Carbon monoxide: Present and future indications for a medical gas

Korean Journal of Internal Medicine

Volumn 28, Issue 2, 2013, Pages 123-140

  Ryter, Stefan W ^a   Choi, Augustine M K ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Acute lung injury; Carbon monoxide; Heme oxygenase (decyclizing); Reperfusion injury; Sepsis

Indexed keywords

BUDESONIDE; CARBON MONOXIDE; HEME OXYGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ANTIINFLAMMATORY AGENT; GAS; HEME; POLLUTANT;

ACUTE LUNG INJURY; ANTIINFLAMMATORY ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; CARBON MONOXIDE INTOXICATION; CELL PROLIFERATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL EVALUATION; DRUG EFFICACY; DRUG MECHANISM; ENVIRONMENTAL EXPOSURE; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; LUNG FIBROSIS; NONHUMAN; ORGAN INJURY; ORGAN TRANSPLANTATION; PHYSICAL CHEMISTRY; PREECLAMPSIA; PULMONARY HYPERTENSION; REPERFUSION INJURY; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STOMACH PARESIS; TRANSCRIPTION REGULATION; TREATMENT DURATION; TREATMENT RESPONSE; VENTILATOR INDUCED LUNG INJURY; ANIMAL; DOSE RESPONSE; EXPOSURE; GAS; INHALATIONAL DRUG ADMINISTRATION; METABOLISM; POLLUTANT; RISK ASSESSMENT;

ADMINISTRATION, INHALATION; ANIMALS; ANTI-INFLAMMATORY AGENTS; CARBON MONOXIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; GASES; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; INHALATION EXPOSURE; RISK ASSESSMENT; SIGNAL TRANSDUCTION;

EID: 84875531912     PISSN: 12263303     EISSN: 20056648     Source Type: Journal    
DOI: 10.3904/kjim.2013.28.2.123     Document Type: Review

References (170)

1. Gentile MA. Inhaled medical gases: more to breathe than oxygen. Respir Care 2011;56:1341-1357.
2. Kashiba M, Kajimura M, Goda N, Suematsu M. From O2 to H2S: a landscape view of gas biology. Keio J Med 2002;51:1-10.
3. Nakao A, Sugimoto R, Billiar TR, McCurry KR. Thera peutic antioxidant medical gas. J Clin Biochem Nutr 2009;44:1-13.
4. Bloch KD, Ichinose F, Roberts JD Jr, Zapol WM. Inhaled NO as a therapeutic agent. Cardiovasc Res 2007 75:339-348.
5. Ryter SW, Choi AM. Gaseous therapeutics in acute lung injury. Compr Physiol 2011;1:105-121.
6. Ryter SW, Choi AM. Heme oxygenase-1/carbon monox ide: from metabolism to molecular therapy. Am J Respir Cell Mol Biol 2009;41:251-260.
7. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applica tions. Physiol Rev 2006;86:583-650.
8. Ryter SW, Morse D, Choi AM. Carbon monoxide: to boldly go where NO has gone before. Sci STKE 2004;2004:RE6.
9. Wu L, Wang R. Carbon monoxide: endogenous produc tion, physiological functions, and pharmacological ap plications. Pharmacol Rev 2005;57:585-630.
10. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays 2004;26:270-280.
11. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 2010 9:728-743.
12. Kashfi K, Olson KR. Biology and therapeutic potential ofhydrogen sulfide and hydrogen sulfide-releasing chi meras. Biochem Pharmacol 2013;85:689-703.
13. Wagner F, Asfar P, Calzia E, Radermacher P, Szabo C. Bench-to-bedside review: hydrogen sulfide: the third gaseous transmitter: applications for critical care. Crit Care 2009;13:213.
14. Liu YH, Yan CD, Bian JS. Hydrogen sulfide: a novel signaling molecule in the vascular system. J Cardiovasc Pharmacol 2011;58:560-569.
15. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 2002;16:1792-1798.
16. Moody BF, Calvert JW. Emergent role of gasotrans- mitters in ischemia-reperfusion injury. Med Gas Res 2011;1:3.
17. Wink DA, Mitchell JB. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotec- tive mechanisms of nitric oxide. Free Radic Biol Med 1998;25:434-456.
18. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A 1968;61:748-755.
19. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase: characterization of the enzyme. J Biol Chem 1969;244:6388-6394.
20. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32- kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arse- nite. Proc Natl Acad Sci U S A 1989;86:99-103.
21. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-554.
22. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase: only one molecular species of the enzyme is inducible. J Biol Chem 1986;261:411-419.
23. Vandiver M, Snyder SH. Hydrogen sulfide: a gaso- transmitter of clinical relevance. J Mol Med (Berl) 2012;90:255-263.
24. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987;84:9265-9269.
25. Ignarro LJ, Byrns RE, Buga GM, Wood KS. Endotheli um-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical proper ties identical to those of nitric oxide radical. Circ Res 1987;61:866-879.
26. Moncada S, Palmer RM, Higgs EA. Nitric oxide: physi ology, pathophysiology, and pharmacology. Pharmacol Rev 1991;43:109-142.
27. Ignarro LJ. Nitric oxide: a unique endogenous signaling molecule in vascular biology. Biosci Rep 1999;19:51-71.
28. Snyder SH, Bredt DS. Biological roles of nitric oxide. Sci Am 1992;266:68-77.
29. Derbyshire ER, Marletta MA. Structure and regula tion of soluble guanylate cyclase. Annu Rev Biochem 2012;81:533-559.
30. Ichinose F, Roberts JD Jr, Zapol WM. Inhaled nitric ox ide: a selective pulmonary vasodilator: current uses and therapeutic potential. Circulation 2004;109:3106-3111.
31. Frostell C, Fratacci MD, Wain JC, Jones R, Zapol WM. Inhaled nitric oxide: a selective pulmonary vasodilator reversing hypoxic pulmonary vasoconstriction. Circu lation 1991;83:2038-2047.
32. Rossaint R, Falke KJ, Lopez F, Slama K, Pison U, Zapol WM. Inhaled nitric oxide for the adult respiratory dis tress syndrome. N Engl J Med 1993;328:399-405.
33. Porta NF, Steinhorn RH. Pulmonary vasodilator ther apy in the NICU: inhaled nitric oxide, sildenafil, and other pulmonary vasodilating agents. Clin Perinatol 2012;39:149-164.
34. Hartsfield CL. Cross talk between carbon monoxide and nitric oxide. Antioxid Redox Signal 2002;4:301-307.
35. Piantadosi CA. Biological chemistry of carbon monox ide. Antioxid Redox Signal 2002;4:259-270.
36. Sjostrand T. The formation of carbon monoxide by the decomposition of haemoglobin in vivo. Acta Physiol Scand 1952;26:338-344.
37. Sjostrand T. Endogenous production of carbon monox ide in man under normal and pathophysiological con ditions. Scand J Clin Lab Invest 1949;1:201-214.
38. Coburn RF, Blakemore WS, Forster RE. Endogenous carbon monoxide production in man. J Clin Invest 1963;42:1172-1178.
39. Tenhunen R, Marver HS, Schmid R. The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin. J Lab Clin Med 1970;75: 410-421.
40. Kageyama H, Hiwasa T, Tokunaga K, Sakiyama S. Isolation and characterization of a complementary DNA clone for a Mr 32,000 protein which is induced with tumor promoters in BALB/c 3T3 cells. Cancer Res 1988;48:4795-4798.
41. Keyse SM, Tyrrell RM. Both near ultraviolet radiation and the oxidizing agent hydrogen peroxide induce a 32- kDa stress protein in normal human skin fibroblasts. J Biol Chem 1987;262:14821-14825.
42. Applegate LA, Luscher P, Tyrrell RM. Induction ofheme oxygenase: a general response to oxidant stress in cul tured mammalian cells. Cancer Res 1991;51:974-978.
43. Otterbein LE, Bach FH, Alam J, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000 6:422-428.
44. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science 1993;259:381-384.
45. Brouard S, Otterbein LE, Anrather J, et al. Carbon mon oxide generated by heme oxygenase 1 suppresses endo thelial cell apoptosis. J Exp Med 2000;192:1015-1026.
46. Kim HP, Ryter SW, Choi AM. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 2006;46:411-449.
47. Durante W, Johnson FK, Johnson RA. Role of carbon monoxide in cardiovascular function. J Cell Mol Med 2006;10:672-686.
48. Suematsu M, Kashiwagi S, Sano T, Goda N, Shinoda Y, Ishimura Y. Carbon monoxide as an endogenous modu lator of hepatic vascular perfusion. Biochem Biophys Res Commun 1994;205:1333-1337.
49. Morita T, Mitsialis SA, Koike H, Liu Y, Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem 1997;272:32804-32809.
50. Suliman HB, Carraway MS, Tatro LG, Piantadosi CA. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci 2007;120(Pt 2):299-308.
51. Lee SJ, Ryter SW, Xu JF, et al. Carbon monoxide activates autophagy via mitochondrial reactive oxygen species formation. Am J Respir Cell Mol Biol 2011 45:867-873.
52. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999 276 (4 Pt 1):L688-L694.
53. Otterbein LE, Otterbein SL, Ifedigbo E, et al. MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant- induced lung injury. Am J Pathol 2003;163:2555-2563.
54. 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;170:613-620.
55. Zhang X, Shan P, Alam J, Davis RJ, Flavell RA, Lee PJ. Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen- activated protein kinase pathway during ischemia- reperfusion lung injury. J Biol Chem 2003;278:22061-22070.
56. Zhang X, Shan P, Otterbein LE, et al. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem 2003;278:1248-1258.
57. MacGarvey NC, Suliman HB, Bartz RR, et al. Activa tion of mitochondrial biogenesis by heme oxygenase-1- mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am J Respir Crit Care Med 2012;185:851-861.
58. Otterbein LE, Zuckerbraun BS, Haga M, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 2003;9:183-190.
59. Sato K, Balla J, Otterbein L, et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejec tion of mouse-to-rat cardiac transplants. J Immunol 2001;166:4185-4194.
60. Song R, Kubo M, Morse D, et al. Carbon monoxide in duces cytoprotection in rat orthotopic lung transplanta tion via anti-inflammatory and anti-apoptotic effects. Am J Pathol 2003;163:231-242.
61. Ryter SW, Choi AM. Heme oxygenase-1/carbon monox ide: novel therapeutic strategies in critical care medi cine. Curr Drug Targets 2010;11:1485-1494.
62. Whiteman M, Le Trionnaire S, Chopra M, Fox B, Whatmore J. Emerging role of hydrogen sulfide in health and disease: critical appraisal ofbiomarkers and pharmaco logical tools. Clin Sci (Lond) 2011;121:459-488.
63. Yang G, Wu L, Jiang B, et al. H2S as a physiologic vaso relaxant: hypertension in mice with deletion of cysta thionine gamma-lyase. Science 2008;322:587-590.
64. Kimura H. Hydrogen sulfide as a neuromodulator. Mol Neurobiol 2002;26:13-19.
65. Szabo C. Hydrogen sulphide and its therapeutic poten tial. Nat Rev Drug Discov 2007;6:917-935.
66. Lowicka E, Beltowski J. Hydrogen sulfide (H2S): the third gas of interest for pharmacologists. Pharmacol Rep 2007;59:4-24.
67. Faller S, Spassov SG, Zimmermann KK, et al. Hydrogen sulfide prevents hyperoxia-induced lung injury by downregulating reactive oxygen species formation and angiopoietin-2 release. Curr Pharm Des. 2012 Oct 18 [Epub].
68. Faller S, Ryter SW, Choi AM, Loop T, Schmidt R, Hoetzel A. Inhaled hydrogen sulfide protects against venti lator-induced lung injury. Anesthesiology 2010;113:104-115.
69. Spiller F, Orrico MI, Nascimento DC, et al. Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am J Respir Crit Care Med 2010;182:360-368.
70. Von Burg R. Carbon monoxide. J Appl Toxicol 1999;19:379-386.
71. Penney D, Benignus V, Kephalopoulos S, Kotzias D, Kleinman M, Verrier A. Carbon monoxide. In: World Health Organization, ed. WHO Guidelines for Indoor Air Quality: Selected Pollutants. Copenhagen: WHO, 2010:55.
72. Raub J. Environmental Health Criteria 213. Carbon Monoxide Second Edition. Geneva: WHO, 1999, 70.
73. Smith RP. Toxic responses of the blood. In: Casarett LJ, Doull J, Klaassen CD, Amdur MO, eds. Casarett and Doull's Toxicology: the Basic Science of Poisons. 3rd ed. New York: Macmillan, 1986:223-224.
74. Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology 2003 187:25-38.
75. Piantadosi CA. Diagnosis and treatment of carbon monoxide poisoning. Respir Care Clin N Am 1999 5:183-202.
76. Rudra CB, Williams MA, Sheppard L, et al. Relation of whole blood carboxyhemoglobin concentration to ambi ent carbon monoxide exposure estimated using regres sion. Am J Epidemiol 2010;171:942-951.
77. Russell MA. Blood carboxyhaemoglobin changes dur ing tobacco smoking. Postgrad Med J 1973;49:684-687.
78. Samoli E, Touloumi G, Schwartz J, et al. Short-term effects of carbon monoxide on mortality: an analysis within the APHEA project. Environ Health Perspect 2007;115:1578-1583.
79. Reboul C, Thireau J, Meyer G, et al. Carbon monoxide exposure in the urban environment: an insidious foe for the heart? Respir Physiol Neurobiol 2012 184:204-212.
80. Kutty RK, Daniel RF, Ryan DE, Levin W, Maines MD. Rat liver cytochrome P-450b, P-420b, and P-420c are de graded to biliverdin by heme oxygenase. Arch Biochem Biophys 1988;260:638-644.
81. Tenhunen R, Ross ME, Marver HS, Schmid R. Reduced nicotinamide-adenine dinucleotide phosphate depen dent biliverdin reductase: partial purification and char acterization. Biochemistry 1970;9:298-303.
82. Vreman HJ, Wong RJ, Stevenson DK. Carbon monox ide in breath, blood, and other tissues. In: Penney DG, ed. Carbon Monoxide Toxicity. Boca Raton: CRC Press, 2000:19-60.
83. Cruse I, Maines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 1988;263:3348-3353.
84. Lee PJ, Jiang BH, Chin BY, et al. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 1997;272:5375-5381.
85. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 1996;14:556-568.
86. Shibahara S, Muller RM, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 1987;262:12889-12892.
87. Alam J, Shibahara S, Smith A. Transcriptional activa tion of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J Biol Chem 1989 264:6371-6375
88. Keyse SM, Applegate LA, Tromvoukis Y, Tyrrell RM. Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibro blasts. Mol Cell Biol 1990;10:4967-4969.
89. Alam J, Cai J, Smith A. Isolation and characterization of the mouse heme oxygenase-1 gene: distal 5' sequences are required for induction by heme or heavy metals. J Biol Chem 1994;269:1001-1009.
90. Alam J, Camhi S, Choi AM. Identification of a second region upstream of the mouse heme oxygenase-1 gene that functions as a basal level and inducer-dependent transcription enhancer. J Biol Chem 1995 270:11977-11984.
91. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regu lates induction of the heme oxygenase-1 gene. J Biol Chem 1999;274:26071-26078.
92. Alam J, Wicks C, Stewart D, et al. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells: role of p38 kinase and Nrf2 transcription factor. J Biol Chem 2000;275:27694-27702.
93. Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999;13:76-86.
94. Kobayashi A, Kang MI, Okawa H, et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 2004;24:7130-7139.
95. Ogawa K, Sun J, Taketani S, et al. Heme mediates de repression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J 2001;20:2835-2843.
96. Sun J, Hoshino H, Takaku K, et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 2002;21:5216-5224.
97. Alam J, Igarashi K, Immenschuh S, Shibahara S, Tyrrell RM. Regulation of heme oxygenase-1 gene transcrip tion: recent advances and highlights from the Interna tional Conference (Uppsala, 2003) on Heme Oxygenase. Antioxid Redox Signal 2004;6:924-933.
98. Alam J, Cook JL. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 2007;36:166-174.
99. Stone JR, Marletta MA. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 1994;33:5636-5640.
100. Furchgott RF, Jothianandan D. Endothelium-depen dent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon mon oxide and light. Blood Vessels 1991;28:52-61.
101. Suematsu M, Goda N, Sano T, et al. Carbon monoxide: an endogenous modulator of sinusoidal tone in the per fused rat liver. J Clin Invest 1995;96:2431-2437.
102. Wang R. Resurgence of carbon monoxide: an endog enous gaseous vasorelaxing factor. Can J Physiol Phar macol 1998;76:1-15.
103. Nakahira K, Kim HP, Geng XH, et al. Carbon monoxide differentially inhibits TLR signaling pathways by regu lating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med 2006;203:2377-2389.
104. Kim HP, Wang X, Zhang J, et al. Heat shock protein-70 mediates the cytoprotective effect of carbon monoxide: involvement of p38 beta MAPK and heat shock factor-1. J Immunol 2005;175:2622-2629.
105. Bilban M, Bach FH, Otterbein SL, et al. Carbon monox ide orchestrates a protective response through PPARga- mma. Immunity 2006;24:601-610.
106. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, Soares MP. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription fac tor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis. J Biol Chem 2002;277:17950-17961.
107. Zhang X, Shan P, Alam J, Fu XY, Lee PJ. Carbon monox ide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during an- oxia-reoxygenation injury. J Biol Chem 2005 280:8714-8721.
108. Wang X, Wang Y, Kim HP, Nakahira K, Ryter SW, Choi AM. Carbon monoxide protects against hyperoxia-in- duced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J Biol Chem 2007 282:1718-1726.
109. Wang X, Wang Y, Lee SJ, Kim HP, Choi AM, Ryter SW. Carbon monoxide inhibits Fas activating antibody- induced apoptosis in endothelial cells. Med Gas Res 2011;1:8.
110. Morita T, Perrella MA, Lee ME, Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci U S A 1995;92:1475-1479.
111. Morita T, Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest 1995;96:2676-2682.
112. Kim HP, Wang X, Nakao A, et al. Caveolin-1 expression by means of p38beta mitogen-activated protein kinase mediates the antiproliferative effect of carbon monox ide. Proc Natl Acad Sci U S A 2005;102:11319-11324.
113. Taille C, El-Benna J, Lanone S, Boczkowski J, Motter lini R. Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of car bon monoxide in human airway smooth muscle. J Biol Chem 2005;280:25350-25360.
114. Rodriguez AI, Gangopadhyay A, Kelley EE, Pagano PJ, Zuckerbraun BS, Bauer PM. HO-1 and CO decrease platelet-derived growth factor-induced vascular smooth muscle cell migration via inhibition of Nox1. Arterio- scler Thromb Vasc Biol 2010;30:98-104.
115. Morse D, Pischke SE, Zhou Z, et al. Suppression of inflammatory cytokine production by carbon monox ide involves the JNK pathway and AP-1. J Biol Chem 2003;278:36993-36998.
116. Mazzola S, Forni M, Albertini M, et al. Carbon monox ide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J 2005;19:2045-2047.
117. Mitchell LA, Channell MM, Royer CM, Ryter SW, Choi AM, McDonald JD. Evaluation of inhaled carbon mon oxide as an anti-inflammatory therapy in a nonhuman primate model of lung inflammation. Am J Physiol Lung Cell Mol Physiol 2010;299:L891-L897.
118. Ghosh S, Wilson MR, Choudhury S, et al. Effects of in haled carbon monoxide on acute lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2005;288:L1003-L1009.
119. Clayton CE, Carraway MS, Suliman HB, et al. Inhaled carbon monoxide and hyperoxic lung injury in rats. Am J Physiol Lung Cell Mol Physiol 2001;281:L949-L957.
120. Fernandez-Gonzalez A, Alex Mitsialis S, Liu X, Kourem-banas S. Vasculoprotective effects of heme oxygenase-1 in a murine model of hyperoxia-induced bronchopul monary dysplasia. Am J Physiol Lung Cell Mol Physiol 2012;302:L775-L784.
121. Hoetzel A, Schmidt R, Vallbracht S, et al. Carbon monoxide prevents ventilator-induced lung injury via caveo- lin-1. Crit Care Med 2009;37:1708-1715.
122. Hoetzel A, Dolinay T, Vallbracht S, et al. Carbon mon oxide protects against ventilator-induced lung injury via PPAR-gamma and inhibition of Egr-1. Am J Respir Crit Care Med 2008;177:1223-1232.
123. Faller S, Foeckler M, Strosing KM, et al. Kinetic effects of carbon monoxide inhalation on tissue protection in ventilator-induced lung injury. Lab Invest 2012;92:999- 1012.
124. Fujita T, Toda K, Karimova A, et al. Paradoxical rescue from ischemic lung injury by inhaled carbon mon oxide driven by derepression of fibrinolysis. Nat Med 2001;7:598-604.
125. Mishra S, Fujita T, Lama VN, et al. Carbon monox ide rescues ischemic lungs by interrupting MAPK- driven expression of early growth response 1 gene and its downstream target genes. Proc Natl Acad Sci USA 2006;103:5191-5196.
126. Schallner N, Fuchs M, Schwer CI, et al. Postcondition ing with inhaled carbon monoxide counteracts apopto- sis and neuroinflammation in the ischemic rat retina. PLoS One 2012;7:e46479.
127. Nakao A, Kimizuka K, Stolz DB, et al. Protective effect of carbon monoxide inhalation for cold-preserved small intestinal grafts. Surgery 2003;134:285-292.
128. Faleo G, Neto JS, Kohmoto J, et al. Carbon monoxide ameliorates renal cold ischemia-reperfusion injury with an upregulation of vascular endothelial growth factor by activation of hypoxia-inducible factor. Transplanta tion 2008;85:1833-1840.
129. Kaizu T, Nakao A, Tsung A, et al. Carbon monoxide in halation ameliorates cold ischemia/reperfusion injury after rat liver transplantation. Surgery 2005;138:229-235.
130. Kohmoto J, Nakao A, Kaizu T, et al. Low-dose carbon monoxide inhalation prevents ischemia/reperfu sion injury of transplanted rat lung grafts. Surgery 2006;140:179-185.
131. Kohmoto J, Nakao A, Sugimoto R, et al. Carbon monox ide-saturated preservation solution protects lung grafts from ischemia-reperfusion injury. J Thorac Cardiovasc Surg 2008;136:1067-1075.
132. Nakao A, Toyokawa H, Tsung A, et al. Ex vivo applica tion of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemia/reperfusion injury. Am J Transplant 2006;6:2243-2255.
133. Pannen BH, Kohler N, Hole B, Bauer M, Clemens MG, Geiger KK. Protective role of endogenous carbon mon oxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J Clin Invest 1998;102:1220-1228.
134. Amersi F, Shen XD, Anselmo D, et al. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfu sion injury through p38 MAP kinase pathway. Hepatol- ogy 2002;35:815-823.
135. Christou H, Morita T, Hsieh CM, et al. Prevention of hypoxia-induced pulmonary hypertension by enhance ment of endogenous heme oxygenase-1 in the rat. Circ Res 2000;86:1224-1229.
136. Minamino T, Christou H, Hsieh CM, et al. Targeted ex pression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci U S A 2001;98:8798-8803.
137. Yet SF, Perrella MA, Layne MD, et al. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest 1999;103:R23-R29.
138. Zuckerbraun BS, Chin BY, Wegiel B, et al. Carbon mon oxide reverses established pulmonary hypertension. J Exp Med 2006;203:2109-2119.
139. 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;65:751-761.
140. Selman M, King TE, Pardo A; American Thoracic Society; European Respiratory Society; American College of Chest Physicians. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its patho genesis and implications for therapy. Ann Intern Med 2001;134:136-151.
141. Zhou Z, Song R, Fattman CL, et al. Carbon monoxide suppresses bleomycin-induced lung fibrosis. Am J Pathol 2005;166:27-37.
142. Choi KM, Gibbons SJ, Nguyen TV, et al. Heme oxygen ase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenter ology 2008;135:2055-2064.
143. Kashyap PC, Choi KM, Dutta N, et al. Carbon monox ide reverses diabetic gastroparesis in NOD mice. Am J Physiol Gastrointest Liver Physiol 2010;298:G1013-G1019.
144. Rodella L, Lamon BD, Rezzani R, et al. Carbon mon oxide and biliverdin prevent endothelial cell slough ing in rats with type I diabetes. Free Radic Biol Med 2006;40:2198-2205.
145. Simon T, Pogu S, Tardif V, et al. Carbon monoxide- treated dendritic cells decrease beta1-integrin induc tion on CD8(+) T cells and protect from type 1 diabetes. Eur J Immunol 2013;43:209-218.
146. Gunther L, Berberat PO, Haga M, et al. Carbon mon oxide protects pancreatic beta-cells from apoptosis and improves islet function/survival after transplantation. Diabetes 2002;51:994-999.
147. Wang H, Lee SS, Gao W, et al. Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes 2005;54:1400-1406.
148. Joe Y, Zheng M, Kim SK, et al. The role of carbon monoxide in metabolic disease. Ann N Y Acad Sci 2011;1229:156-161.
149. Lancel S, Montaigne D, Marechal X, et al. Carbon mon oxide improves cardiac function and mitochondrial population quality in a mouse model of metabolic syn drome. PLoS One 2012;7:e41836.
150. Bainbridge SA, Sidle EH, Smith GN. Direct placental effects of cigarette smoke protect women from pre eclampsia: the specific roles of carbon monoxide and antioxidant systems in the placenta. Med Hypotheses 2005;64:17-27.
151. Ahmed A, Rahman M, Zhang X, et al. Induction of placental heme oxygenase-1 is protective against TN- Falpha-induced cytotoxicity and promotes vessel relax ation. Mol Med 2000;6:391-409.
152. Yusuf K, Kamaluddeen M, Wilson RD, Akierman A. Carboxyhemoglobin levels in umbilical cord blood of women with pre-eclampsia and intrauterine growth restriction. J Perinat Med 2012 Jun 24 [Epub]. http://dx.doi.org/10.1515/jpm-2011-0312.
153. Bainbridge SA, Belkacemi L, Dickinson M, Graham CH, Smith GN. Carbon monoxide inhibits hypoxia/re oxygenation-induced apoptosis and secondary necrosis in syncytiotrophoblast. Am J Pathol 2006;169:774-783.
154. Zhai D, Guo Y, Smith G, Krewski D, Walker M, Wen SW. Maternal exposure to moderate ambient carbon mon oxide is associated with decreased risk of preeclampsia. Am J Obstet Gynecol 2012 207:57.
155. Motterlini R, Mann BE, Foresti R. Therapeutic applica tions of carbon monoxide-releasing molecules. Expert Opin Investig Drugs 2005;14:1305-1318.
156. Foresti R, Bani-Hani MG, Motterlini R. Use of carbon monoxide as a therapeutic agent: promises and chal lenges. Intensive Care Med 2008;34:649-658.
157. Motterlini R, Sawle P, Hammad J, et al. CORM-A1: a new pharmacologically active carbon monoxide-releas ing molecule. FASEB J 2005;19:284-286.
158. Kretschmer R, Gessner G, Gorls H, Heinemann SH, Westerhausen M. Dicarbonyl-bis(cysteamine)iron(II): a light induced carbon monoxide releasing molecule based on iron (CORM-S1). J Inorg Biochem 2011;105:6-9.
159. Hasegawa U, van der Vlies AJ, Simeoni E, Wandrey C, Hubbell JA. Carbon monoxide-releasing micelles for immunotherapy. J Am Chem Soc 2010;132:18273-18280.
160. Motterlini R, Sawle P, Hammad J, et al. Vasorelaxing effects and inhibition of nitric oxide in macrophages by new iron-containing carbon monoxide-releasing mol ecules (CO-RMs). Pharmacol Res 2013;68:108-117.
161. Foresti R, Hammad J, Clark JE, et al. Vasoactive proper ties of CORM-3, a novel water-soluble carbon monoxide- releasing molecule. Br J Pharmacol 2004;142:453-460.
162. Sawle P, Foresti R, Mann BE, Johnson TR, Green CJ, Motterlini R. Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macro phages. Br J Pharmacol 2005;145:800-810.
163. Sun B, Zou X, Chen Y, Zhang P, Shi G. Preconditioning of carbon monoxide releasing molecule-derived CO at tenuates LPS-induced activation ofHUVEC. Int J Biol Sci 2008;4:270-278.
164. Sun B, Sun H, Liu C, Shen J, Chen Z, Chen X. Role of CO-releasing molecules liberated CO in attenuating leukocytes sequestration and inflammatory responses in the lung of thermally injured mice. J Surg Res 2007;139:128-135.
165. Cepinskas G, Katada K, Bihari A, Potter RF. Carbon monoxide liberated from carbon monoxide-releasing molecule CORM-2 attenuates inflammation in the liver of septic mice. Am J Physiol Gastrointest Liver Physiol 2008;294:G184-G191.
166. Mizuguchi S, Stephen J, Bihari R, et al. CORM-3- derived CO modulates polymorphonuclear leukocyte migration across the vascular endothelium by reducing levels of cell surface-bound elastase. Am J Physiol Heart Circ Physiol 2009;297:H920-H929.
167. Lancel S, Hassoun SM, Favory R, Decoster B, Motterlini R, Neviere R. Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J Pharmacol Exp Ther 2009;329:641-648.
168. Musameh MD, Green CJ, Mann BE, Fuller BJ, Motter lini R. Improved myocardial function after cold storage with preservation solution supplemented with a carbon monoxide-releasing molecule (CORM-3). J Heart Lung Transplant 2007;26:1192-1198.
169. Mayr FB, Spiel A, Leitner J, et al. Effects of carbon mon oxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 2005;171:354-360.
170. Bathoorn E, Slebos DJ, Postma DS, et al. Anti-inflam matory effects of inhaled carbon monoxide in patients with COPD: a pilot study. Eur Respir J 2007;30:1131-1137.