Heme oxygenase-1/carbon monoxide: From metabolism to molecular therapy

American Journal of Respiratory Cell and Molecular Biology

Volumn 41, Issue 3, 2009, Pages 251-260

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

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Bilirubin; Carbon monoxide; Heme oxygenase 1; Lung injury

Indexed keywords

ADENOVIRUS VECTOR; BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; HEME; HEME OXYGENASE 1; LENTIVIRUS VECTOR; RETROVIRUS VECTOR;

ACUTE LUNG INJURY; AEROBIC METABOLISM; ANTIINFLAMMATORY ACTIVITY; BLOOD VESSEL INJURY; CARBON MONOXIDE BLOOD LEVEL; CELL PROTECTION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL TRIAL; CONCENTRATION RESPONSE; DRUG MECHANISM; ENDOTOXEMIA; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME REGULATION; ESSENTIAL HYPERTENSION; GENE CONTROL; HOMEOSTASIS; HUMAN; LIVER INJURY; LOW DRUG DOSE; NONHUMAN; ORGAN TRANSPLANTATION; OXIDATIVE STRESS; PATHOGENESIS; PATHOGENICITY; PNEUMONIA; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PULMONARY HYPERTENSION; REVIEW; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; BILIRUBIN; BILIVERDINE; CARBON MONOXIDE; CLINICAL TRIALS AS TOPIC; CYTOPROTECTION; GENE THERAPY; HEME; HEME OXYGENASE-1; HOMEOSTASIS; HUMANS; IRON; MOLECULAR STRUCTURE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 69449098185     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0170TR     Document Type: Review

References (125)

1. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase: characterization of the enzyme. J Biol Chem 1969;244:6388-6394.
2. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 1968;61:748-755.
3. Mumby S, Upton RL, Chen Y, Stanford SJ, Quinlan GJ, Nicholson AG, Gutteridge JM, Lamb NJ, Evans TW. Lung heme oxygenase-1 is elevated in acute respiratory distress syndrome. Crit Care Med 2004;32:1130-1135. (Pubitemid 38620980)
4. Hoetzel A, Dolinay T, Vallbracht S, Zhang Y, Kim HP, Ifedigbo E, Alber S, Kaynar AM, Schmidt R, Ryter SW, et al. Carbon monoxide protects against ventilator-induced lung injury via PPAR-gamma and inhibition of Egr-1. Am J Respir Crit Care Med 2008;177:1223-1232. (Pubitemid 351860931)
5. Hoetzel A, Leitz D, Schmidt R, Tritschler E, Bauer I, Loop T, Humar M, Geiger KK, Pannen BH. Mechanism of hepatic heme oxygenase-1 induction by isoflurane. Anesthesiology 2006;104:101-109.
6. 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. (Pubitemid 126442947)
7. Minamino T, Christou H, Hsieh CM, Liu Y, Dhawan V, Abraham NG, Perrella MA, Mitsialis SA, Kourembanas S. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci USA 2001;98:8798-8803. (Pubitemid 32678107)
8. Liu X, Pachori AS, Ward CA, Davis JP, Gnecchi M, Kong D, Zhang L, Murduck J, Yet SF, Perrella MA, et al. Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function. FASEB J 2006;20:207-216. (Pubitemid 44933167)
9. Vulapalli SR, Chen Z, Chua BH, Wang T, Liang CS. Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis. Am J Physiol Heart Circ Physiol 2002;283:H688-H694. (Pubitemid 34790864)
10. Thompson D, Basu-Modak S, Gordon M, Poore S, Markovitch D, Tyrrell RM. Exercise-induced expression of heme oxygenase-1 in human lymphocytes. Free Radic Res 2005;39:63-69. (Pubitemid 40326160)
11. Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, Grey ST, Colvin RB, Choi AM, Poss KD, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998;4:1073-1077. (Pubitemid 28417343)
12. Sato K, Balla J, Otterbein L, Smith RN, Brouard S, Lin Y, Csizmadia E, Sevigny J, Robson SC, Vercellotti G, et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-torat cardiac transplants. J Immunol 2001;166:4185-4194. (Pubitemid 32224952)
13. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Gracxa-Souza AV, Ollinger R, Czismadia E, May GA, Ifedigbo E, Otterbein LE, et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 2004;18:771-772.
14. 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 arsenite. Proc Natl Acad Sci USA 1989;86:99-103.
15. Applegate LA, Luscher P, Tyrrell RM. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 1991;51:974-978.
16. Maines MD, Kappas A. Cobalt induction of hepatic heme oxygenase; with evidence that cytochrome P-450 is not essential for this enzyme activity. Proc Natl Acad Sci USA 1974;71:4293-4297.
17. Welch WJ, Feramisco JR. Purification of the major mammalian heat shock proteins. J Biol Chem 1982;257:14949-14959.
18. Li GC, Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci USA 1982;79:3218-3222.
19. 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.
20. 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. (Pubitemid 18224435)
21. Shibahara S, Sato M, Muller RM, Yoshida T. Structural organization of the human heme oxygenase gene and the function of its promoter. Eur J Biochem 1989;179:557-563. (Pubitemid 19062330)
22. Shibahara S, Müller RM, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 1987;262:12889-12892.
23. Yoshida T, Biro P, Cohen T, Müller RM, Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur J Biochem 1988;171:457-461. (Pubitemid 18060902)
24. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
25. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000;6:422-428.
26. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 2003;9:183-190. (Pubitemid 36227720)
27. Fondevila C, Shen XD, Tsuchiyashi S, Yamashita K, Csizmadia E, Lassman C, Busuttil RW, Kupiec-Weglinski JW, Bach FH. Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 2004;40:1333-1341. (Pubitemid 39657007)
28. Adin CA, Croker BP, Agarwal A. Protective effects of exogenous bilirubin on ischemia-reperfusion injury in the isolated, perfused rat kidney. Am J Physiol Renal Physiol 2005;288:F778-F784. (Pubitemid 40381746)
29. Yamashita K, McDaid J, Ollinger R, Tsui TY, Berberat PO, Usheva A, Csizmadia E, Smith RN, Soares MP, Bach FH. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J 2004;18:765-767.
30. 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.
31. Trakshel GM, Kutty RK, Maines MD. Purification and characterization of the major constitutive form of testicular heme oxygenase. J Biol Chem 1986;261:11131-11137.
32. Cruse I, Maines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 1998;263:3348-3353.
33. Rotenberg MO, Maines MD. Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J Biol Chem 1990;265:7501-7506. (Pubitemid 20162495)
34. Rotenberg MO, Maines MD. 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 1991;290:336-344.
35. Ishikawa K, Sato M, Yoshida T. Expression of rat heme oxygenase in Esherichia coli as a catalytically active, full length form that binds to bacterial membranes. Eur J Biochem 1991;202:161-165.
36. Kim HP, Wang X, Galbiati F, Ryter SW. Choi AMK. Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J 2004;18:1080-1089. (Pubitemid 38859216)
37. Slebos DJ, Ryter SW, van der Toorn M, Liu F, Guo F, Baty CJ, Karlsson JM, Watkins SC, Kim HP, Wang X, et al. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am J Respir Cell Mol Biol 2007;36:409-417.
38. Lin Q, Weis S, Yang G, Weng YH, Helston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F, et al. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 2007;282:20621-20633. (Pubitemid 47100046)
39. Pickett CB, Nguyen T, Nioi P. The Nrf2-ARE signaling pathway and its activation by oxidative stress. J Biol Chem 2009;284:13291-13295.
40. Alam J, Cai J, Smith A. Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 59 sequences are required for induction by heme or heavy metals. J Biol Chem 1994;269:1001-1009. (Pubitemid 24981976)
41. 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.
42. Alam J, Den Z. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J Biol Chem 1992;267:21894-21900.
43. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999;274:26071-26078. (Pubitemid 129520030)
44. Itoh K, Wakabayashi N, Katoh Y, Ishii T, O'Connor T, Yamamoto M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 2003;8:379-391. (Pubitemid 36504013)
45. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999;13:76-86. (Pubitemid 29045117)
46. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M. 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. (Pubitemid 39014439)
47. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 2002;99:11908-11913. (Pubitemid 34994497)
48. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 2002;21:5216-5224.
49. Sun J, Brand M, Zenke Y, Tashiro S, Groudine M, Igarashi K. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc Natl Acad Sci USA 2004;101:1461-1466. (Pubitemid 38234177)
50. Takeda K, Ishizawa S, Sato M, Yoshida T, Shibahara S. Identification of a cis-acting element that is responsible for cadmium-mediated induction of the human heme oxygenase gene. J Biol Chem 1994;269:22858-22867. (Pubitemid 24273402)
51. Yang G, Nguyen X, Ou J, Rekulapelli P, Stevenson DK, Dennery PA. Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 2001;97:1306-1313. (Pubitemid 32183753)
52. Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A. The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol 2004;286:F425-F441. (Pubitemid 38233635)
53. Choi AM, Alam J. Heme oxygenase-1: Function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 1996;15:9-19. (Pubitemid 126439851)
54. 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.
55. Exner M, Minar E, Wagner O, Schillinger M. The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med 2004;37:1097-1104. (Pubitemid 39296737)
56. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet 2000;66:187-195. (Pubitemid 30481482)
57. Exner M, Schillinger M, Minar E, Mlekusch W, Schlerka G, Haumer M, Mannhalter C, Wagner O. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty. J Endovasc Ther 2001;8:433-440. (Pubitemid 33032454)
58. Chen YH, Chau LY, Lin MW, Chen LC, Yo MH, Chen JW, Lin S. Heme oxygenase-1 gene promotor microsatellite polymorphism is associated with angiographic restenosis after coronary stenting. Eur Heart J 2004;25:39-47. (Pubitemid 38055591)
59. Schillinger M, Exner M, Minar E, Mlekusch W, Müllner M, Mannhalter C, Bach FH, Wagner O. Heme oxygenase-1 genotype and restenosis after balloon angioplasty: a novel vascular protective factor. J Am Coll Cardiol 2004;43:950-957. (Pubitemid 38352971)
60. Rueda B, Oliver J, Robledo G, López-Nevot MA, Balsa A, Pascual-Salcedo D, González-Gay MA, González-Escribano MF, Martín J. HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis Rheum 2007;56:3953-3958. (Pubitemid 350262322)
61. Exner M, Böhmig GA, Schillinger M, Regele H, Watschinger B, Hörl WH, Raith M, Mannhalter C, Wagner OF. Donor heme oxygenase-1 genotype is associated with renal allograft function. Transplantation 2004;77:538-542. (Pubitemid 38282808)
62. Ullrich R, Exner M, Schillinger M, Zuckermann A, Raith M, Dunkler D, Horvat R, Grimm M, Wagner O. Microsatellite polymorphism in the heme oxygenase-1 gene promoter and cardiac allograft vasculopathy. J Heart Lung Transplant 2005;24:1600-1605. (Pubitemid 41396459)
63. Courtney AE, McNamee PT, Middleton D, Heggarty S, Patterson CC, Maxwell AP. Association of functional heme oxygenase-1 gene promoter polymorphism with renal transplantation outcomes. Am J Transplant 2007;7:908-913. (Pubitemid 46481204)
64. 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. J Clin Invest 1999;103:129-135. (Pubitemid 29031171)
65. Poss KD, Tonegawa S. Heme oxygenase-1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA 1997;94:10919-10924. (Pubitemid 27430836)
66. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase-1 deficient cells. Proc Natl Acad Sci USA 1997;94:10925-10930. (Pubitemid 27430837)
67. Duckers HJ, Boehm M, True AL, Yet SF, San H, Park JL, Webb RC, Lee ME, Nabel GJ, Nabel EG. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med 2001;7:693-698. (Pubitemid 32588025)
68. Fujita T, Toda K, Karimova A, Yan SF, Naka Y, Yet SF, Pinsky DJ. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat Med 2001;7:598-604. (Pubitemid 32448328)
69. Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest 1999;103:R23-R29. (Pubitemid 29207256)
70. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, Ith B, Melo LG, Zhang L, Ingwall JS, et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res 2001;89:168-173. (Pubitemid 34135825)
71. Zampetaki A, Minamino T, Mitsialis SA, Kourembanas S. Effect of heme oxygenase-1 overexpression in two models of lung inflammation. Exp Biol Med (Maywood) 2003;228:442-446. (Pubitemid 37203657)
72. Grochot-Przeczek A, Lach R, Mis J, Skrzypek K, Gozdecka M, Sroczynska P, Dubiel M, Rutkowski A, Kozakowska M, Zagorska A, et al. Heme oxygenase-1 accelerates cutaneous wound healing in mice. PLoS One 2009;4:e5803.
73. Abraham NG, Asija A, Drummond G, Peterson S. Heme oxygenase-1 gene therapy: recent advances and therapeutic applications. Curr Gene Ther 2007;7:89-108. (Pubitemid 46681767)
74. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen ME, Shibahara S, Kappas A. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci USA 1995;92:6798-6802.
75. Abraham NG, da Silva JL, Lavrovsky Y, Stoltz RA, Kappas A, Dunn MW, Schwartzman ML. Adenovirus-mediated heme oxygenase-1 gene transfer into rabbit ocular tissues. Invest Ophthalmol Vis Sci 1995;36:2202-2210.
76. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxic lung injury. J Clin Invest 1999;103:1047-1054. (Pubitemid 29169613)
77. Lee PJ, Alam J, Wiegand GW, Choi AM. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA 1996;93:10393-10398. (Pubitemid 26314633)
78. Sabaawy HE, Zhang F, Nguyen X, ElHosseiny A, Nasjletti A, Schwartzman M, Dennery P, Kappas A, Abraham NG. Human heme oxygenase-1 gene transfer lowers blood pressure and promotes growth in spontaneously hypertensive rats. Hypertension 2001;38:210-215. (Pubitemid 34224746)
79. Hurttila H, Koponen JK, Kansanen E, Jyrkkänen HK, Kivelä A, Kylätie R, Ylä-Herttuala S, Levonen AL. Oxidative stress-inducible lentiviral vectors for gene therapy. Gene Ther 2008;15:1271-1279.
80. Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity: heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 2000;28:289-309.
81. Ryter SW, Morse D, Choi AM. Carbon monoxide and bilirubin: potential therapies for pulmonary/vascular injury and disease. Am J Respir Cell Mol Biol 2007;36:175-182. (Pubitemid 46233470)
82. Stocker R, Yamamoto Y, McDonagh A, Glazer A, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987;235:1043-1045. (Pubitemid 17049750)
83. Foresti R, Green CJ, Motterlini R. Generation of bile pigments by haem oxygenase: a refined cellular strategy in response to stressful insults. Biochem Soc Symp 2004;71:177-192. (Pubitemid 41185485)
84. Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 1999;13:1800-1809.
85. Kvam E, Hejmadi V, Ryter S, Pourzand C, Tyrrell RM. Heme oxygenase activity causes transient hypersensitivity to oxidative ultraviolet A radiation that depends on release of iron from heme. Free Radic Biol Med 2000;28:1191-1196. (Pubitemid 30417461)
86. Vile GF, Tyrrell RM. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J Biol Chem 1993;268:14678-14681. (Pubitemid 23206605)
87. Vile GF, Basu-Modak S, Waltner C, Tyrrell RM. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci USA 1994;91:2607-2610. (Pubitemid 24139396)
88. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science 1993;259:381-384. (Pubitemid 23055683)
89. Suematsu M, Kashiwagi S, Sano T, Goda N, Shinoda Y, Ishimura Y. Carbon monoxide as an endogenous modulator of hepatic vascular perfusion. Biochem Biophys Res Commun 1994;205:1333-1337.
90. Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM, Soares MP. Carbon monoxide generated by heme oxygenase-1 suppresses endothelial cell apoptosis. J Exp Med 2000;192:1015-1026. (Pubitemid 30765694)
91. Morse D, Lin L, Choi AM, Ryter SW. Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease. Free Radic Biol Med 2009;47:1-12.
92. 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. (Pubitemid 28023614)
93. Von Burg R. Toxicology update: carbon monoxide. J Appl Toxicol 1999;19:379-386.
94. 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. (Pubitemid 39202202)
95. Kim HP, Ryter SW, Choi AM. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 2006;46:411-449.
96. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997;37:517-554.
97. Ryter SW, Morse D, Choi AMK. Carbon monoxide: to boldly go where NO has gone before. Sci STKE 2004;230:re6.
98. Morita T, Perrella MA, Lee ME, Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA 1995;92:1475-1479.
99. Otterbein LE, Otterbein SL, Ifedigbo E, Liu F, Morse DE, Fearns C, Ulevitch RJ, Knicklebein R, Flavell RA, Choi AM. MKK3 mitogen activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant induced lung injury. Am J Pathol 2003;163:2555-2563. (Pubitemid 37466496)
100. Nakahira K, Kim HP, Geng XH, Nakao A, Wang X, Murase N, Drain PF, Wang X, Sasidhar M, Nabel EG, et al. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med 2006;203:2377-2389. (Pubitemid 44498371)
101. TailléC, El-Benna J, Lanone S, Boczkowski J, Motterlini R. Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J Biol Chem 2005;280:25350-25360. (Pubitemid 40962237)
102. Kim HP, Wang Y, Suh GY, Zhang J, Ryter SW, Choi AMK. Heat shock factor-1 mediates the cytoprotective effect of carbon monoxide. J Immunol 2005;175:2622-2629.
103. Bilban M, Bach FH, Otterbein SL, Ifedigbo E, d'Avila JC, Esterbauer H, Chin BY, Usheva A, Robson SC, Wagner O, et al. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 2006;24:601-610.
104. Kim HP, Wang X, Nakao A, Kim SI, Murase N, Choi ME, Ryter SW, Choi AM. Caveolin-1 expression by means of p38beta mitogenactivated protein kinase mediates the antiproliferative effect of carbon monoxide. Proc Natl Acad Sci USA 2005;102:11319-11324. (Pubitemid 41153818)
105. Wang XM, Kim HP, Nakahira K, Ryter SW, Choi AM. The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1. J Immunol 2009;182:3809-3818.
106. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999;276:L688-L694. (Pubitemid 29211371)
107. Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, Davis RJ, Choi AM, Lee PJ. 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. (Pubitemid 36790808)
108. Hoetzel A, Schmidt R, Vallbracht S, Goebel U, Dolinay T, Kim HP, Ifedigbo E, Ryter SW, Choi AM. Carbon monoxide prevents ventilator-induced lung injury via caveolin-1. Crit Care Med 2009;37:1708-1715.
109. Zuckerbraun BS, Chin BY, Wegiel B, Billiar TR, Czsimadia E, Rao J, Shimoda L, Ifedigbo E, Kanno S, Otterbein LE. Carbon monoxide reverses established pulmonary hypertension. J Exp Med 2006;203:2109-2119. (Pubitemid 44352232)
110. Nakao A, Kimizuka K, Stolz DB, Seda Neto J, Kaizu T, Choi AM, Uchiyama T, Zuckerbraun BS, Bauer AJ, Nalesnik MA, et al. Protective effect of carbon monoxide inhalation for cold-preserved small intestinal grafts. Surgery 2003;134:285-292. (Pubitemid 37070351)
111. Song R, Kubo M, Morse D, Zhou Z, Zhang X, Dauber JH, Fabisiak J, Alber SM, Watkins SC, Zuckerbraun BS, et al. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am J Pathol 2003;163:231-242. (Pubitemid 36759607)
112. Nakao A, Toyokawa H, Tsung A, Nalesnik MA, Stolz DB, Kohmoto J, Ikeda A, Tomiyama K, Harada T, Takahashi T, et al. Ex vivo application of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemia/reperfusion injury. Am J Transplant 2006;6:2243-2255. (Pubitemid 44359410)
113. Nakao A, Neto JS, Kanno S, Stolz DB, Kimizuka K, Liu F, Bach FH, Billiar TR, Choi AM, Otterbein LE, et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2000;5:282-291. (Pubitemid 40179514)
114. Kohmoto J, Nakao A, Kaizu T, Tsung A, Ikeda A, Tomiyama K, Billiar TR, Choi AM, Murase N, McCurry KR. Low-dose carbon monoxide inhalation prevents ischemia/reperfusion injury of transplanted rat lung grafts. Surgery 2006;140:179-185. (Pubitemid 44202625)
115. Ollinger R, Bilban M, Erat A, Froio A, McDaid J, Tyagi S, Csizmadia E, Graca-Souza AV, Liloia A, Soares MP, et al. Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 2005;112:1030-1039. (Pubitemid 41170272)
116. Mayr FB, Spiel A, Leitner J, Marsik C, Germann P, Ullrich R, Wagner O, Jilma B. Effects of carbon monoxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 2005;171:354-360. (Pubitemid 40223403)
117. Bathoorn E, Slebos DJ, Postma DS, Koeter GH, van Oosterhout AJ, van der Toorn M, Boezen HM, Kerstjens HA. Anti-inflammatory effects of inhaled carbon monoxide in patients with COPD: a pilot study. Eur Respir J 2007;30:1131-1137. (Pubitemid 351194760)
118. Kinobe RT, Dercho RA, Nakatsu K. Inhibitors of the heme oxygenase - carbon monoxide system: on the doorstep of the clinic? Can J Physiol Pharmacol 2008;86:577-599.
119. Motterlini R, Mann BE, Foresti R. Therapeutic applications of carbon monoxide-releasing molecules. Expert Opin Investig Drugs 2005;14:1305-1318. (Pubitemid 41601449)
120. Zuckerbraun BS, Billiar TR, Otterbein SL, Kim PK, Liu F, Choi AM, Bach FH, Otterbein LE. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med 2003;198:1707-1716. (Pubitemid 37494163)
121. Kaizu T, Nakao A, Tsung A, Toyokawa H, Sahai R, Geller DA, Murase N. Carbon monoxide inhalation ameliorates cold ischemia/ reperfusion injury after rat liver transplantation. Surgery 2005;138:229-235. (Pubitemid 41253805)
122. Mazzola S, Forni M, Albertini M, Bacci ML, Zannoni A, Gentilini F, Lavitrano M, Bach FH, Otterbein LE, Clement MG. Carbon monoxide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J 2005;19:2045-2047. (Pubitemid 41759760)
123. 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.
124. Musameh MD, Green CJ, Mann BE, Fuller BJ, Motterlini 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. (Pubitemid 350090021)
125. Zhou Z, Song R, Fattman CL, Greenhill S, Alber S, Oury TD, Choi AM, Morse D. Carbon monoxide suppresses bleomycin-induced lung fibrosis. Am J Pathol 2005;166:27-37. (Pubitemid 40051657)