Carbon monoxide: The bad and the good side of the coin, from neuronal death to anti-inflammatory activity

Inflammation Research

Volumn 55, Issue 7, 2006, Pages 261-273

  Mannaioni, P F ^a   Vannacci, A ^a   Masini, E ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Carbon monoxide; CO poisoning; Heme oxygenase; Inflammation, CO releasing molecules

Indexed keywords

3 NITROTYROSINE; ACETYLCYSTEINE; BIOCHEMICAL MARKER; CARBON MONOXIDE; FREE RADICAL; GLUTATHIONE; HEME OXYGENASE; MITOGEN ACTIVATED PROTEIN KINASE; NEURON SPECIFIC ENOLASE; NITRIC OXIDE SYNTHASE; PROTEIN S100B; REACTIVE OXYGEN METABOLITE; SCAVENGER; TEMPOL; XANTHINE DEHYDROGENASE;

AKINETIC MUTISM; AMNESIA; APOPTOSIS; BASOPHIL; BEHAVIOR CHANGE; BRAIN DAMAGE; BRAIN DISEASE; CARBON MONOXIDE INTOXICATION; CELL PROLIFERATION; CHEMICAL STRUCTURE; DEMYELINATION; GRAFT REJECTION; HUMAN; HYPERBARIC OXYGEN; INFLAMMATION; LETHARGY; LEUKOCYTE ADHERENCE; LEUKOPENIA; LIPID PEROXIDATION; MAST CELL; MEDICAL LITERATURE; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATION REDUCTION REACTION; OXYGEN THERAPY; PARKINSONISM; PLEIOTROPY; PROTEIN STRUCTURE; REOXYGENATION; REVIEW; THROMBOCYTE AGGREGATION INHIBITION; VASODILATATION; WHITE MATTER;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CARBON MONOXIDE; CARBON MONOXIDE POISONING; CELL DEATH; HEME OXYGENASE (DECYCLIZING); HUMANS; HYPERBARIC OXYGENATION; INFLAMMATION; MODELS, BIOLOGICAL; NEURONS;

EID: 33748480423     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-006-0084-y     Document Type: Review

References (125)

1. Weaver LK, Hopkins RO, Chan KJ, Churchill S, Elliott CG, Clemmer TP et al. Hyperbaric oxygen for acute carbon monoxide poisoning. N Engl J Med 2002; 347: 1057-67.
2. Cobb N and Etzel RA. Unintentional carbon monoxide-related deaths in the United States, 1979 through 1988. JAMA 1991; 266: 659-63.
3. Blumenthal I. Carbon monoxide poisoning. J R Soc Med 2001; 94: 270-2.
4. Annane D, Chevret S, Jars-Guincestre C, Chillet P, Elkharrat D, Gajdos P et al. Prognostic factors in unintentional mild carbon monoxide poisoning. Int Care Med 2001; 27: 1776-81.
5. Gandini C, Butera R, Locatelli C, Manzo L. Ossido di carbonio: in: Chiesara E, Mannaioni PF, Marozzi E (Eds) Tossicologia Medica, Torino, UTET. 2005.
6. Barret L, Danel V and Faure J. Carbon monoxide poisoning, a diagnosis frequently overlooked. J Toxicol Clin Toxicol 1985; 23: 309-13.
7. Varon J, Marik PE, Fromm RE, Jr, Gueler A. Carbon monoxide poisoning: a review for clinicians. J Emerg Med 1999; 17: 87-93.
8. Min SK. A brain syndrome associated with delayed neuropsychiatric sequelae following acute carbon monoxide intoxication. Acta Psychiatr Scand 1986; 73: 80-6.
9. Hart IK, Kennedy PG, Adams JH, Cunningham NE. Neurological manifestation of carbon monoxide poisoning. Postgrad Med J 1988; 64: 213-6.
10. Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology 2003; 187: 25-38.
11. Thom SR, Keim LW. Carbon monoxide poisoning: a review epidemiology, pathophysiology, clinical findings, and treatment options including hyperbaric oxygen therapy. J Toxicol Clin Toxicol 1989; 27: 141-56.
12. Yoshii F, Kozuma R, Takahashi W, Haida M, Takagi S, Shinohara Y. Magnetic resonance imaging and 11C-N-methylspiperone/positron emission tomography studies in a patient with the interval form of carbon monoxide poisoning. J Neurol Sci 1998; 160: 87-91.
13. Sakamoto K, Murata T, Omori M, Kimura H, Nishio M, Murata I et al. Clinical studies on three cases of the interval form of carbon monoxide poisoning: serial proton magnetic resonance spectroscopy as a prognostic predictor. Psych Res 1998; 83: 179-92.
14. Parkinson RB, Hopkins RO, Cleavinger HB, Weaver LK, Victoroff J, Foley JF et al. White matter hyperintensities and neuropsychological outcome following carbon monoxide poisoning. Neurology 2002; 58: 1525-32.
15. Hsiao CL, Kuo HC, Huang CC. Delayed encephalopathy after carbon monoxide intoxication-long-term prognosis and correlation of clinical manifestations and neuroimages. Acta Neurol Taiwan 2004; 13: 64-70.
16. Rasmussen LS, Poulsen MG, Christiansen M, Jansen EC. Biochemical markers for brain damage after carbon monoxide poisoning. Acta Anaesthesiol Scand 2004; 48: 469-73.
17. Sokal JA, Kralkowska E. The relationship between exposure duration, carboxyhemoglobin, blood glucose, pyruvate and lactate and the severity of intoxication in 39 cases of acute carbon monoxide poisoning in man. Arch Toxicol 1985; 57: 196-9.
18. Thom SR, Dehydrogenase conversion to oxidase and lipid peroxidation in brain after carbon monoxide poisoning. J Appl Physiol 1992; 73: 1584-9.
19. Zhang J, Piantadosi CA. Mitochondrial oxidative stress after carbon monoxide hypoxia in the rat brain. J Clin Invest 1992; 90: 1193-9.
20. Halperin MH, McFarland RA, Niven JI, Roughton FJ. The time course of the effects of carbon monoxide on visual thresholds. J Physiol 1959; 146: 583-93.
21. Thom SR. Leukocytes in carbon monoxide-mediated brain oxidative injury. Toxicol Appl Pharmacol 1993; 123: 234-47.
22. Ischiropoulos H, Beers MF, Ohnishi ST, Fisher D, Garner SE, Thom SR. Nitric oxide production and perivascular nitration in brain after carbon monoxide poisoning in the rat. J Clin Invest 1996; 97: 2260-7.
23. Sluijter ME. The treatment of carbon monoxide poisoning by administration of oxygen at high atmospheric pressure. Prog Brain Res 1967; 24: 123-82.
24. Jamieson D, Chance B, Cadenas E, Boveris A. The relation of free radical production to hyperoxia. Annu Rev Physiol 1986; 48: 703-19.
25. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 1981; 256: 10986-92.
26. Hansen TN, Smith CV, Gest AL, Smith HW, Giesler M. Biochemical manifestations of oxygen toxicity in the newborn lamb. Pediatr Res 1990; 28: 613-7.
27. Dennog C, Radermacher P, Barnett YA, Speit G. Antioxidant status in humans after exposure to hyperbaric oxygen. Mutat Res 1999; 428: 83-9.
28. Benedetti S, Lamorgese A, Piersantelli M, Pagliarani S, Benvenuti F, Canestrari F. Oxidative stress and antioxidant status in patients undergoing prolonged exposure to hyperbaric oxygen. Clin Biochem 2004; 37: 312-7.
29. Lu MY, Kang BH, Wan FJ, Chen CS, Huang KL. Hyperbaric oxygen attenuates lipopolysaccharide-induced acute lung injury. Intensive Care Med 2002; 28: 636-41.
30. Pedoto A, Nandi J, Yang ZJ, Wang J, Bosco G, Oler A et al. Beneficial effect of hyperbaric oxygen pretreatment on lipopolysaccharide-induced shock in rats. Clin Exp Pharmacol Physiol 2003; 30: 482-8.
31. Padgaonkar VA, Giblin FJ, Fowler K, Leverenz VR, Reddan JR, Dziedzic DC. Heme oxygenase synthesis is induced in cultured lens epithelium by hyperbaric oxygen or puromycin. Exp Eye Res 1997; 65: 435-43.
32. Speit G, Dennog C, Eichhorn U, Rothfuss A, Kaina B. Induction of heme oxygenase-1 and adaptive protection against the induction of DNA damage after hyperbaric oxygen treatment. Carcinogenesis 2000; 21: 1795-9.
33. Huang TY, Tsai PS, Wang TY, Huang CL, Huang CJ. Hyperbaric oxygen attenuation of lipopolysaccharide-induced acute lung injury involves heme oxygenase-1. Acta Anaesthesiol Scand 2005; 49: 1293-301.
34. Foresti R, Motterlini R. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic Res 1999; 31: 459-75.
35. Bishop A, Yet SF, Lee ME, Perrella MA, Demple B. A key role for heme oxygenase-1 in nitric oxide resistance in murine motor neurons and glia. Biochem Biophys Res Commun 2004; 325: 3-9.
36. Zuckerbraun BS, Billiar TR. Heme oxygenase-1: a cellular Hercules. Hepatology 2003; 37: 742-4.
37. Thiemermann C. Inhaled CO: deadly gas or novel therapeutic? Nat Med 2001; 7: 534-5.
38. Mathieu D, Nolf M, Durocher A, Saulnier F, Frimat P, Furon D et al. Acute carbon monoxide poisoning. Risk of late sequelae and treatment by hyperbaric oxygen. J Toxicol Clin Toxicol 1985; 23: 315-24.
39. Hampson NB, Simonson SG, Kramer CC. Piantadosi CA. Central nervous system oxygen toxicity during hyperbaric treatment of patients with carbon monoxide poisoning. Undersea Hyperb Med 1996; 23: 215-9.
40. Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology 2003; 187: 25-38.
41. Murata M, Suzuki M, Hasegawa Y, Nohara S, Kurachi M. Improvement of occipital alpha activity by repetitive hyperbaric oxygen therapy in patients with carbon monoxide poisoning: a possible indicator for treatment efficacy. J Neurol Sci 2005; 235: 69-74.
42. Juurlink DN, Buckley NA, Stanbrook MB, Isbister GK, Bennett M, McGuigan MA. Hyperbaric oxygen for carbon monoxide poisoning. Cochrane Database Syst Rev 2005; CD002041.
43. Grehant M. Les gaz du sang. C. Masson, Paris, In. 1894.
44. de Saint-Martin, SVR. Le dosage de petites quantites di oxide de carbone dans l'air et dans le sang normal. CR Acad Sci 1898; 126: 1036-9.
45. Sjostrand T. Endogenous formation of carbon monoxide in man under normal and pathological conditions. Scand J Clin Lab Invest 1949; 1: 201-14.
46. Engstedt L. Endogenous formation of carbon monoxide in hemolytic disease; with special regard to quantitative comparisons to other hemolytic indices. Acta Med Scand 1957; 159: 1-63.
47. Pugh LG. Carbon monoxide content of the blood and other observations on Weddell seals. Nature 1959; 183: 74-6.
48. Coburn RF, Blakemore WS, Forster RE. Endogenous carbon monoxide production in man. J Clin Invest 1963; 42: 1172-8.
49. Coburn RF, Forster RE, Kane PB. Considerations of the physiological variables that determine the blood carboxyhemoglobin concentration in man. J Clin Invest 1965; 44: 1899-910.
50. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 1968; 61: 748-55.
51. Abraham NG, Lin JH, Schwartzman ML, Levere RD, Shibahara S. The physiological significance of heme oxygenase. Int J Biochem 1988; 20: 543-58.
52. Maines MD. New developments in the regulation of heme metabolism and their implications. Crit Rev Toxicol 1984; 12: 241-314.
53. Elbirt KK, Bonkovsky HL. Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 1999; 111: 438-47.
54. Abraham NG (Ed). Heme oxygenase in biology and medicine. Kluwer Academic/Plenum Publishers New York, Boston, 2002.
55. Marks GS. Heme oxygenase: the physiological role of one of its metabolites, carbon monoxide and interactions with zinc protoporphyrin, cobalt protoporphyrin and other metalloporphyrins. Cell Mol Biol (Noisy-le-grand) 1994; 40: 863-70.
56. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays 2004; 26: 270-80.
57. Villamor E, Perez-Vizcaino F, Cogolludo AL, Conde-Oviedo J, Zaragoza-Arnaez F, Lopez-Lopez JG et al. Relaxant effects of carbon monoxide compared with nitric oxide in pulmonary and systemic vessels of newborn piglets. Pediatr Res 2000; 48: 546-53.
58. Song R, Mahidhara RS, Liu F, Ning W, Otterbein LE, Choi AM. Carbon monoxide inhibits human airway smooth muscle cell proliferation via mitogen-activated protein kinase pathway. Am J RespirCell Mol Biol 2002; 27: 603-10.
59. Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 2000; 192: 1015-26.
60. Shu-Hui J, Chau LY. Induction of apoptosis in vascular smooth muscle cells by heme oxygenase-1 derived carbon monoxide. In: Abraham NG (Ed), Heme oxygenase in biology and medicine. Kluwer Academic/Plenum Publishers, 2002; 439-49.
61. Nakao A, Kimizuka K, Stolz DB, Neto JS, Kaizu T, Choi AM et al. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am J Pathol 2003; 163: 1587-98.
62. Song R, Kubo M, Morse D, Zhou Z, Zhang X, Dauber JH et al. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am J Pathol 2003; 163: 231-42.
63. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 1987; 32: 497-504.
64. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science 1993; 259: 381-4.
65. Yamamoto T, Nozaki-Taguchi N. 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 1995; 704: 256-62.
66. Parfenova H, Daley ML, Carratu P, Leffler CW. Heme oxygenase inhibition reduces neuronal activation evoked by bicuculline in newborn pigs. Brain Res 2004; 1014: 87-96.
67. Otterbein LE, Bach FH, Alam J, Soares M, Tao LH, Wysk M et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6: 422-8.
68. Pae HO, Oh GS, Choi BM, Chae SC, Kim YM, Chung KR et al. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of IL-2 production. J Immunol 2004; 172: 4744-51.
69. Dijkstra G, Blokzijl H, Bok L, Homan M, van Goor H, Faber KN et al. Opposite effect of oxidative stress on inducible nitric oxide synthase and haem oxygenase-1 expression in intestinal inflammation: anti-inflammatory effect of carbon monoxide. J Pathol 2004; 204: 296-303.
70. Tsui TY, Siu YT, Schlitt HJ, Fan ST. Heme oxygenase-1-derived carbon monoxide stimulates adenosine triphosphate generation in human hepatocyte. Biochem Biophys Res Commun 2005; 336: 898-902.
71. Gibbons SJ, Farrugia G. The role of carbon monoxide in the gastrointestinal tract. J Physiol 2004; 556: 325-36.
72. Sacerdoti D, Abraham NG, Oyekan AO, Yang L, Gatta A, McGiff JC. Role of the heme oxygenases in abnormalities of the mesenteric circulation in cirrhotic rats. J Pharmacol Exp Ther 2004; 308: 636-43.
73. Suematsu M, Tsukada K, Tajima T, Yamamoto T, Ochiai D, Watanabe H et al. Carbon monoxide as a guardian against hepatobiliary dysfunction. Alcohol Clin Exp Res 2005; 29: 134S-139S.
74. Zhou HL, Lu FH, Latham C, Zander DS, Visner GA. Heme oxygenase-1 expression in human lungs with cystic fibrosis and cytoprotective effects against Pseudomonas aeruginosa in vitro. Am J Resp Critical Care Med 2004; 170: 633-40.
75. Chauveau C, Remy S, Royer PJ, Hill M, Tanguy-Royer S, Hubert FX et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 2005; 106: 1694-702.
76. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999; 276: L688-L694.
77. Dolinay T, Szilasi M, Liu M, Choi AM. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury. Am J Respir Crit Care Med 2004; 170: 613-20.
78. Zayasu K, Sekizawa K, Okinaga S, Yamaya M, Ohrui T, Sasaki H. Increased carbon monoxide in exhaled air of asthmatic patients. Am J Respir Crit Care Med 1997; 156: 1140-3.
79. Shi Y, Pan F, Li H, Pan J, Qin S, Jiang D, Shen C. Plasma carbon monoxide levels in term newborn infants with sepsis. Biol Neonate 2000; 78: 230-2.
80. Carter EP, Garat C, Imamura M. Continual emerging roles of HO-1: protection against airway inflammation. Am J Physiol Lung Cell Mol Physiol 2004; 287: L24-L25.
81. Mayr FB, Spiel A, Leitner J, Marsik C, Germann P, Ullrich R et al. Effects of carbon monoxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 2005; 171: 354-60.
82. Willis D, Moore AR, Frederick R, Willoughby DA. Heme oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 1996; 2: 87-90.
83. Chung SW, Chen YH, Perrella MA. Role of Ets-2 in the regulation of heme oxygenase-1 by endotoxin. J Biol Chem 2005; 280: 4578-84.
84. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165: 1045-53.
85. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 1999; 103: 129-35.
86. Neto JS, Nakao A, Kimizuka K, Romanosky AJ, Stolz DB, Uchiyama T et al. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol 2004; 287: F979-F989.
87. Ott MC, Scott JR, Bihari A, Badhwar A, Otterbein LE, Gray DK et al. Inhalation of carbon monoxide prevents liver injury and inflammation following hind limb ischemia/reperfusion. FASEB J 2005; 19: 106-8.
88. Nakao A, Moore BA, Murase N, Liu F, Zuckerbraun BS, Bach FH et al. Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility. Gut 2003; 52: 1278-85.
89. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med 2005; 202: 1703-13.
90. Zuckerbraun BS, Otterbein LE, Boyle P, Jaffe R, Upperman J, Zamora R et al. Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2005; 289: G607-G613.
91. Devesa I, Ferrandiz ML, Guillen I, Cerda JM, Alcaraz MJ. Potential role of heme oxygenase-1 in the progression of rat adjuvant arthritis. Lab Invest 2005; 85: 34-44.
92. Di Bello MG, Berni L, Gai P, Mirabella C, Ndisang JF, Masini E et al. A regulatory role for carbon monoxide in mast cell function. Inflamm Res 1998; 47 Suppl 1: S7-S8.
93. Ndisang JF, Gai P, Berni L, Mirabella C, Baronti R, Mannaioni PF et al. Modulation of the immunological response of guinea pig mast cells by carbon monoxide. Immunopharmacology 1999; 43: 65-73.
94. Pearce FL, Ennis M. Isolation and some properties of mast cells from the mesentery of the rat and guinea pig. Agents Actions 1980; 10: 124-31.
95. Foreman JC. Mst cells and basophil leukocytes. In: Dale MM, Foreman JC (Eds). Text book or immunopharmacology Blackwell, Oxford, 1984; 49-53.
96. Vannacci A, Baronti R, Zagli G, Marzocca C, Pierpaoli S, Bani D et al. Carbon monoxide modulates the response of human basophils to FcepsilonRI stimulation through the heme oxygenase pathway. Eur J Pharmacol 2003; 465: 289-97.
97. Ndisang JF, Wang R, Vannacci A, Marzocca C, Fantappie O, Mazzanti R et al. Haeme oxygenase-1 and cardiac anaphylaxis. Br J Pharmacol 2001; 134: 1689-96.
98. Ndisang J F, Masini E, Mannaioni PF, Wang R. Carbon monoxide and cardiovascular inflammation. In: Wang R (Ed). Carbon monoxide and cardiovascular functions. CRC press, 2002; 165-80.
99. Ndisang JF, Moncini M, Gai P, Berni L, Cecere G, Masini E et al. Induction of heme oxygenase provides protection against cardiac anaphylaxis. Inflamm Res 2000; 49 Suppl 1: S76-S77.
100. Vannacci A, Marzocca C, Zagli G, Pierpaoli S, Bani D, Masini E et al. Generation of nitric oxide and carbon monoxide provides protection against cardiac anaphylaxis. In: Abraham Nader G (Ed). Heme oxigenase in biology and medicine, Kluwer Academic/Plenum publishers, 2002; 431-5.
101. + channels. In: Carbon monoxide and cardio-vascular functions. Wang R (Ed). CRC press 2002; 83-102.
102. Dubuis E, Potier M, Wang R, Vandier C. Continuous inhalation of carbon monoxide attenuates hypoxic pulmonary hypertension development presumably through activation of BKCa channels. Cardiovasc Res 2005; 65: 751-61.
103. Motterlini R, Foresti R, Intaglietta M, Winslow RM. NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol 1996; 270: H107-H114.
104. 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 1999; 30: 61-9.
105. Giannini L, Vannacci A, Fabrizi F, Uliva C, Bani D, Masini E et al. Protection from cardiac injury by induction of heme oxygenase-1 and nitric oxide synthase in a focal ischemia/ reperfusion model. Cell Mol Biol 2005; 51: 383-401.
106. Otterbein LE. Carbon monoxide: innovative anti-inflammatory properties of an age-old gas molecule. Antioxid Redox Signal 2002; 4: 309-19.
107. Goldstein L, Teng ZP, Zeserson E, Patel M, Regan RF. Hemin induces an iron-dependent, oxidative injury to human neuron-like cells. J Neurosci Res 2003; 73: 113-21.
108. Chauveau C, Bouchet D, Roussel JC, Mathieu P, Braudeau C, Renaudin K et al. Gene transfer of heme oxygenase-1 and carbon monoxide delivery inhibit chronic rejection. Am J Transplant 2002; 2: 581-92.
109. Alessio E, Milani B, Bolle M, Mestroni G, Faleschini P, Todone F et al. Carbonyl Derivatives of Chloride Dimethyl-Sulfoxide Ruthenium(Ii) Complexes - Synthesis, Structural Characterization, and Reactivity of Ru(Co)(X)(Dmso)(4-X) Cl-2 Complexes (X=1-3). Inorg Chem 1995; 34: 4722-34.
110. Motterlini R, Foresti R, Green JC. Studies on the development of carbon monoxide releasing molecular: potential application for the treatment of cardio-vascular dysfunction. In: Wang R (Ed). Carbon monoxide and cardiovascular functions. CRC press 2002; 249-71.
111. Herrman WA. 100 years of metal carbonyls: a seren-dipitous chemical discovery of major scientific and industrial impact. J Organo Met Chem 1990; 383: 21-44.
112. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 2002; 90: E17-E24.
113. Vannacci A, Di Felice A, Giannini L, Marzocca C, Pierpaoli S, Zagli G et al. The effect of a carbon monoxide-releasing molecule on the immunological activation of guinea-pig mast cells and human basophils. Inflamm Res 2004; 53: S9-S10.
114. Clark JE, Naughton P, Shurey S, Green CJ, Johnson TR, Mann BE et al. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res 2003; 93: E2-E8.
115. Guo Y, Stein AB, Wu WJ, Tan W, Zhu X, Li QH et al. Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am J Physiol Heart Circ Physiol 2004; 286: H1649-H1653.
116. Vannacci A, Marzocca C, Giannini L, Mazzetti L, Franchi-Micheli S, Failli P et al. Evalutation of the effects of a novel carbon monoxide releasing molecole (CORM-3) in an in vitro model of cardio-vascular inflammation. Inflamm Res; in press
117. Motterlini R, Sawle P, Hammad J, Bains S, Alberto R, Foresti R et al. CORM-A1: a new pharmacologically active carbon monoxide-releasing molecule. FASEB J 2005; 19: 284-6.
118. Friebe A, Schultz G, Koesling D. Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. EMBO J 1996; 15: 6863-8.
119. Thom SR. Antagonism of carbon monoxide-mediated brain lipid peroxidation by hyperbaric oxygen. Toxicol Appl Pharmacol 1990; 105: 340-4.
120. Brown SD, Piantadosi CA. Invivo Binding of Carbon-Monoxide to Cytochrome-C Oxidase in Rat-Brain. J Appl Physiol 1990; 68: 604-10.
121. Wang R (Ed). Carbon monoxide and cardiovascular functions. Boca Raton London New York Washington: CRC press 2003.
122. Grosser N, Abate A, Oberle S, Vreman HJ, Dennery PA, Becker JC et al. Heme oxygenase-1 induction may explain the antioxidant profile of aspirin. Biochem Biophys Res Commun 2003; 308: 956-60.
123. Chiang N, Bermudez EA, Ridker PM, Hurwitz S, Serhan CN. Aspirin triggers antiinflammatory 15-epi-lipoxin A4 and inhibits thromboxane in a randomized human trial. Proc Natl Acad Sci USA 2004; 101: 15178-83.
124. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, Villela CG, Fierro IM. Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am J Physiol Cell Physiol 2005; 289: C557-C563.
125. Barinaga M. Carbon-Monoxide - Killer to Brain Messenger in One-Step. Science 1993; 259: 309