The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis

References

• Palmer R.M.J., Ashton D.S., Moncada S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 1988; 333: 664–666
   PubMed Web of Science ®Google Scholar
• Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide physiology, pathophysiology, and pharmacology. Pharmacological Review 1991; 43: 109–142
   PubMed Web of Science ®Google Scholar
• Furchgott R.F., Jothianandan D. Endothelium-dependent and -independent vasodilation involving cGMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels 1991; 28: 52–61
   PubMedGoogle Scholar
• Zakhary R., Gaine S.P., Dinerman J.L., Ruat M., Flavahan N.A., Snyder S.H. Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proceeding of the National Academy of Sciences of the United States of America 1996; 93: 795–798
   PubMed Web of Science ®Google Scholar
• Motterlini R., Gonzales A., Foresti R., Clark J.E., Green C.J., Winslow R.M. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circulation Research 1998; 83: 568–577
   PubMed Web of Science ®Google Scholar
• Sammut I.A., Foresti R., Clark J.E., Exon D.J., Vesely M.J.J., Sarathchandra P., Green C.J., Motterlini R. Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. British Journal of Pharmacology 1998; 125: 1437–1444
   PubMed Web of Science ®Google Scholar
• Maines M.D. Carbon monoxide: an emerging regulator of cGMP in the brain. Molecular and Cellular Neurosciences 1993; 4: 389–397
   PubMed Web of Science ®Google Scholar
• Verma A., Hirsch D.J., Glatt C.E., Ronnett G.V., Snyder S.H. Carbon monoxide: a putative neural messenger. Science 1993; 259: 381–384
   PubMed Web of Science ®Google Scholar
• Durante W., Kroll M.H., Christodoulides N., Peyton K.J., Schafer A.I. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circulation Research 1997; 80: 557–564
   PubMed Web of Science ®Google Scholar
• Morita T., Perrella M.A., Lee M.E., Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proceeding of the National Academy of Sciences of the United States of America 1995; 92: 1475–1479
   PubMed Web of Science ®Google Scholar
• Ingi T., Cheng J., Ronnett G.V. Carbonmonoxide: an endogenous modulator of the nitric oxidecyclic GMP signaling system. Neuron 1996; 16: 835–842
   PubMed Web of Science ®Google Scholar
• Brune B., Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Molecular Pharmacology 1988; 32: 497–504
   Google Scholar
• Friebe A., Mullershausen F., Smolenski A., Walter U., Schultz G., Koesling D. YC-1 potentiates nitric oxide- and carbon monoxide-induced cyclic GMP effects in human platelets. Molecular Pharmacology 1998; 54: 962–967
   PubMed Web of Science ®Google Scholar
• Tenhunen R., Marver H.S., Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. Journal of Biological Chemistry 1969; 244: 6388–6394
   PubMed Web of Science ®Google Scholar
• Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB Journal 1988; 2: 2557–2568
   PubMed Web of Science ®Google Scholar
• Abraham N.G., Drummond G.S., Lutton J.D., Kappas A. The biological significance and physiological role of heme oxygenase. Cellular Physiology and Biochemistry 1996; 6: 129–168
   Web of Science ®Google Scholar
• Suematsu M., Wakabayashi Y., Ishimura Y. Gaseous monoxides. A new class of microvascular regulator in the liver. Cardiovascular Research 1996; 32: 679–686
   PubMed Web of Science ®Google Scholar
• Choi A.M.K., Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. American Journal of Respiratory Cell and Molecular Biology 1996; 15: 9–19
   PubMed Web of Science ®Google Scholar
• Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annual Review of Pharmacology and Toxicology 1997; 37: 517–554
   PubMed Web of Science ®Google Scholar
• Wang R. Resurgence of carbon monoxide: an endogenous gaseous vasorelaxing factor. Canadian Journal of Physiology and Pharmacology 1998; 76: 1–15
   PubMedGoogle Scholar
• Durante W., Schafer A.I. Carbon monoxide and vascular cell function (Review). International Journal of Molecular Medicine 1998; 2: 255–262
   PubMedGoogle Scholar
• Snyder S.H., Jaffrey S.R., Zakhary R. Nitric oxide and carbon monoxide: parallel roles as neural messengers. Brain Research Reviews 1998; 26: 167–175
   PubMedGoogle Scholar
• Johnson R.A., Kozma F., Colombari E. Carbon monoxide: from toxin to endogenous modulator of cardiovascular functions. Brazilian Journal of Medical and Biological Research 1999; 32: 1–14
   PubMedGoogle Scholar
• Siow R.C.M., Sato H., Mann G.E. Heme oxygenase carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide?. Cardiovascular Research 1999; 41: 385–394
   PubMed Web of Science ®Google Scholar
• Ignarro L. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annual Review of Pharmacology and Toxicology 1990; 30: 535–560
   PubMed Web of Science ®Google Scholar
• Maines M.D., Trakshel G.M., Kutty R.K. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: only one molecular species of the enzyme is inducible. Journal of Biological Chemistry 1986; 261: 411–419
   PubMed Web of Science ®Google Scholar
• McCoubrey W.M., Maines M.D. The structure, organization and differential expression of the gene encoding rat heme oxygenase-2. Gene 1994; 139: 155–161
   PubMed Web of Science ®Google Scholar
• Cruse I., Maines M.D. Evidence suggesting that the two forms of heme oxygenase are products of different genes. Journal of Biological Chemistry 1988; 263: 3348–3353
   PubMed Web of Science ®Google Scholar
• Trakshel G.M., Maines M.D. Multiplicity of heme oxygenase isozymes: HO-1 and HO-2 are different molecular species in rat and rabbit. Journal of Biological Chemistry 1989; 264: 1323–1328
   PubMed Web of Science ®Google Scholar
• McCoubrey W.K., Huang T.J., Maines M.D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. European Journal of Biochemistry 1997; 247: 725–732
   PubMedGoogle Scholar
• Raju V.S., McCoubrey W.K., Maines M.D. Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochimica Biophysica Acta 1997; 1351: 89–104
   PubMedGoogle Scholar
• Suematsu M., Goda N., Sano T., Kashiwagi S., Egawa T., Shinoda Y., Ishimura Y. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. Journal of Clinical Investigation 1995; 96: 2431–2437
   PubMed Web of Science ®Google Scholar
• Dore S., Takahashi M., Ferris C.D., Hester L.D., Guastella D., Snyder S.H. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proceeding of the National Academy of Sciences of the United States of America 1999; 96: 2445–2450
   PubMed Web of Science ®Google Scholar
• Lautier D., Luscher P., Tyrrell R.M. Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis 1992; 13: 227–232
   PubMed Web of Science ®Google Scholar
• Lee P.J., Alam J., Sylvester S.L., Inamdar N., Otterbein L., Choi A.M.K. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. American Journal of Respiratory Cell and Molecular Biology 1996; 14: 556–568
   PubMed Web of Science ®Google Scholar
• Rizzardini M., Carelli M., Cabello Porras M.R., Cantoni L. Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochemical Journal 1994; 304: 477–483
   PubMedGoogle Scholar
• Motterlini R., Foresti R., Intaglietta M., Winslow R.M. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. American Journal of Physiology 1996; 270: H107–H114
   PubMed Web of Science ®Google Scholar
• Foresti R., Clark J.B., Green C.J., Motterlini R. Thiol compounds interact with nitric oxide in regulating heme oxygenase-1 induction in endothelial cells. Involvement of superoxide and peroxynitrite anions. Journal of Biological Chemistry 1997; 272: 18411–18417
   PubMed Web of Science ®Google Scholar
• Foresti R., Sarathchandra P., Clark J.E., Green C.J., Motterlini R. Peroxynitrite induces haem oxygenase-1 in vascular endothelial cells: a link to apoptosis. Biochemical Journal 1999; 339: 729–736
   PubMed Web of Science ®Google Scholar
• Balla J., Jacob H.S., Balla G., Nath K., Eaton J.W., Vercellotti G.M. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proceeding of the National Academy of Sciences of the United States of America 1993; 90: 9285–9289
   PubMed Web of Science ®Google Scholar
• Balla J., Nath K.A., Balla G., Juckett M.B., Jacob H.S., Vercellotti G.M. Endothelial cell heme oxygenase and ferritin induction in rat lung by hemoglobin in vivo. American Journal of Physiology 1995; 268: L321–L327
   PubMed Web of Science ®Google Scholar
• Motterlini R., Foresti R., Intaglietta M., Vandegriff K., Winslow R.M. Oxidative-stress response in vascular endothelial cells exposed to acellular hemoglobin solutions. American Journal of Physiology 1995; 269: H648–H655
   PubMed Web of Science ®Google Scholar
• Nath K.A., Balla G., Vercellotti G.M., Balla J., Jacob H.S., Levitt M.D., Rosenberg M.E. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. Journal of Clinical Investigation 1992; 90: 267–270
   PubMed Web of Science ®Google Scholar
• Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., Vercellotti G.M. Ferritin: a cytoprotective antioxidant stratagem of endothelium. Journal of Biological Chemistry 1992; 267: 18148–18153
   PubMed Web of Science ®Google Scholar
• Otterbein L., Sylvester S.L., Choi A.M.K. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. American Journal of Respiratory Cell and Molecular Biology 1995; 13: 595–601
   PubMedGoogle Scholar
• Otterbein L., Chin D.Y., Otterbein S.L., Lowe V.C., Fessler H.E., Choi A.M.K. Mechanism of hemoglobin-induced protection against endotoxemia in rats: a ferritin-independent pathway. American Journal of Physiology 1997; 272: L268–L275
   PubMedGoogle Scholar
• Clark J.E., Saltzman D.J., Salaria R., Green C.J., Motterlini R. Myocardial preconditioning: possible involvement of heme oxygenase-1 in protection against ischaemia-reperfusion injury. 20th European Conference on Microcirculation, P.H. Carpentier, E. Vicaut, J.L. Guilmot. Monduzzi Editore Bologna. 1998; 113–117, In
   Google Scholar
• Poss K.D., Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proceeding of the National Academy of Sciences of the United States of America 1997; 94: 10925–10930
   PubMed Web of Science ®Google Scholar
• Soares M.P., Lin Y., Anrather J., Csizmadia E., Takigami K., Sato K., Grey S.T., Colvin R.P., Choi A.M., Poss K.D., Bach F.H. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nature Medicine 1998; 4: 1073–1077
   PubMed Web of Science ®Google Scholar
• Hancock W.W., Buelow R., Sayegh M.H., Turka L.A. Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes. Nature Medicine 1998; 4: 1392–1396
   PubMed Web of Science ®Google Scholar
• Coceani F., Kelsey L., Seidlitz E., Marks G.S., McLaughlin B.E., Vreman H.J., Stevenson D.K., Rabinovitch M., Ackerley C. Carbon monoxide formation in the ductus arteriosus in the lamb: implications for the regulation of muscle tone. British Journal of Pharmacology 1997; 120: 599–608
   PubMedGoogle Scholar
• Acevedo C.H., Ahmed A. Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy. Journal of Clinical Investigation 1998; 101: 949–955
   PubMed Web of Science ®Google Scholar
• Dennery P.A., Sridhar K.J., Lee C.S., Wong H.E., Shokoohi V., Rodgers P.A., Spitz D.R. Heme oxygenase-mediated resistance to oxygen toxicity in hamster fibroblasts. Journal of Biological Chemistry 1997; 272: 14937–14942
   PubMed Web of Science ®Google Scholar
• Moore E.G., Gibson Q.H. Cooperativity in the dissociation of nitric oxide from hemoglobin. Journal of Biological Chemistry 1976; 251: 2788–2794
   PubMed Web of Science ®Google Scholar
• Berger R.L., Davids N., Perrella M. Simulation of hemoglobin kinetics using finite element numerical methods. Methods in Enzymology 1994; 232: 517–558
   PubMedGoogle Scholar
• Sharma V.S., Ranney H.M. The dissociation of NO from nitrosylhemoglobin. Journal of Biological Chemistry 1978; 253: 6467–6472
   PubMedGoogle Scholar
• Gibson Q.H., Roughton F.J.W. The kinetics and equilibria of the reactions of nitric oxide with sheep hemoglobin. Journal of Physiology 1957; 136: 507–526
   PubMed Web of Science ®Google Scholar
• Motterlini R., Vandegriff K., Winslow R. Hemoglobin-NO interaction and its implications. Transfusion Medicine Review 1996; 10: 77–84
   PubMedGoogle Scholar
• Wennmalm A., Benthin G., Edlund A., Jungersten L., Kieler-Jensen N., Lundin S., Westfelt U.N., Petersson A.S., Waagstein F. Metabolism and excretion of nitric oxide in humans. An experimental and clinical study. Circulation Research 1993; 73: 1121–1127
   PubMed Web of Science ®Google Scholar
• Sjostrand T. Endogenous formation of carbon monoxide in man under normal and pathological conditions. Scandinavian Journal of Clinical and Laboratory Investigation 1949; 1: 201–214
   Web of Science ®Google Scholar
• Coburn R.F., Williams W.J., White P., Kahn S.B. The production of carbon monoxide from hemoglobin in vivo. Journal of Clinical Investigation 1967; 46: 346–356
   PubMed Web of Science ®Google Scholar
• Wagner C.T., Durante W., Christodoulides N., Hellums J.D., Schafer A.I. Hemodynamic forces induce the expression of heme oxygenase in cultured vascular smooth muscle cells. Journal of Clinical Investigation 1997; 100: 589–596
   PubMed Web of Science ®Google Scholar
• Mcquillan L.P., Leung G.K., Marsden P.A., Kostyk S.K., Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscriptional mechanisms. American Journal of Physiology 1995; 267: H1921–H1927
   Google Scholar
• Liao J.K., Zulueta J.J., Yu F.S., Peng H.B., Cote C.G., Hassoun P.M. Regulation of bovine endothelial constitutive nitric oxide synthase by oxygen. Journal of Clinical Investigation 1995; 96: 2661–2666
   PubMedGoogle Scholar
• Palmer L.A., Semenza G.L., Stoler M.H., Johns R.A. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIFf-1. American Journal of Physiology 1998; 274: L212–L219
   PubMed Web of Science ®Google Scholar
• Motterlini R., Foresti R., Salaria R., Clark J.E., Green C.J. Hypoxia induces endothelial heme oxygenase-1 via transient up-regulation of inducible nitric oxide synthase. Nitric Oxide: Biology and Chemistry 1998; 2: 317–317
   Google Scholar
• Caudill T.K., Resta T.C., Kanagy N.L., Walker B.R. Role of endothelial carbon monoxide in attenuated vasoreactivity following chronic hypoxia. American Journal of Physiology 1998; 275: R1025–R1030
   PubMedGoogle Scholar
• Morita T., Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. Journal of Clinical Investigation 1996; 96: 2676–2682
   Google Scholar
• Morita T., Mitsialis S.A., Koike H., Liu Y.X., Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. Journal of Biological Chemistry 1997; 272: 32804–32809
   PubMed Web of Science ®Google Scholar
• Hartsfield C.L., Alam J., Cook J.L., Choi A.M.K. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. American Journal of Physiology 1997; 273: L980–L988
   PubMedGoogle Scholar
• Vesely M.J.J., Green C.J., Motterlini R. Heme oxygenase-1 expression in skeletal muscle is fibre-type specific. 20th European Conference on Microcirculation, P.H. Carpentier, E. Vicaut, J.L. Guilmot. Monduzzi Editore, Bologna 1998; 279–282, In
   Google Scholar
• Essig D.A., Borger D.R., Jackson D.A. Induction of heme oxygenase-1 (HSP32) mRNA in skeletal muscle following contractions. American Journal of Physiology 1997; 272: C59–C67
   PubMed Web of Science ®Google Scholar
• Kobzik L., Reid M.B., Bredt D.S., Stamler J.S. Nitric oxide in skeletal muscle. Nature 1994; 372: 546–548
   PubMed Web of Science ®Google Scholar
• Kharitonov V.G., Sharma V.S., Pilz R.B., Magde D., Koesling D. Basis of guanylate cyclase activation by carbon monoxide. Proceeding of the National Academy of Sciences of the United States of America 1995; 92: 2568–2571
   PubMedGoogle Scholar
• Stone J.R., Marletta M.A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous states. Biochemistry 1994; 33: 5636–5640
   PubMed Web of Science ®Google Scholar
• Schmidt H.H.H.W., Lohmann S.M., Walter U. The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochimica Biophysica Acta 1993; 1178: 153–175
   PubMed Web of Science ®Google Scholar
• Ignarro L.J., Barrot B., Wood K.S. Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. Journal of Biological Chemistry 1984; 259: 6201–6207
   PubMedGoogle Scholar
• Friebe A., Schultz G., Koesling D. Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. Embo Journal 1996; 15: 6863–6868
   PubMed Web of Science ®Google Scholar
• Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 1994; 78: 931–936
   PubMed Web of Science ®Google Scholar
• Bolotina V.M., Najibi S., Palacino J.J., Pagano P.J., Cohen R.A. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 1994; 368: 850–853
   PubMed Web of Science ®Google Scholar
• Xu L., Eu J.P., Meissner G., Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 1998; 279: 234–237
   PubMed Web of Science ®Google Scholar
• Mannick J.B., Miao X.Q., Stamler J.S. Nitric oxide inhibits Fas-induced apoptosis. Journal of Biological Chemistry 1997; 272: 24125–24128
   PubMed Web of Science ®Google Scholar
• Rossig L., Fichtlscherer B., Breitschopf K., Haendeler J., Zeiher A.M., Mulsch A., Dimmeler S. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. Journal of Biological Chemistry 1999; 274: 6823–6826
   PubMed Web of Science ®Google Scholar
• Mannick J.B., Hausladen A., Liu L.M., Hess D.T., Zeng M., Miao Q.X., Kane L.S., Gow A.J., Stamler J.S. Fas-induced caspase denitrosylation. Science 1999; 284: 651–654
   PubMed Web of Science ®Google Scholar
• Nunoshiba T., deRojas-Walker T., Wishnok J.S., Tannenbaum S.R., Demple B. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proceeding of the National Academy of Sciences of the United States of America 1993; 90: 9993–9997
   PubMed Web of Science ®Google Scholar
• Hausladen A., Privalle C.T., Keng T., De Angelo J., Stamler J.S. Nitrosative stress: activation of the transcription factor OxyR. Cell 1996; 86: 719–729
   PubMed Web of Science ®Google Scholar
• Motterlini R., Hidalgo A., Sammut I., Shah K.A., Mohammed S., Srai K., Green C.J. A precursor of the nitric oxide donor SIN-1 modulates the stress protein heme oxygenase-1 in rat liver. Biochemical and Biophysical Research Communications 1996; 225: 167–172
   PubMedGoogle Scholar
• Clark J.E., Green C.J., Motterlini R. Involvement of the heme oxygenase-carbon monoxide pathway in keratinocytes. Biochemical and Biophysical Research Communications 1997; 241: 215–220
   PubMedGoogle Scholar
• Vesley M.J.J., Exon D.J., Clark J.E., Foresti R., Green C.J., Motterlini R. Heme oxygenase-1 induction in skeletal muscle cells: hemin and sodium nitroprus-side are regulators in vitro. American Journal of Physiology 1998; 275: C1087–C1094
   PubMedGoogle Scholar
• Kim Y.M., deVera M.E., Watkins S.C., Billiar T.R. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-a-induced apoptosis by inducing heat shock protein 70 expression. Journal of Biological Chemistry 1997; 272: 1402–1411
   PubMed Web of Science ®Google Scholar
• Malyshev I.Y., Manukhina E.B., Mikoyan V.D., Kubrina L.N., Vanin A.F. Nitric oxide is involved in heat-induced HSP70 accumulation. FEBS Letters 1995; 370: 159–162
   PubMed Web of Science ®Google Scholar
• Bolli R., Manchikalapudi S., Tang X.L., Takano H., Qiu Y.M., Guo Y.R., Zhang Q., Jadoon A.K. The protective effect of late preconditioning against myocardial stunning in conscious rabbits is mediated by nitric oxide synthase. Evidence that nitric oxide acts both as a trigger and as a mediator of the late phase of ischemic preconditioning. Circulation Research 1997; 81: 1094–1107
   PubMed Web of Science ®Google Scholar
• Takano H., Manchikalapudi S., Tang X.L., Qiu Y.M., Rizvi A., Jadoon A.K., Zhang Q., Bolli R. Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits. Circulation 1998; 98: 441–449
   PubMed Web of Science ®Google Scholar
• Qiu Y.M., Rizvi A., Tang X.L., Manchikalapudi S., Takano H., Jadoon A.K., Wu W.J., Bolli R. Nitric oxide triggers late preconditioning against myocardial infarction in conscious rabbits. American Journal of Physiology 1997; 273: H2931–H2936
   PubMedGoogle Scholar
• Wang R., Wu L.Y., Wang Z.Z. The direct effect of carbon monoxide on KCa channels in vascular smooth muscle cells. Pflugers Archives 1997; 434: 285–291
   PubMed Web of Science ®Google Scholar
• Wang R., Wu L. The chemical modification of KCa channels by carbon monoxide in vascular smooth muscle cells. Journal of Biological Chemistry 1997; 272: 8222–8226
   PubMed Web of Science ®Google Scholar
• Wang R., Wang Z.Z., Wu L.Y. Carbon monoxide-induced vasorelaxation and the underlying mechanisms. British Journal of Pharmacology 1997; 121: 927–934
   PubMed Web of Science ®Google Scholar
• Kerby R.L., Ludden P.W., Roberts G.P. Carbon monoxide-dependent growth of Rhodospirillum rubrum. Journal of Bacteriology 1995; 177: 2241–2244
   PubMedGoogle Scholar
• Shelver D., Kerby R.L., He Y.P., Roberts G.P. Carbon monoxide-induced activation of gene expression in Rhodospirillum rubrum requires the product of cooA, a member of the cyclic AMP receptor protein family of transcriptional regulators. Journal of Bacteriology 1995; 177: 2157–2163
   PubMed Web of Science ®Google Scholar
• Aono S., Nakajima H., Saito K., Okada M. A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in rhodospirillum-rubrum. Biochemical and Biophysical Research Communications 1996; 228: 752–756
   PubMedGoogle Scholar
• Shelver D., Kerby R.L., He Y.P., Roberts G.P. CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proceeding of the National Academy of Sciences of the United States of America 1997; 94: 11216–11220
   PubMedGoogle Scholar
• Bonam D., Ludden P.W. Purification and characterization of carbon monoxide dehydrogenase, a nickel, zinc, iron-sulfur protein, from Rhodospirillum rubrum. Journal of Biological Chemistry 1987; 262: 2980–2987
   PubMed Web of Science ®Google Scholar
• Young L.J., Caughey W.S. Mitochondrial oxygenation of carbon monoxide. Biochemical Journal 1986; 239: 225–227
   PubMedGoogle Scholar
• Young L.J., Caughey W.S. Oxygenation of carbon-monoxide by bovine heart cytochrome-c-oxidase. Biochemistry 1986; 25: 152–161
   PubMedGoogle Scholar
• Fenn W.O., Cobb D.M. The burning of carbon monoxide by heart and skeletal muscle. American Journal of Physiology 1932; 102: 393–401
   Google Scholar
• Stamler J.S., Simon D.I., Osborne J.A., Mullins M.E., Jaraki O., Michel T., Singel D.J., Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proceeding of the National Academy of Sciences of the United States of America 1992; 89: 444–448
   PubMed Web of Science ®Google Scholar
• Stamler J.S., Jaraki O., Osborne J., Simon D.I., Keaney J., Vita J., Singel D., Valeri C.R., Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proceeding of the National Academy of Sciences of the United States of America 1992; 89: 7674–7677
   PubMed Web of Science ®Google Scholar
• Jia L., Bonaventura C., Bonaventura J., Stamler J.S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996; 380: 221–226
   PubMed Web of Science ®Google Scholar
• Feelisch M., Stamler J.S. Preparation and detection of S-nitrosothiols. Methods in Nitric Oxide Research, M. Feelisch, J.S. Stamler. Wiley, New York 1996; 521–539, In
   Google Scholar
• Ewing J.F., Maines M.D. Glutathione depletion induces heme oxygenase-1 (HSP32) mRNA and protein in rat brain. Journal of Neurochemistry 1993; 60: 1512–1519
   PubMed Web of Science ®Google Scholar
• Grundemar L., Ny L. Pitfalls using metalloporphyrins in carbon monoxide research. Trends in Pharmacological Sciences 1997; 18: 193–195
   PubMed Web of Science ®Google Scholar
• Lee J., Hunt J.A., Groves J.T. Manganese porphyrins as redox-coupled peroxynitrite reductases. Journal of American Chemical Society 1998; 120: 6053–6061
   Web of Science ®Google Scholar
• Salvemini D., Wang Z.Q., Stern M.K., Currie M.G., Misko T.P. Peroxynitrite decomposition catalysts: therapeutics for peroxynitrite-mediated pathology. Proceeding of the National Academy of Sciences of the United States of America 1998; 95: 2659–2663
   PubMed Web of Science ®Google Scholar
• Misko T.P., Highkin M.K., Veenhuizen A.W., Manning P.T., Stern M.K., Currie M.G., Salvemini D. Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. Journal of Biological Chemistry 1998; 273: 15646–15653
   PubMed Web of Science ®Google Scholar
• Maines M.D. Carbon monoxide and nitric oxide homology: differential modulation of heme oxygenases in brain and detection of protein and activity. Methods in Enzymology 1996; 268: 473–488
   PubMedGoogle Scholar
• Hausladen A., Stamler J.S. Nitric oxide in plant immunity. Proceeding of the National Academy of Sciences of the United States of America 1998; 95: 10345–10347
   PubMedGoogle Scholar
• Schmidt H.H.H.W., Siebe J., Clement B., Feelisch M. 1H-[1,2,4]oxadiazolo(4,3-alquinoxalin-1-(ODQ) is not a selective inhibitor of soluble guanylyl cyclase: interference with NO-synthase and nitrovasodilator biotransformation. British Journal of Pharmacology 1998; 123: P6–P6
   Google Scholar
• Bryk R., Wolff D.J. Mechanism of inducible nitric oxide synthase inactivation by aminoguanidine and L-N6-(1-iminoethyl)lysine. Biochemistry 1998; 37: 4844–4852
   PubMedGoogle Scholar
• Motterlini R., Foresti R., Intaglietta M., Winslow R.M. Heme oxygenase activation by nitric oxide protects endothelial cells against oxidative stress. Pharmacological Research 1995; 31: 162–162
   Google Scholar
• Kim Y.M., Bergonia H.A., Muller C., Pitt B.R., Watkins W.D., Lancaster J.R., Jr. Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. Journal of Biological Chemistry 1995; 270: 5710–5713
   PubMed Web of Science ®Google Scholar
• Hara E., Takahashi K., Tominaga T., Kumabe T., Kayama T., Suzuki H., Fujita H., Yoshimoto T., Shirato K., Shibahara S. Expression of heme oxygenase and inducible nitric oxide synthase messenger RNA in human brain tumors. Biochemical and Biophysical Research Communications 1996; 224: 153–158
   PubMedGoogle Scholar
• 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. Journal of Hepatology 1999; 30: 61–69
   PubMed Web of Science ®Google Scholar
• Immenschuh S., Hinke V., Ohlmann A., GifhornKatz S., Katz N., Jungermann K., Kietzmann T. Transcriptional activation of the haem oxygenase-1 gene by cGMP via a cAMP resonse element activator protein-1 element in primary cultures of rat hepatocytes. Biochemical Journal 1998; 334: 141–146
   PubMedGoogle Scholar
• Feelisch M. The use of nitric oxide donors in pharmacological studies. Naunyn-Schmiedebergs Archives of Pharmacology 1998; 358: 113–122
   PubMed Web of Science ®Google Scholar
• Stamler J.S., Singel D.J., Loscalzo J. Biochemistry of nitric oxide and its redox activated forms. Science 1992; 258: 1898–1902
   PubMed Web of Science ®Google Scholar
• Xia Y., Roman L.J., Masters B.S.S., Zweier J.L. Inducible nitric-oxide synthase generates superoxide from the reductase domain. Journal of Biological Chemistry 1998; 273: 22635–22639
   PubMed Web of Science ®Google Scholar
• White K.A., Marletta M.A. Nitric oxide synthase is a cytochrome P 450 type protein. Journal of Biological Chemistry 1992; 269: 26390–26395
   Google Scholar
• Chakder S., Rathi S., Ma X.L., Rattan S. Heme oxygenase inhibitor zinc protoporphyrin-ix causes and activation of nitric-oxide synthase in the rabbit internal anal-sphincter. Journal of Pharmacology and Experimental Therapeutics 1996; 277: 1376–1382
   PubMedGoogle Scholar
• Gross S.S., Wolin M.S. Nitric-oxide: pathophysiological mechanisms. Annual Review of Physiology 1995; 57: 737–769
   PubMed Web of Science ®Google Scholar
• Turcanu V., Dhouib M., Poindron P. Nitric oxide synthase inhibition by haem oxygenase decreases macrophage nitric-oxide-dependent cytotoxicity: a negative feedback mechanism for the regulation of nitric oxide production. Research in Immunology 1998; 149: 741–744
   PubMedGoogle Scholar
• Hausladen A., Gow A.J., Stamler J.S. Nitrosative stress: metabolic pathway involving the flavohemoglobin. Proceeding of the National Academy of Sciences of the United States of America 1998; 95: 14100–14105
   PubMed Web of Science ®Google Scholar
• MembrilloHernandez J., Coopamah M.D., Anjum M.F., Stevanin T.M., Kelly A., Hughes M.N., Poole R.K. The flavohemoglobin of Escherichia Coli confers resistance to a nitrosating agent, a “nitric oxide releaser,” and paraquat and is essential for transcriptional responses to oxidative stress. Journal of Biological Chemistry 1999; 274: 748–754
   PubMedGoogle Scholar
• McDonagh A.F. Is bilirubin good for you. Clinics in Perinatology 1990; 17: 359–369
   PubMed Web of Science ®Google Scholar
• Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235: 1043–1046
   PubMed Web of Science ®Google Scholar
• Dennery P.A., McDonagh A.F., Spitz D.R., Rodgers P.A., Stevenson D.K. Hyperbilirubinemia results in reduced oxidative injury in neonatal gunn rats exposed to hyperoxia. Free Radical Biology and Medicine 1995; 19: 395–404
   PubMed Web of Science ®Google Scholar
• Hooper D.C., Spitsin S., Kean R.B., Champion J.M., Dickson G.M., Chaudhry I., Koprowski H. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proceeding of the National Academy of Sciences of the United States of America 1998; 95: 675–680
   PubMed Web of Science ®Google Scholar
• Skinner K.A., White C.R., Patel R., Tan S., Barnes S., Kirk M., Darley Usmar V., Parks D.A. Nitrosation of uric acid by peroxynitrite. Formation of a vasoactive nitric oxide donor. Journal of Biological Chemistry 1998; 273: 24491–24497
   PubMed Web of Science ®Google Scholar
• Lane N.J. Blood ties. Sciences-New York 1998; 38: 24–29
   Google Scholar
• Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. Journal of Clinical Investigation 1999; 103: 129–135
   PubMed Web of Science ®Google Scholar