate cyclase activation and tissue relaxation. J. Chem. Soc. 11:1073-75
26. 4. J. Physiol. 134:123-34
27. Gibson QH. 1978. The oxygenation of hemoglobin. In The Porphyrins, ed. D Dolphin, 5:153-203. New York: Academic
28. Brown SB. 1976. Stereospecific heme cleavage. A model for the formation of bile pigment isomers in vivo and in vitro. Biochem. J. 159:23-26
29. Sano S, Sano T, Morishima I, Shiro Y, Maeda Y. 1986. On the mechanism of the chemical and enzymatic oxygenation of α oxyprotohemin IX to Fe-biliverdin Xα. Proc. Natl. Acad. Sci. USA 83:531-35
30. Sjöstrand T. 1949. Endogenous formation of carbon monoxide in man under normal and pathological conditions. J. Clin. Lab. Invest. 1:201-8
31. Troxler RF, Brown A, Lester R, White P. 1970. Bile pigment formation in plants. Science 167:192-94
32. Beale SI, Lornejo J. 1984. Enzymatic heme oxygenase activity in soluble extracts of the unicellular red alga, cyanidium caldarium. Arch. Biochem. Biophys. 235:371-84
33. Tenhunen R, Marver HS, Schmid R. 1968. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. USA 61:748-55
34. Kutty RK, Maines MD. 1987. Characterization of an NADH-dependent heme degrading system in ox heart mitochondria. Biochem. J. 246:467-74
35. Guengerich FP. 1978. Destruction of heme and hemoproteins mediated by liver microsomal reduced nicotinamide adenine dinucleotide phosphate-cytochrome P-450 reductase. Biochemistry 17:3633-39
36. Yoshida T, Takahashi S, Kikuchi G. 1974. Partial purification and reconstruction of the heme oxygenase system from pig spleen microsomes. J. Biochem. 75:1187-91
37. Cruse I, Maines MD. 1988. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J. Biol. Chem. 263:3348-53
38. Keyse SM, Tyrrell AM. 1989. Herne oxygenase is the major 32 kDa stress protein induced in human skin fibroblasts of UVA radiation, hydrogen peroxide and sodium arsenite. Proc. Natl. Acad. Sci. USA 86:99-103
39. Shibahara S, Müller R, Taguchi H, Yoshida T. 1985. Cloning and expression of cDNA for rat heme oxygenase. Proc. Natl. Acad. Sci. USA 82:7865-69
40. Rotenberg MO, Maines MD. 1990. Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J. Biol. Chem. 265:7501-6
41. Müller RM, Taguchi H, Shibahara S. 1987. Nucleotide sequence and organization of the rat heme oxygenase gene. J. Biol. Chem. 262:6795-802
42. McCoubrey WK Jr, Maines MD. 1994. The structure, organization, and differential expression of the gene encoding rat heme oxygenase-2. Gene 139:155-61
43. Kutty RK, Kutty G, Rodriquez IR, Chader GJ, Wiggert B. 1994. Chromosomal localization of the human heme oxygenase genes: Heme oxygenase-1 (HMOX1) maps to chromosome 22q12 and heme oxygenase-2 (HMOX2) maps to chromosome 16p13.3. Genomics 20:513-16
44. Sun Y, Rotenberg MO, Maines MD. 1990. Developmental expression of heme oxygenase isozymes in rat brain: Two HO-2 mRNAs are detected. J. Biol. Chem. 265:8212-17
45. McCoubrey WK Jr, Ewing JF, Maines MD. 1992. Human heme oxygenase: characterization and expression of a full length cDNA and evidence suggesting the two HO-2 transcripts differ by choice of polyadenylation signal. Arch. Biochem. Biophys. 295:13-20
46. McCoubrey WK Jr, Eke B, Maines MD. 1995. Multiple transcripts encoding HO-2 in rat testis: Developmental and cell specific regulation of transcripts and protein. Biol. Reprod. 53:1330-38
47. Rotenberg MO, Maines MD. 1991. Characterization of a cDNA encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: possible heme-binding site? Arch. Biochem. Biophys. 290:336-44
48. Evans C-O, Healey JF, Green Y, Bonkovsky HL. 1991. Cloning, sequencing and expression of cDNA for chick liver haem oxygenase. Biochem. J. 273:659-66
49. Schacter BA, Cripps V, Troxler RF, Offner GD. 1990. Structural studies on bovine spleen heme oxygenase: immunological and structural diversity among mammalian heme oxygenase enzymes. Arch. Biochem. Biophys. 282:404-12
50. McCoubrey WK Jr, Maines MD. 1993. Domains of rat heme oxygenase-2. The amino terminus and histidine 151 are required for catalytic activity. Arch. Biochem. Biophys. 302:402-8
51. Wilks A, Ortiz de Montellano PR, Sun J, Loehr TM. 1966. Heme oxygenase (HO-1): His-132 stabilizes a distal water ligand and assists catalysis. Biochemistry 35:930-36
52. Maines MD. 1981. Zinc-protoporphynn is a selective inhibitor of heme oxygenase activity in the neonatal rat. Biochim. Biophys. Acta 673:339-50
53. Kappas A, Drummond GS. 1985. Metalloporphyrins: a class of compounds of pharmacological interests. BioEssays 3:256-59
54. Alam J, Shibahara S, Smith A. 1989. Transcriptional activator of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J. Biol. Chem. 264:6371-75
55. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AMK. 1995. Induction of HO-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am. J. Respir. Cell. Mol. Biol. 13:387-98
56. Lavrosky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. 1994. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the premotor region of the human heme oxygenase-1 gene. Proc. Natl. Acad. Sci. USA 91:5987-91
57. Raju VS, Maines MD. 1997. Regulation of heme oxygenase-2 mRNA and protein by glucocorticoids: Characterization of a functional GRE. Biochim. Biophys. Acta 1350: In press
58. Weber CM, Eke BC, Maines MD. 1994. Corticosterone regulates heme oxygenase-2 and NO synthase transcription and protein expression in rat brain. J. Neurochem. 63:953-62
59. Maines MD, Eke BC, Zhao X. 1996. Corticosterone promotes increased heme oxygenase-2 protein and transcript expression in the newborn rat. Brain Res. 722:83-94
60. Blake MJ, Gershon D, Fargnoli J, Halbrook NJ. 1990. Discordant expression of heat shock protein mRNAs in tissues of heat-stressed rats. J. Biol. Chem. 265:15275-79
61. Raju VS, Maines MD. 1993. Coordinated expression and mechanisms of induction of HSP32 (heme oxygenase-1) mRNA by hyperthermia in rat organs. Biochem. Biophys. Acta 1217:273-80
62. Ewing JF, Maines MD. 1991. 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 88:5364-58
63. Ewing JF, Haber SN, Maines MD. 1992. Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: Hyperthermia causes rapid induction of mRNA and protein. J. Neurochem. 58:4023-29
64. Braggins PE, Trakshel GM, Kutty RK, Maines MD. 1986. Characterization of two heme oxygenase isoforms in rat spleen: comparison with the hematin-induced and constitutive isoforms of the liver. Biochem. Biophys. Res. Commun. 141:528-33
65. Nishimura RN, Dwyer BE, Lu S-Y. 1996. Localization of heme oxygenase in rat retina: effect of light adaption. Neurosci. Lett. 205:13-16
66. Trakshel GM, Kutty RK, Maines MD. 1988. Resolution of the rat brain heme oxygenase activity: absence of a detectable amount of the inducible form (HO-1). Arch. Biochem. Biophys. 260:732-39
67. Trakshel GM, Maines MD. 1989. Multiplicity of heme oxygenase isozymes-HO-1 and HO-2 are different molecular species in rat and rabbit. J. Biol. Chem. 264:1323-28
68. Ewing JF, Maines MD. 1992. In situ hybridization and immunohistochemical localization of heme oxygenase-2 mRNA and protein in normal rat brain: differential distribution of isozyme 1 and 2. Mol. Cell. Neurosci. 3:4559-70
69. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. 1993. Carbon monoxide: a putative neural messenger. Science 259:381-84
70. Matz P, Turner C, Weinstein PR, Massa SM, Panter SS, Sharp FR. 1991. Heme oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. Brain Res. 713:11-22
71. Maines MD, Mark J, Ewing J. 1993. Heme oxygenase, a likely regulator of cGMP production in the brain: Induction in vivo of HO-1 compensates for depression in NO synthase activity. Mol. Cell. Neurosci. 4:398-405
72. Ewing JF, Maines MD. 1993. Glutathione depletion induces heme oxygenase-1 (HSP32) mRNA and protein in rat brain. J. Neurochem. 60:1512-19
73. Dwyer BE, Nishimura RN, Lu SY. 1995. Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Mol. Brain. Res. 30:37-47
74. Premkumar DRD, Smith MA, Richey PL, Petersen RB, Castellani R, et al. 1995. Induction of heme oxygenase-1 in mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem. 65:1399-402
75. Vollerthun R, Höhler B, Kummer W. 1996. Heme oxygenase-2 in primary afferent neurons of the guinea pig. Histochem. Cell. Biol. 105:453-58
76. Zakhary R, Gaine SP, Dinerman JL, Ruat M, Flavahan NA, Snyder SH. 1996. Heme oxygenase 2: Endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc. Natl. Acad. Sci. USA 93:795-98
77. Kutty RK, Kutty G, Wiggert B, Chader GJ, Darrow RM, Organisciak DT. 1995. Induction of heme oxygenase-1 in the retina by intense visible light: suppression by the antioxidant dimethylthiourea. Proc. Natl. Acad. Sci. USA 92:1177-81
78. Ewing JF, Weber CM, Maines MD. 1993. Biliverdin reductase is heat resistant and co-expressed with constitutive and heat shock form of heme oxygenase. J. Neurochem. 61:1015-23
79. Schmidt HH, Gacne CD, Nokong M, Pollock JS, Miller MF, Murad F. 1992. Mapping of neural nitric oxide synthase in the rat suggests frequent colocalization with NADPH diaphorase but not with soluble guanylate cyclase, and novel paraneural functions for nitronergic signal transduction. J. Histochem. Cytochem. 40:1439-56
80. Vincent SR, Kimura GK. 1992. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-84
81. De Vente JJ, Bol GJ, Steinbusch HWM. 1989. Localization of cGMP in the cerebellum of the adult rat brain: an immunochemical study. Brain Res. 504:332-37
82. Vincent SR, Das S, Maines MD. 1994. Brain heme oxygenase isoenzymes and nitric oxide synthase are colocalized in select neurons. Neuroscience 63:223-31
83. Landfield PW, Waymire PW, Lynch G. 1978. Hippocampal aging and adrenocorticoids: quantitative correlations. Science 202:1098-102
84. Sapolsky RM. 1985. A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults. J. Neurosci. 5:1228-32
85. McEwen BS, Gould E. 1990. Adrenal steroid influences on the survival of hippocampal neurons. Biochem. Pharmacol. 40:2393-402
86. Smith MA. 1996. Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors. Behav. Brain. Res. 78:25-36
87. Ewing JF, Maines MD 1995. Distribution of constitutive (HO-2) and heat inducible heme oxygenase (HO-1) isozymes in rat testes: HO-2 displays stage-specific expression in germ cells. Endocrinology 136:2294-302
88. Maines MD, Ewing JF. 1996. Stress response of the rat testis: in situ hybridization and immunohistochemical analysis of heme oxygenase-1 (HSP32) induction by hyperthermia. Biol. Reprod. 54:1070-79
89. Maines MD, Abrahamsson PA. 1996. Expression of heme oxygenase (HSP32) in human prostate: normal, hyperplastic and tumor tissue distribution. Urology 47:727-33
90. Maines MD, Mayer RD, Ewing JF, McCoubrey WK. 1993. Induction of kidney HO-1 (HSP32) mRNA and protein by ischemia: possible role of heme as both promoter of tissue damage and regulator of HSP32. J. Pharmacol. Exp. Ther. 264:457-62
91. Ewing JF, Raju VS, Maines MD. 1994. Induction of heart heme oxygenase-1 (HSP32) by hyperthermia: possible role in stress-mediated elevation of cyclic 3′:5′-Guanosine monophosphate J. Pharmacol. Exp. Ther. 271:408-14
92. Raju VS, Maines MD. 1996. Renal ischemia/reperfusion in rats upregulates HO-1 (HSP32) expression and increases cGMP in the rat heart. J. Pharmacol. Exp. Ther. 277:1814-22
93. Prabhakhar NR, Dinerman JL, Agani FH, Snyder SH. 1995. Carbon monoxide: a role in carotid body chemore-ception. Proc. Natl. Acad. Sci. USA 92:1994-97
94. Morita T, Perrella MA, Lee M-E, Kourembanas S. 1995. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc. Natl. Acad. Sci. USA 92:1475-79
95. Grozdanovic Z, Gossrau R. 1996. Expression of heme oxygenase-2 (HO-2)-like immunoreactivity in rat tissue. Acta Histochem. 98:203-14
96. Lin JH-C, Villalon P, Nelson JC, Abraham NG. 1989. Expression of rat liver heme oxygenase gene during development. Arch. Biochem. Biophys. 270:623-29
97. Sun Y, Maines MD. 1990. Heme oxygenase-2 mRNA: developmental expression in the rat liver and response to cobalt chloride. Arch. Biochem. Biophys. 282:240-45
98. Suematsu M, Goda N, Sano T, Kashiwagi S, Egawa T, et al. 1995. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J. Clin. Invest. 96:2431-37
99. Nathan CF. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:3051-64
100. North AJ, Lau KS, Brannon TS, Wu LC, Wells LB, et al. 1996. Oxygen upregulates nitric oxide synthase gene expression in bovine fetal pulmonary artery endothelial cells. Am. J. Physiol. 270:L643-49
101. Nath KA, Balla G, Vercellotti GM, Balla J, Jacob HS, et al. 1992. Induction of HO is a rapid, protective response in rhabdomyolysis in the rat. J. Clin. Invest. 90:267-70
102. Willis D, Moore AR, Frederick R, Willoughby DA. 1996. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat. Med. 2:87-90
103. Hirsch DB, Steiner JP, Dawson TM, Mammen A, Hayek E, Snyder SH. 1993. Neurotransmitter release regulated by nitric oxide in PC-12 cells and brain synaptosomes. Curr. Biol. 3:749-54
104. Stamler JS, Singel DJ, Loscalzo J. 1992. Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898-902
105. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. 1990. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87:1620-24
106. Hibbs JB, Taintor RR, Vavrin Z, Rachlin EM. 1988. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157:87-94
107. Willis D, Tomlinson A, Frederick R, Paul-Clark MS, Willoughby DA. 1995. Modulation of heme oxygenase activity in rat brain and spleen by inhibitors and donors of nitric oxide. Biochem. Biophys. Res. Commun. 214:1152-56
108. Nunokawa Y, Ishida N, Tanaka S. 1993. Cloning of inducible nitric oxide synthase in rat vascular smooth muscle cells. Biochem. Biophys. Res Commun. 191:89-94
109. Silvagno F, Xia H, Bredt DS. 1996. Neuronal nitric oxide synthase-μ, an alternatively spliced isoform expressed in differential skeletal muscle. J. Biol. Chem. 271:11204-8
110. Garbers DL. 1979. Purification of soluble guanylate cyclase from rat lung. J. Biol. Chem. 254:240-43
111. Grenzen R, Böhme E, Hofmann F, Schultz G. 1981. Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett. 132:71-74
112. Craven PA, DeRubertis FR. 1983. Requirement for heme in the activation of purified guanylate cyclase by nitric oxide. Biochim. Biophys. Acta 745:310-21
113. Rublevskaya IN, Maines MD. 1994. Interaction of Fe-protoporphyrin IX and heme analogues with purified recombinant Heme oxygenase-2, the constitutive isozyme of the brain and testes. J. Biol. Chem. 269:26390-95
114. White KA, Marietta MA. 1992. Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry 31:6627-31
115. McMillan K, Bredt DS, Hirsch DJ, Snyder SH, Clark JE, Masters BSS. 1992. Cloned, expressed rat cerebellar NOS containing stoichiometric amounts of heme which binds CO. Proc. Natl. Acad. Sci. USA 89:11141-45
116. Wang J, Rousseau DL, Abu-Soud HM, Stuehr DJ. 1994. Heme coordination of NO in NO synthase. Proc. Natl. Acad. Sci. USA 91:10512-16
117. Maines MD, Kappas A. 1977. Enzymatic oxidation of cobalt-protoporphyrin-IX: observations on the mechanism of heme oxygenase. Biochemistry 16:419-22
118. Marks GS, Brian JF, Nakatsu K, McLaughlin BE. 1991. Does carbon monoxide have a physiological function? Trends Pharmacol. Sci. 12:185-88
119. Kharitonov VG, Sharma VS, Pilz RB, Magde D, Koesling D. 1995. Basis of guanylate cyclase activation by carbon monoxide. Proc. Natl. Acad. Sci. USA 92:2568-71
120. Brüne B, Ullrich V. 1987. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32:497-504
121. Ramos KS, Lin H, McGrath JJ. 1989. Modulation of cyclic guanosine monophosphate levels in cultured aortic smooth muscle cells by carbon monoxide. Biochem. Pharmacol. 38:1368-70
122. Utz J, Ullrich V. 1991. Carbon monoxide relaxes ilial smooth muscle through activation of guanylate cyclase. Biochem. Pharmacol. 41:1195-2001
123. Ingi T, Cheng J, Ronnett GV. 1996. Carbon monoxide: An endogenous modulator of the nitric oxide-cyclic GMP signaling system. Neuron 16:835-42
124. Luo D, Vincent SR. 1994. Metalloporphyrins inhibit nitric oxide-dependent cGMP formation in vivo. Eur. J. Pharmacol. 267:263-67
125. Ny L, Andersson K-E, Grundemar L. 1995. Inhibition by zinc protoporphyrin-IX of receptor-mediated relaxation of the rat aorta in a manner distinct from inhibition of haem oxygenase. Br. J. Pharmacol. 115:186-90
126. Maines MD, Kappas A. 1976. The induction of heme oxidation in various tissues by trace metals: evidence for the catabolism of endogenous heme by hepatic heme oxygenase. Ann. Clin. Res. 8:38-46
127. Maines MD. 1980. Regional distribution of the enzymes of heme biosynthesis and the inhibition of δ-aminolevulinate synthetase by manganese in the rat brain. Biochem. J. 190:315-21
128. Maines MD, Kappas A. 1975. The degradative effects of porphyrins and heme compounds on the components of the microsomal mixed function oxidase. J. Biol. Chem. 250:2363-69
129. Trakshel GM, Sluss PM, Maines MD. 1992. Comparative effects of tin and zinc-protoporphyrin on steroidogenesis: Tin-protoporphyrin is a potent inhibitor of cytochrome P450-dependent activities in the rat adrenals. Pediatr. Res. 31:1140-49
130. Kutty RK, Daniel RF, Ryan DE, Levin W, Maines MD. 1988. Rat liver cytochrome P-450b, P-420b, and P-420c are degraded to biliverdin by heme oxygenase. Arch. Biochem. Biophys. 260:638-44
131. Kutty RK, Maines MD. 1984. Effects of induction of heme oxygenase by cobalt and tin in the in vivo degradation of myoglobin. Biochem. Pharmacol. 18:2924-26
132. Kutty RK, Maines MD. 1982. Oxidation of heme c derivatives by purified heme oxygenase: evidence for the presence of one molecular species of heme oxygenase in rat liver. J. Biol. Chem. 257:9944-52
133. Eisenstein RS, Garcia-Magol D, Pettingell W, Muncro HN. 1991. Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of Fe. Proc. Natl. Acad. Sci. USA 88:688-92
134. Aust SD, Svingen BA. 1982. Role of Fe in enzymatic lipid peroxidation. In Free Radicals in Biology, ed. WA Pryor, pp. 1-28. New York: Academic
135. Gibson QH, Roughlon FJW. 1955. The reactions of sheep haemoglobin with nitric oxide. J. Physiol. 128:69-70P
136. Xie Q-W, Leung M, Fuortes M, Sassa S, Nathan C. 1996. Complementation analysis of mutants of nitric oxide synthase reveals that the active site requires two hemes. Proc. Natl. Acad. Sci. USA 93:4891-96
137. Weiss G, Werner-Felmayer G, Werner ER, Grünewald K, Wachter H, Hentze MW. 1994. Iron regulates NO synthase activity by controlling nuclear transcription. J. Exp. Med. 180:969-76
138. Maines MD, Polevoda BV, Huang TJ, McCoubrey WK Jr. 1996. Human biliverdin IXα reductase is a zinc-metalloprotein; Characterization of purified and Escherichia coli expresses enzymes. Eur. J. Biochem. 235:372-81
139. Griscavage JM, Rogers NE, Sherman MD, Ignarro LJ. 1993. Induction of nitric oxide synthase mRNA expression. Suppression by exogenous nitric oxide. J. Immunol. 151:6329-37
140. Colasanti M, Persichini T, Menegazzi M, Mariotto S, Giordano E, et al. 1995. Inducible nitric oxide synthase from a rat alveolar macrophage cell line is inhibited by nitric oxide. J. Biol. Chem. 270:26731-33
141. Chakder S, Rathi S, Ma X-L, Rattan S. 1996. Heme oxygenase inhibitor zinc protoporphyrin IX causes an activation of nitric oxide in the rabbit internal anal sphincter. J. Pharmacol. Exp. Ther. 277:1376-82
142. Motterlini R, Foresti R, Intaglietta M, Winslow RM. 1996. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am. J. Physiol. 270:H107-14
143. Maines MD, Trakshel G. 1992. Differential regulation of heme oxygenase isozymes by Sn- and Zn-protoporphyrins: possible relevance to suppression of hyperbilirubinemia. Biochim. Biophys. Acta 1131:166-74
144. Vreman HJ, Cipkala DA, Stevenson DK. 1996. Characterization of porphyrin heme oxygenase inhibitors. Can. J. Physiol. Pharmacol. 74:278-85
145. Sardana MD, Kappas A. 1987. Dual control mechanism for heme oxygenase: tin (IV)-protoporphyrin potently inhibits enzyme activity while markedly increasing content of enzyme protein in liver. Proc. Natl. Acad. Sci. USA 84:2464-68
146. Maines MD, Kappas A. 1978. Prematurely evoked synthesis and induction of δ-aminolevulinate synthetase in neonatal liver. Evidence for metal ion repression of enzyme formation. J. Biol. Chem. 253:2321-26
147. Melefors O, Goossen B, Johansson HE, Stripecke R, Gray NK, Hentze MW. 1993. Translational control of 5-aminolevulinate synthase mRNA by iron-responsive elements in erythroid cells. J. Biol. Chem. 268:5974-78
148. Theil E. 1990. Regulation of ferritin and transferrin receptor mRNAs. J. Biol. Chem. 265:4771-74
149. Weiss GB, Goosen W, Doppler D, Fuchs K, Pantopoulos G, et al. 1993. Translational regulation via iron-responsive elements by the nitric oxide/NO-synthase pathway. EMBO J. 12:3651-57
150. Hecker M, Mülsch A, Busse R. 1994. Subcellular localization and characterization of neuronal nitric oxide synthase. J. Neurochem. 62:1524-29
151. McCoubrey WK Jr, Cooklis MA, Maines MD. 1995. The structure, organization and differential expression of the rat gene for biliverdin reductase. Gene 160:235-40
152. Pollock JS, Föstermann U, Mitchell JA, Warner TD, Schmidt HHHW, et al. 1991. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA 88:10480-84
153. Ow DW, Sundaresan V, Rothstein DM, Brown SE, Ausubel FM. 1983. Promoters regulated by the glnG (ntrC) and nigA gene products share a heptameric consensus sequence in the -15 region. Proc. Natl. Acad. Sci. USA 80:2524-28
154. Lee-Huang S, Lin J-J, Kung H-G, Huang PL, Lee L. 1993. The 3′ flanking region of the human erythropoietin encoding gene contains nitrogen-regulatory/oxygen sensing consensus sequences and tissue-specific transcriptional regulatory elements. Gene 137:203-10
155. Ross J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423-50
156. Zhang L, Guarente L. 1995. Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J. 14:313-20
157. Deleted in proof
158. Vile GF, Tyrell M. 1994. Oxidative stress resulting from UVA irradiation of human skin fibroblasts leads to a HO dependent increase in ferritin. J. Biol. Chem. 268:14678-81
159. Tacchini L, Pogliachi G, Radise L, Anzon E, Bernelli-Zazzera B. 1995. Differential activation of heat-shock and oxidation-specific stress genes in chemically induced oxidative stress. Biochem. J. 309:453-59
160. Menegazzi M, Guerriero C, Carcereri de Prati A, Cardinale C, Suzuku H, Armato U. 1996. TPA and cycloheximide modulate the activation of NFkB and the induction and stability of nitric oxide synthase transcript in primary neonatal rat hepatocytes. FEBS Lett. 379:279-85
161. Wolin MS. 1996. Reactive oxygen species and vascular signal transduction mechanisms. Microcirculation 3:1-17
162. Zhuo M, Small SA, Kandel ER, Hawkins RD. 1993. Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260:1946-50
163. Stevens CF, Wang Y. 1993. Reversal of long-term potentiation by inhibitors of haem oxygenase. Nature 364:147-49
164. Glaum SR, Miller RJ. 1993. Zinc protoporphyrin-IX blocks the effects of metabotropic glutamate receptor activation in the rat nucleus tractus solitarii. Mol. Pharmacol. 43:965-69
165. Shinomura T, Nakao S-I, Mori K. 1994. Reduction of depolarization-induced glutamate released by heme oxygenase inhibitor: possible role of carbon monoxide in synaptic transmission. Neurosci. Lett. 166:131-34
166. Fin C, Schmitz PK, DaSilva RC, Bernabeu R, Medina JH, Izquierdo I. 1994. Intrahippocampal, but not intraamygdala, infusion of an inhibitor of heme oxygenase causes retrograde amnesia in the rat. Eur. J. Pharmacol. 271:227-29
167. Shraga-Levine Z, Galron R, Sokolovsky M. 1994. Cyclic GMP formation in rat cerebellar slices is stimulated by endothelins via nitric oxide formation and by sarafotoxins via formation of carbon monoxide. Biochemistry 33:14656-59
168. Pozzoli G, Mancuso C, Mirtella A, Preziosi P, Grossman AB, Navarra P. 1994. Carbon monoxide as a novel neuroendocrine modulator: inhibition of stimulated corticotropin-releasing hormone release from acute rat hypothalamic explants. Endocrinology 135:2314-17
169. Hawkins RD, Zhuo M, Arancio O. 1994. Nitric oxide and carbon monoxide as possible retrograde messengers in hippocampal long-term potentiation. J. Neurobiol. 25:652-65
170. Yamamoto T, Nozaki-Taguchi N. 1995. Zinc protoporphyrin IX, an inhibitor of the enzyme that produces carbon monoxide, blocks spinal nociceptive transmission evoked by formalin injection in the rat. Brain Res. 704:256-62
171. Lamar CA, Mahesh VB, Brann DW. 1996. Regulation of gonadotropinreleasing hormone (GnRH) secretion by heme molecules: a regulatory role for carbon monoxide? Endocrinology 137:790-93
172. + pump as a site of action for carbon monoxide and glutamate: a mechanism for long-term modulation of cellular activity. Neuron 14:781-94
173. Pineda J, Kogan JH, Aghajanian GK. 1996. Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase: involvement of a nonselective cationic channel. J. Neurosci. 16:1389-99
174. Furchgott RF, Jothianandan D. 1991. Endothelium-dependent and -independent vasodilation involving cGMP: relaxation induced by NO, CO and light. Blood Vessels 28:52-61
175. Lefer DJ, Ma X-L, Lefer AM. 1993. A comparison of vascular biological actions of carbon monoxide and nitric oxide. Methods Find. Exp. Clin. Pharmacol. 15:617-22
176. Brian JE, Heistad DD, Faraci FM. 1994. Effect of carbon monoxide on rabbit cerebral arteries. Stroke 24:639-44
177. Johnson RA, Lavesa M, Askari B, Abraham NG, Nasjletti A. 1995. A heme oxygenase product, presumably carbon monoxide mediates a vasodepressor function in rats. Hypertension 25:166-69
178. Christodoulides N, Durante W, Kroll KH, Schafer AI. 1995. Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation 91:2306-9
179. Fukushima T, Okinaga S, Sekizawa K, Ohrui T, Yamaya M, Sasaki H. 1995. The role of carbon monoxide in lucigenin-dependent chemiluminescence of rat alveolar macrophages. Eur. J. Pharmacol. 289:103-7
180. Rattan S, Chakder S. 1993. Inhibitory effect of CO on internal anal sphincter: Heme oxygenase inhibitor inhibits NANC relaxation. Am. J. Physiol. 265:0799-804
181. Farrugia G, Irons WA, Rae JL, Sarr MG, Szurszewski JH. 1993. Activation of whole cell currents in isolated human jejunal circular smooth muscle cells by carbon monoxide. Am. J. Physiol. 264:G1184-89
182. Ny L, Grundemar L, Larsson B, Alm P, Ekström P, Andersson K-E. 1995. Carbon monoxide as a putative messenger molecule in the feline lower esophageal sphincter of the cat. NeuroReport 6:1261-65
183. Agarwal A, Kim Y, Matas AJ, Alam J, Nath KA. 1996. Gas-generating systems in acute renal allograft rejection in the rat. Transplantation 61:93-98
184. Garthwaite J, Charles SL, Chess-Williams R. 1988. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385-88
185. Dawson TM, Snyder SH. 1994. Gaseous biological messengers: Nitric oxide and carbon monoxide in the brain. J. Neurosci. 4:S147-59
186. Zinkard WC, Stumpo RJ, Thompson C, Patel J, Pullan M. 1993. Lack of involvement of nitric oxide in NMDA-induced neuronal cell death in cortical culture. NeuroReport 5:148-50
187. White RE, Lee AB, Sheherbatko AD, Lincoln TM, Schonbrunn A, Armstrong DL. 1993. Potassium channel stimulation by natriuretic peptides through cGMP dependent dephosphorylation. Nature 361:263-66
188. Grant SGN, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER. 1992.
189. 2+ channel activity in area CA1 of hippocampus. Proc. Natl. Acad. Sci. USA 88:6467-71
190. 2+-independent NO synthase. FASEB J. 291:145-49
191. Maines MD, Eke BC, Weber CM, Ewing JF. 1995. Corticosterone has a permissive effect on expression of heme oxygenase-1 CA1-CA3 neurons of hippocampus in thermal-stressed rats. J. Neurochem. 64:1769-79
192. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F. 1983. Intracellular injection of EGTA blocks induction of hippocampal long-term potentiation. Nature 305:719-21
193. Armanini MP, Hutchins C, Stein BA, Sapolsky RM. 1990. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res. 532:7-12
194. Mattson MP. 1994. Calcium and neuronal injury in Alzheimer's disease. Contributions of beta-amyloid precursor protein mismetabolism, free radicals, and metabolic compromise. Ann. NY Acad. Sci. 740:50-76
195. Malenka RC, Kauer JA, Zucker RS, Nicoll RA. 1988. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242:81-84
196. Sapolsky RM. 1990. Glucocorticoid hippocampal damage and the glutamatergic synapse. Prog. Brain Res. 96:13-23
197. Poss KD, Thomas MJ, Abralidze AK, O'Dell TJ, Tonegawa S. 1995. Hippocampal long-term potentiation is normal in heme oxygenase-2 mutant mice. Neuron 15:867-73
198. Grundemar L, Johansson MB, Ekelund M, Högestätt ED. 1995. Haem oxygenase activity in blood vessel homogenates as measured by carbon monoxide production. Acta Physiol. Scand. 153:203-4
199. Cook MN, Nakatsu K, Marks GS, McLaughlin BE, Vreman HJ, et al. 1995. Heme oxygenase activity in the adult rat aorta and liver as measured by carbon monoxide formation. Can. J. Physiol. Pharmacol. 73:515-18
200. Sadoff JD, Scholz PM, Weiss HR. 1996. Endogenous basal nitric oxide production does not control myocardial oxygen consumption or function. Proc. Soc. Exp. Biol. Med. 211:332-38
201. Lapresle J, Fardeau M. 1991. The central nervous system and carbon monoxide poisoning II. Anatomical study of brain lesions following intoxication with carbon monoxide (22 cases). Acta Neuropathol. 6:327-48
202. 201a. McDonald LJ, Murad F. 1996. Nitric oxide and cyclic GMP signaling. Proc. Soc. Exp. Biol. Med. 211:1-6
203. Willis D, Moore AR, Frederick R, Willoughby DA. 1996. Heme oxygenase: A novel target for the modulation of the inflammatory response. Nat. Med. 2:87-90
204. Genco CA, Odusanya BM, Brown G. 1994. Binding and accumulation of hemin in porphyromonas gingvalis are induced by hemin. Infect. Immun. 62:2885-92
205. Vogt BA, Alam J, Croatt AJ, Vercellotti GM, Nath KA. 1995. Acquired resistance to acute oxidative stress, possible role of HO and ferritin. Lab. Invest. 72:474-83
206. Mascalchi M, Petruzzi P, Zampa V. 1996. MRI of cerebellar white matter damage due to carbon monoxide poisoning: Case report. Neuroradiology 38:S73-S74
207. Bianco F, Floris R. 1996. MRI appearances consistent with haemorrhagic infarction as an early manifestation of carbon monoxide poisoning. Neuroradiology 38:S70-S72
208. Fakuda K, Panter SS, Sharp FR, Noble LJ. 1995. Induction of HO-1 after traumatic brain injury in the rat. Neurosci. Lett. 199:127-30
209. Young RA. 1990. Stress proteins and immunology. Annu. Rev. Immunol. 8:401-20
210. + oligodendrocytes in multiple sclerosis. Proc. Natl. Acad. Sci. USA 88:6452-56
211. Ohno M, Komiyama A, Martin PM, Suzuki K. 1993. Proliferation of microglia/macrophages in the demyelination of NS and PNS of twitcher mouse. Brain Res. 602:265-74
212. Hutter CDD, Blair ME. 1996. Carbon monoxide - does fetal exposure cause sudden infant death syndrome? Med. Hypotheses 46:1-4
213. Barinaga M. 1993. Carbon monoxide: killer to brain messenger in one step. Science 259:309