Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease

Free Radical Biology and Medicine

Volumn 47, Issue 1, 2009, Pages 1-12

  Morse, Danielle ^a   Lin, Ling ^b   Choi, Augustine M K ^a   Ryter, Stefan W ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Carbon monoxide; Free radicals; Heme oxygenase 1

Indexed keywords

BILIRUBIN; BILIVERDIN; GAMMA INTERFERON; HEAT SHOCK TRANSCRIPTION FACTOR 1; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; IRON; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; AUTOPHAGY; CELL DEATH; CELL PROTECTION; CELLULAR DISTRIBUTION; CYTOTOXICITY; DNA BINDING; DNA REPLICATION; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL STRESS; HUMAN; LUNG INJURY; LUNG TRANSPLANTATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REOXYGENATION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; APOPTOSIS; BILIVERDINE; CARBON MONOXIDE; CELL PROLIFERATION; HEME; HEME OXYGENASE-1; HUMANS; IRON; LUNG; ORGAN TRANSPLANTATION; OXIDATIVE STRESS; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 67349252035     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.04.007     Document Type: Review

References (200)

1. Ryter S.W., Alam J., and Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86 (2006) 583-650
2. Morse D., and Choi A.M. Heme oxygenase-1: the "emerging molecule" has arrived. Am. J. Respir. Cell Mol. Biol. 27 (2002) 8-16
3. Ryter S., Otterbein L.E., Morse D., and Choi A.M. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234-235 (2002) 249-263
4. Tenhunen R., Marver H.S., and Schmid R. Microsomal heme oxygenase: characterization of the enzyme. J. Biol. Chem. 244 (1969) 6388-6394
5. Poss K.D., and Tonegawa S. Heme oxygenase-1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. USA 94 (1997) 10919-10924
6. Poss K.D., and Tonegawa S. Reduced stress defense in heme oxygenase-1 deficient cells. Proc. Natl. Acad. Sci. USA 94 (1997) 10925-10930
7. Fujita T., Toda K., Karimova A., Yan S.F., Naka Y., Yet S.F., and Pinsky D.J. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 7 (2001) 598-604
8. Dennery P.A., Visner G., Weng Y.H., Nguyen X., Lu F., Zander D., and Yang G. Resistance to hyperoxia with heme oxygenase-1 disruption: role of iron. Free Radic. Biol. Med. 34 (2003) 124-133
9. Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., and Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103 (1999) 129-135
10. Ryter S.W., Kim H.P., Nakahira K., Zuckerbraun B.S., Morse D., and Choi A.M. Protective functions of heme oxygenase-1 and carbon monoxide in the respiratory system. Antioxid. Redox Signal. 9 (2007) 2157-2173
11. Ryter S., Morse D., and Choi A.M. Carbon monoxide and bilirubin: potential therapies for pulmonary/vascular injury and disease. Am. J. Respir. Cell Mol. Biol. 36 (2007) 175-182
12. Lin Q.S., Weis S., Yang G., Zhuang T., Abate A., and Dennery P.A. Catalytic inactive heme oxygenase-1 protein regulates its own expression in oxidative stress. Free Radic. Biol. Med. 44 (2008) 847-855
13. Kirkham P., and Rahman I. Oxidative stress in asthma and COPD: antioxidants as a therapeutic strategy. Pharmacol. Ther. 111 (2006) 476-494
14. Mercer B.A., and D'Armiento J.M. Emerging role of MAP kinase pathways as therapeutic targets in COPD. Int. J. Chronic Obstruct. Pulm. Dis. 1 (2006) 137-150
15. Otterbein L.E., Soares M.P., Yamashita K., and Bach F.H. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24 (2003) 449-455
16. Jozkowicz A., Was H., and Dulak J. Heme oxygenase-1 in tumors: is it a false friend?. Antioxid. Redox Signal. 9 (2007) 2099-2117
17. Galluzzi L., Maiuri M.C., Vitale I., Zischka H., Castedo M., Zitvogel L., and Kroemer G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 14 (2007) 1237-1243
18. Johnstone R.W., Ruefli A.A., and Lowe S.W. Apoptosis: a link between cancer genetics and chemotherapy. Cell 108 (2002) 153-164
19. Rashedi I., Panigrahi S., Ezzati P., Ghavami S., and Los M. Autoimmunity and apoptosis-therapeutic implications. Curr. Med. Chem. 14 (2007) 3139-3151
20. Park J.W., Ryter S.W., and Choi A.M. Functional significance of apoptosis in chronic obstructive pulmonary disease. COPD 4 (2007) 347-353
21. Ryter S.W., Kim H.P., Hoetzel A., Park J.W., Nakahira K., Wang X., and Choi A.M. Mechanisms of cell death in oxidative stress. Antioxid. Redox Signal. 9 (2007) 49-89
22. Thannickal V.J., and Horowitz J.C. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc. Am. Thorac. Soc. 3 (2006) 350-356
23. Soares M.P., and Bach F.H. Heme oxygenase-1 in organ transplantation. Front. Biosci. 12 (2007) 4932-4945
24. Majno G., and Joris I. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146 (1995) 3-15
25. Kroemer G., Dallaporta B., and Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60 (1998) 619-642
26. Youle R.J., and Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev., Mol. Cell Biol. 9 (2008) 47-59
27. Huang D.C., and Strasser A. BH3-only proteins-essential initiators of apoptotic cell death. Cell 103 (2000) 839-842
28. Nagata S. Fas ligand-induced apoptosis. Annu. Rev. Genet. 33 (1999) 29-55
29. Wang K., Grossm A., Waksman G., and Korsmeyer S.J. Mutagenesis of the BH3 domain of BAX identifies residues critical for dimerization and killing. Mol. Cell Biol. 18 (1998) 6083-6089
30. Antonsson B., Montessuit S., Lauper S., Eskes R., and Martinou J.C. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J. 345 (2000) 271-278
31. Riedl S.J., and Salvesen G.S. The apoptosome: signaling platform of cell death. Nat. Rev., Mol. Cell Biol. 8 (2007) 405-413
32. Saelens X., Festjens N., Vande W.L., van Gurp M., van Loo G., and Vandenabeele P. Toxic proteins released from mitochondria in cell death. Oncogene 23 (2004) 2861-2874
33. Walsh C.M., Luhrs K.A., and Arechiga A.F. The "fuzzy logic" of the death-inducing signaling complex in lymphocytes. J. Clin. Immunol. 23 (2003) 333-353
34. Kelekar A. Autophagy. Ann. N.Y. Acad. Sci. 1066 (2006) 259-271
35. Kondo Y., Kanzawa T., Sawaya R., and Kondo S. The role of autophagy in cancer development and response to therapy. Nat. Rev., Cancer 5 (2005) 726-734
36. Mizushima N., Levine B., Cuervo A.M., and Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 451 (2008) 1069-1075
37. Kiffin R., Bandyopadhyay U., and Cuervo A.M. Oxidative stress and autophagy. Antioxid. Redox Signal. 8 (2006) 152-162
38. Cuervo A.M. Autophagy: in sickness and in health. Trends Cell Biol. 14 (2004) 70-77
39. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., and Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402 (1999) 672-676
40. He H., Dang Y., Dai F., Guo Z., Wu J., She X., Pei Y., Chen Y., Ling W., Wu C., Zhao S., Liu J.O., and Yu L. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J. Biol. Chem. 278 (2003) 29278-29287
41. Galluzzi L., Vicencio J.M., Kepp O., Tasdemir E., Maiuri M.C., and Kroemer G. To die or not to die: that is the autophagic question. Curr. Mol. Med. 8 (2008) 78-91
42. Maiuri M.C., Zalckvar E., Kimchi A., and Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev., Mol. Cell Biol. 8 (2007) 741-752
43. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., and Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6 (2004) 1221-1228
44. Crighton D., Wilkinson S., O'Prey J., Syed N., Smith P., Harrison P.R., Gasco M., Garrone O., Crook Y., and Ryan K.M. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126 (2006) 121-134
45. Kroemer G., and Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev., Mol. Cell Biol. 9 (2008) 1004-1010
46. Keyse S.M., and Tyrrell R.M. 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 86 (1989) 99-103
47. Trakshel G.M., Kutty R.K., and Maines M.D. Purification and characterization of the major constitutive form of testicular heme oxygenase. J. Biol. Chem. 261 (1986) 11131-11137
48. Cruse I., and Maines M.D. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J. Biol. Chem. 263 (1988) 3348-3353
49. Rotenberg M.O., and Maines M.D. Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J. Biol. Chem. 265 (1990) 7501-7506
50. Rotenberg M.O., and Maines M.D. Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: possible heme-binding site?. Arch. Biochem. Biophys. 290 (1991) 336-344
51. Ishikawa K., Sato M., and Yoshida T. Expression of rat heme oxygenase in Escherichia coli as a catalytically active, full length form that binds to bacterial membranes. Eur. J. Biochem. 202 (1991) 161-165
52. Shibahara S., Muller R.M., Taguchi H., and Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc. Natl. Acad. Sci. USA 82 (1985) 7865-7869
53. McCoubrey W.K., and Maines M.D. Domains of rat heme oxygenase-2: the amino terminus and histidine 151 are required for heme oxidation. Arch. Biochem. Biophys. 302 (1993) 402-408
54. McCoubrey W.K., Huang T.J., and Maines M.D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 247 (1997) 725-732
55. Hayashi S., Omata Y., Sakamoto H., Higashimoto Y., Hara T., Sagara Y., and Noguchi M. Characterization of rat heme oxygenase-3 gene: implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 336 (2004) 241-250
56. Lin Q., Weis S., Yang G., Weng Y.H., Helston R., Rish K., Smith A., Bordner J., Polte T., Gaunitz F., and Dennery P.A. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J. Biol. Chem. 282 (2007) 20621-20633
57. Sacca P., Meiss R., Casas G., Mazza O., Calvo J.C., Navone N., and Vazquez E. Nuclear translocation of haeme oxygenase-1 is associated to prostate cancer. Br. J. Cancer 97 (2007) 1683-1689
58. Kim H.P., Wang X., Galbiati F., Ryter S.W., and Choi A.M.K. Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J. 18 (2004) 1080-1089
59. Feron O., Belhassen L., Kobzik L., Smith T.W., Kelly R.A., and Michel T. Endothelial nitric oxide synthase targeting to caveolae: specific interactions with caveolin-1 isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 271 (1996) 22810-22814
60. Slebos D.J., Ryter S.W., van der Toorn M., Liu F., Guo F., Baty C.J., Karlsson J.M., Watkins S.C., Kim H.P., Wang X., Lee J.S., Postma D.S., Kauffman H.F., and Choi A.M. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am. J. Respir. Cell Mol. Biol. 36 (2007) 409-417
61. Converso D.P., Taille C., Carreras M.C., Jaitovich A., Poderoso J.J., and Boczkowski J. HO-1 is located in liver mitochondria and modulates mitochondrial heme content and metabolism. FASEB J. 20 (2006) 1236-1238
62. Scapagnini G., Foresti R., Calabrese V., Giuffrida Stella A.M., Green C.J., and Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 61 (2002) 554-556
63. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., De Galarreta C.M., and Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 279 (2004) 8919-8929
64. Foresti R., Hoque M., Monti D., Green C.J., and Motterlini R. Differential activation of heme oxygenase-1 by chalcones and rosolic acid in endothelial cells. J. Pharmacol. Exp. Ther. 312 (2005) 686-693
65. Saunders E.L., Maines M.D., Meredith M.J., and Freeman M.L. Enhancement of heme oxygenase-1 synthesis by glutathione depletion in Chinese hamster ovary cells. Arch. Biochem. Biophys. 288 (1991) 368-373
66. Lautier D., Luscher P., and Tyrrell R.M. Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis 13 (1992) 227-232
67. Rizzardini M., Carelli M., Cabello Porras M.R., and Cantoni L. Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochem. J. 304 (1994) 477-483
68. Shibahara S., Han F., Li B., and Takeda K. Hypoxia and heme oxygenases: oxygen sensing and regulation of expression. Antioxid. Redox Signal. 9 (2007) 2209-2225
69. Alam J., and Cook J.L. How many transcription factors does it take to turn on the heme oxygenase-1 gene?. Am. J. Respir. Cell Mol. Biol. 36 (2007) 166-174
70. Alam J., Cai J., and 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. 269 (1994) 1001-1009
71. Alam J., Camhi S., and Choi A.M. 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. 270 (1995) 11977-11984
72. Inamdar N.M., Ahn Y.I., and Alam J. The heme-responsive element of the mouse heme oxygenase-1 gene is an extended AP-1 binding site that resembles the recognition sequences for MAF and NF-E2 transcription factors. Biochem. Biophys. Res. Commun. 221 (1996) 570-576
73. Igarashi K., and Sun J. The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid. Redox Signal. 8 (2006) 107-118
74. Sun J., Hoshino H., Takaku K., Nakajima O., Muto A., Suzuki H., Tashiro S., Takahashi S., Shibahara S., Alam J., Taketo M.M., Yamamoto M., and Igarashi K. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 21 (2002) 5216-5224
75. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., and Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274 (1999) 26071-26078
76. Oyake T., Itoh K., Motohashi H., Hayashi N., Hoshino H., Nishizawa M., Yamamoto M., and Igarashi K. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 16 (1996) 6083-6095
77. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., Bannai S., and Yamamoto M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275 (2000) 16023-16029
78. Ishii T., Itoh K., Ruiz E., Leake D.S., Unoki H., Yamamoto M., and Mann G.E. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ. Res. 94 (2004) 609-616
79. Sun J., Brand M., Zenke Y., Tashiro S., Groudine M., and 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 101 (2004) 1461-1466
80. Suzuki H., Tashiro S., Sun J., Doi H., Satomi S., and Igarashi K. Cadmium induces nuclear export of Bach1, a transcriptional repressor of heme oxygenase-1 gene. J. Biol. Chem. 278 (2003) 49246-49253
81. Stewart D., Killeen E., Naquin R., Alam S., and Alam J. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 278 (2003) 2396-2402
82. Alam J., Killeen E., Gong P., Naquin R., Hu B., Stewart D., Ingelfinger J.R., and Nath K.A. Heme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2. Am. J. Physiol., Renal Physiol. 284 (2003) F743-F752
83. Itoh K., Wakabayashi N., Katoh Y., Ishii T., O'Connor T., and Yamamoto M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8 (2003) 379-391
84. Kobayashi M., Itoh K., Suzuki T., Osanai H., Nishikawa K., Katoh Y., Takagi Y., and Yamamoto M. Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7 (2002) 807-820
85. Cho H.Y., Reddy S.P., and Kleeberger S.R. Nrf2 defends the lung from oxidative stress. Antioxid. Redox Signal. 8 (2006) 76-87
86. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., and Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13 (1999) 76-86
87. Kang M.I., Kobayashi A., Wakabayashi N., Kim S.G., and Yamamoto M. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc. Natl. Acad. Sci. USA 101 (2004) 2046-2051
88. Zipper L.M., and Mulcahy R.T. The Keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J. Biol. Chem. 277 (2002) 36544-36552
89. Jeong W.S., Jun M., and Kong A.N. Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid. Redox Signal. 8 (2006) 99-106
90. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., and 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 99 (2002) 11908-11913
91. Wakabayashi N., Itoh K., Wakabayashi J., Motohashi H., Noda S., Takahashi S., Imakado S., Kotsuji T., Otsuka F., Roop D.R., Harada T., Engel J.D., and Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat. Genet. 35 (2003) 238-245
92. Rangasamy T., Cho C.Y., Thimmulappa R.K., Zhen L., Srisuma S.S., Kensler T.W., Yamamoto M., Petrache I., Tuder R.M., and Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 114 (2004) 1248-1259
93. Shibahara S., Muller R.M., and Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J. Biol. Chem. 262 (1987) 12889-12892
94. Lee P.J., Jiang B.H., Chin B.Y., Iyer N.V., Alam J., Semenza G.L., and Choi A.M. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272 (1997) 5375-5381
95. Takeda K., Ishizawa S., Sato M., Yoshida T., and Shibahara S. Identification of a cis-acting element that is responsible for cadmium-mediated induction of the human heme oxygenase gene. J. Biol. Chem. 269 (1994) 22858-22867
96. Kronke G., Bochkov V.N., Huber J., Gruber F., Bluml S., Furnkranz A., Kadl A., Binder B.R., and Leitinger N. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J. Biol. Chem. 278 (2003) 51006-51014
97. Yang G., Nguyen X., Ou J., Rekulapelli P., Stevenson D.K., and Dennery P.A. Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 97 (2001) 1306-1313
98. Sikorski E.M., Hock T., Hill-Kapturczak N., and Agarwal A. The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury. Am. J. Physiol., Renal Physiol. 286 (2004) F425-F441
99. Shibahara S., Sato M., Muller R.M., and Yoshida T. Structural organization of the human heme oxygenase gene and the function of its promoter. Eur. J. Biochem. 179 (1989) 557-563
100. Tyrrell R.M., Applegate L.A., and Tromvoukis Y. The proximal promoter region of the human heme oxygenase gene contains elements involved in stimulation of transcriptional activity by a variety of agents including oxidants. Carcinogenesis 14 (1993) 761-765
101. Muraosa Y., and Shibahara S. Identification of a cis-regulatory element and putative trans-acting factors responsible for 12-O-tetradecanoylphorbol-13-acetate (TPA)-mediated induction of heme oxygenase expression in myelomonocytic cell lines. Mol. Cell. Biol. 13 (1993) 7881-7891
102. Nascimento A.L., Luscher P., and Tyrrell R.M. Ultraviolet A (320-380 nm) radiation causes an alteration in the binding of a specific protein/protein complex to a short region of the promoter of the human heme oxygenase 1 gene. Nucleic Acids Res. 21 (1993) 1103-1109
103. Deramaudt B.M., Remy P., and Abraham N.G. Upregulation of human heme oxygenase gene expression by Ets-family proteins. J. Cell. Biochem. 72 (1999) 311-321
104. Lavrovsky Y., Schwartzman M.L., Levere R.D., Kappas A., and Abraham N.G. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc. Natl. Acad. Sci. USA 91 (1994) 5987-5991
105. Deramaudt T.B., da Silva J.L., Remy P., Kappas A., and Abraham N.G. Negative regulation of human heme oxygenase in microvessel endothelial cells by dexamethasone. Proc. Soc. Exp. Biol. Med. 222 (1999) 185-193
106. Takahashi S., Matsuura N., Kurokawa T., Takahashi Y., and Miura T. Co-operation of the transcription factor hepatocyte nuclear factor-4 with Sp1 or Sp3 leads to transcriptional activation of the human haem oxygenase-1 gene promoter in a hepatoma cell line. Biochem. J. 367 (2002) 641-652
107. Takahashi S., Takahashi Y., Ito K., Nagano T., Shibahara S., and Miura T. Positive and negative regulation of the human heme oxygenase-1 gene expression in cultured cells. Biochim. Biophys. Acta 1447 (1999) 231-235
108. Yamada N., Yamaya M., Okinaga S., Nakayama K., Sekizawa K., Shibahara S., and Sasaki H. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am. J. Hum. Genet. 66 (2000) 187-195
109. Fu W.P., Sun C., Dai L.M., Yang L.F., and Zhang Y.P. Relationship between COPD and polymorphisms of HOX-1 and mEPH in a Chinese population. Oncol. Rep. 17 (2007) 483-488
110. Fu W.P., Zhao Z.H., Fang L.Z., Sun C., Liu L., Zhang J.Q., Zhang Y.P., and Dai L.M. Heme oxygenase-1 polymorphism associated with severity of chronic obstructive pulmonary disease. Chin. Med. J. (Engl.) 120 (2007) 12-16
111. Nakayama K., Kikuchi A., Yasuda H., Ebihara S., Sasaki T., Ebihara T., and Yamaya M. Heme oxygenase-1 gene promoter polymorphism and decline in lung function in Japanese men. Thorax 61 (2006) 921
112. Guenegou A., Leynaert B., Benessiano J., Pin I., Demoly P., Neukirch F., Boczkowski J., and Aubier M. Association of lung function decline with the heme oxygenase-1 gene promoter microsatellite polymorphism in a general population sample: results from the European Community Respiratory Health Survey (ECRHS), France. J. Med. Genet. 43 (2006) e43
113. Siedlinski M., van Diemen C.C., Postma D.S., and Boezen H.M. Heme oxygenase 1 variations and lung function decline in smokers: proof of replication. J. Med. Genet. 45 (2008) 400
114. Alexeeff S.E., Litonjua A.A., Wright R.O., Baccarelli A., Suh H., Sparrow D., Vokonas P.S., and Schwartz J. Ozone exposure, antioxidant genes, and lung function in an elderly cohort: VA normative aging study. Occup. Environ. Med. 65 (2008) 736-742
115. He J.Q., Ruan J., Connett J.E., Anthonisen N.R., Pare P.D., and Sandford A.J. Antioxidant gene polymorphisms and susceptibility to a rapid decline in lung function in smokers. Am. J. Respir. Crit. Care Med. 166 (2002) 323-328
116. Hersh C.P., Demeo D.L., Lange C., Litonjua A.A., Reilly J.J., Kwiatkowski D., Laird N., Sylvia J.S., Sparrow D., Speizer F.E., Weiss S.T., and Silverman E.K. Attempted replication of reported chronic obstructive pulmonary disease candidate gene associations. Am. J. Respir. Cell Mol. Biol. 33 (2005) 71-78
117. Hirai H., Kubo H., Yamaya M., Nakayama K., Numasaki M., Kobayashi S., Suzuki S., Shibahara S., and Sasaki H. Microsatellite polymorphism in heme oxygenase-1 gene promoter is associated with susceptibility to oxidant-induced apoptosis in lymphoblastoid cell lines. Blood 102 (2003) 1619-1621
118. Petrache I., Otterbein L.E., Alam J., Wiegand G.W., and Choi A.M. Heme oxygenase-1 inhibits TNF-alpha-induced apoptosis in cultured fibroblasts. Am. J. Physiol., Lung Cell Mol. Physiol. 278 (2000) L312-L319
119. Brouard S., Otterbein L.E., Anrather J., Tobiasch E., Bach F.H., Choi A.M., and Soares M.P. Carbon monoxide generated by heme oxygenase-1 suppresses endothelial cell apoptosis. J. Exp. Med. 192 (2000) 1015-1026
120. Brouard S., Berberat P.O., Tobiasch E., Seldon M.P., Bach F.H., and Soares M.P. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis. J. Biol. Chem. 277 (2002) 17950-17961
121. Kim H.P., Wang X., Suh G.Y., Zhang J., Ryter S.W., and Choi A.M.K. Heat shock factor-1 mediates the cytoprotective effect of carbon monoxide. J. Immunol. 175 (2005) 2622-2629
122. Liu X.M., Chapman G.B., Peyton K.J., Schafer A.I., and Durante W. Antiapoptotic action of carbon monoxide on cultured vascular smooth muscle cells. Exp. Biol. Med. (Maywood) 228 (2003) 572-575
123. Liu X.M., Chapman G.B., Peyton K.J., Schafer A.I., and Durante W. Carbon monoxide inhibits apoptosis in vascular smooth muscle cells. Cardiovasc. Res. 55 (2002) 396-405
124. Thom S.R., Fisher D., Xu Y.A., Notarfrancesco K., and Ischiropoulos H. Adaptive responses and apoptosis in endothelial cells exposed to carbon monoxide. Proc. Natl. Acad. Sci. USA 97 (2000) 1305-1310
125. Liu X.M., Chapman G.B., Wang H., and Durante W. Adenovirus-mediated heme oxygenase-1 gene expression stimulates apoptosis in vascular smooth muscle cells. Circulation 105 (2002) 9-84
126. Fogg S., Agarwal A., Nick H.S., and Visner G.A. Iron regulates hyperoxia-dependent human heme oxygenase 1 gene expression in pulmonary endothelial cells. Am. J. Respir. Cell Mol. Biol. 20 (1999) 797-804
127. Lee P.J., Alam J., Sylvester S.L., Inamdar N., Otterbein L., and Choi A.M. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am. J. Respir. Cell Mol. Biol. 14 (1996) 556-568
128. Lee P.J., Alam J., Wiegand G.W., and Choi A.M. 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 93 (1996) 10393-10398
129. Otterbein L.E., Otterbein S.L., Ifedigbo E., Liu F., Morse D.E., Fearns C., Ulevitch R.J., Knicklebein R., Flavell R.A., and Choi A.M. MKK3 mitogen activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant induced lung injury. Am. J. Pathol. 163 (2003) 2555-2563
130. Zhang X., Shan P., Jiang G., Zhang S.S., Otterbein L.E., Fu X.Y., and Lee P.J. Endothelial STAT3 is essential for the protective effects of HO-1 in oxidant-induced lung injury. FASEB J. 20 (2006) 2156-2158
131. Wang X., Wang Y., Kim H.P., Nakahira K., Ryter S.W., and Choi A.M. Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J. Biol. Chem. 282 (2007) 1718-1726
132. Zhang X., Shan P., Alam J., Davis R.J., Flavell R.A., and Lee P.J. 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. 278 (2003) 22061-22070
133. Zhang X., Shan P., Otterbein L.E., Alam J., Flavell R.A., Davis R.J., Choi A.M., and Lee P.J. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase and involves caspase-3. J. Biol. Chem. 278 (2003) 1248-1258
134. Zhang X., Shan P., Alam J., Fu X.Y., and Lee P.J. Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury. J. Biol. Chem. 280 (2005) 8714-8721
135. Rahman I., and MacNee W. Role of oxidants/antioxidants in smoking-induced lung diseases. Free Radic. Biol. Med. 21 (1996) 669-681
136. Rennard S.I. Cigarette smoke in research. Am. J. Respir. Cell Mol. Biol. 31 (2004) 479-480
137. Liu X., Conner H., Kobayashi T., Kim H., Wen F., Abe S., Fang Q., Wang X., Hashimoto M., Bitterman P., and Rennard S.I. Cigarette smoke extract induces DNA damage but not apoptosis in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 33 (2005) 121-129
138. Hoshino Y., Mio T., Nagai S., Miki H., Ito I., and Izumi T. Cytotoxic effects of cigarette smoke extract on an alveolar type II cell-derived cell line. Am. J. Physiol. 281 (2001) L509-L516
139. Park J.W., Kim H.P., Lee S.-J., Wang X., Wang Y., Ifedigbo E., Watkins S.C., Ohba M., Ryter S.W., Vyas Y.M., and Choi A.M. Protein kinase Cα and ζ differentially regulate death-inducing signaling complex formation in cigarette smoke extract-induced apoptosis. J. Immunol. 180 (2008) 4668-4678
140. Fukano Y., Yoshimura H., and Yoshida T. Heme oxygenase-1 gene expression in human alveolar epithelial cells (A549) following exposure to whole cigarette smoke on a direct in vitro exposure system. Exp. Toxicol. Pathol. 57 (2006) 411-418
141. Knorr-Wittmann C., Hengstermann A., Gebel S., Alam J., and Muller T. Characterization of Nrf2 activation and heme oxygenase-1 expression in NIH3T3 cells exposed to aqueous extracts of cigarette smoke. Free Radic. Biol. Med. 39 (2005) 1438-1448
142. Palozza P., Serini S., Curro D., Calviello G., and Igarashi K. Mancuso, C. beta-Carotene and cigarette smoke condensate regulate heme oxygenase-1 and its repressor factor Bach1: relationship with cell growth. Antioxid. Redox Signal. 8 (2006) 1069-1080
143. Reiter T.A., Pang B., Dedon P., and Demple B. Resistance to nitric oxide-induced necrosis in heme oxygenase-1 overexpressing pulmonary epithelial cells associated with decreased lipid peroxidation. J. Biol. Chem. 281 (2006) 36603-36612
144. Kim H.P., Wang X., Chen Z.-H., Lee S.-J., Huang M.-H., Wang Y., Ryter S.W., and Choi A.M.K. Autophagic proteins regulate cigarette smoke induced apoptosis: protective role of heme oxygenase-1. Autophagy 4 (2008) 887-895
145. Jimbo A., Fujita E., Kouroko Y., Ohnishi J., Inohara N., Kuida K., Sakamaki K., Yonehara S., and Momoi T. ER stress induces caspase-8 activation, stimulating cytochrome c release and caspase-9 activation. Exp. Cell Res. 283 (2003) 156-166
146. Rao R.V., Castro-Obregon S., Frankowski H., Schuler M., Stoka V., del Rio G., Bredesen D.E., and Ellerby H.M. Coupling endoplasmic reticulum stress to the cell death program: an Apaf-1-independent intrinsic pathway. J. Biol. Chem. 277 (2002) 21836-21842
147. Liu X.M., Peyton K.J., Ensenat D., Wang H., Schafer A.I., Alam J., and Durante W. Endoplasmic reticulum stress stimulates heme oxygenase-1 gene expression in vascular smooth muscle: role in cell survival. J. Biol. Chem. 280 (2005) 872-877
148. Kim K.M., Pae H.O., Zheng M., Park R., Kim Y.M., and Chung H.T. Carbon monoxide induces heme oxygenase-1 via activation of protein kinase R-like endoplasmic reticulum kinase and inhibits endothelial cell apoptosis triggered by endoplasmic reticulum stress. Circ. Res. 101 (2007) 919-927
149. Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., and Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science 235 (1987) 1043-1046
150. Foresti R., Green C.J., and Motterlini R. Generation of bile pigments by haem oxygenase: a refined cellular strategy in response to stressful insults. Biochem. Soc. Symp. 71 (2004) 177-192
151. Baranano D.E., Rao M., Ferris C.D., and Snyder S.H. Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. USA 99 (2002) 16093-16098
152. Tang L.M., Wang Y.P., Wang K., Pu L.Y., Zhang F., Li X.C., Kong L.B., Sun B.C., Li G.Q., and Wang X.H. Exogenous biliverdin ameliorates ischemia-reperfusion injury in small-for-size rat liver grafts. Transplant. Proc. 39 (2007) 1338-1344
153. Nakao A., Murase N., Ho C., Toyokawa H., Billiar T.R., and Kanno S. Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation 112 (2005) 587-591
154. Ollinger R., Bilban M., Erat A., Froio A., McDaid J., Tyagi S., Csizmadia E., Graca-Souza A.V., Liloia A., Soares M.P., Otterbein L.E., Usheva A., Yamashita K., and Bach F.H. Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 112 (2005) 1030-1039
155. Maines M.D. New insights into biliverdin reductase functions: linking heme metabolism to cell signaling. Physiology (Bethesda) 20 (2005) 382-389
156. Miralem T., Hu Z., Torno M.D., Lelli K.M., and Maines M.D. siRNA-mediated gene silencing of human biliverdin reductase, but not that of heme oxygenase-1, attenuates arsenite-mediated induction of the oxygenase and increases apoptosis in 293A kidney cells. J. Biol. Chem. 280 (2005) 17084-17092
157. Pachori A.S., Smith A., McDonald P., Zhang L., Dzau V.J., and Melo L.G. Heme-oxygenase-1-induced protection against hypoxia/reoxygenation is dependent on biliverdin reductase and its interaction with PI3K/Akt pathway. J. Mol. Cell. Cardiol. 43 (2007) 580-592
158. Balla G., Vercellotti G.M., Eaton J.W., and Jacob H.S. Iron loading of endothelial cells augments oxidant damage. J. Lab. Clin. Med. 116 (1990) 546-554
159. Greene B.T., Thorburn J., Willingham M.C., Thorburn A., Planalp R.P., Brechbiel M.W., Jennings-Gee J., Wilkinson J., Torti F.M., and Torti S.V. Activation of caspase pathways during iron chelator-mediated apoptosis. J. Biol. Chem. 277 (2002) 25568-25575
160. Suttner D.M., and Dennery P.A. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J. 13 (1999) 1800-1809
161. Suttner D.M., Sridhar K., Lee C.S., Tomura T., Hansen T.N., and Dennery P.A. Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells. Am. J. Physiol. 276 (1999) L443-L451
162. Kvam E., Hejmadi V., Ryter S., Pourzand C., and Tyrrell R.M. Heme oxygenase activity causes transient hypersensitivity to oxidative ultraviolet A radiation that depends on release of iron from heme. Free Radic. Biol. Med. 28 (2000) 1191-1196
163. Ferris C.D., Jaffrey S.R., Sawa A., Takahashi M., Brady S.D., Barrow R.K., Tysoe S.A., Wolosker H., Baranano D.E., Dore S., Poss K.D., and Snyder S.H. Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1 (1999) 152-157
164. Vile G.F., Basu-Modak S., Waltner C., and Tyrrell R.M. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. USA 91 (1994) 2607-2610
165. Lin F., and Girotti A.W. Hemin-enhanced resistance of human leukemia cells to oxidative killing: antisense determination of ferritin involvement. Arch. Biochem. Biophys. 352 (1998) 51-58
166. Berberat P.O., Katori M., Kaczmarek E., Anselmo D., Lassman C., Ke B., Shen X., Busuttil R.W., Yamashita K., Csizmadia E., Tyagi S., Otterbein L.E., Brouard S., Tobiasch E., Bach F.H., Kupiec-Weglinski J.W., and Soares M.P. Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury. FASEB J. 17 (2003) 1724-1726
167. Baranano D.E., Wolosker H., Bae B.I., Barrow R.K., Snyder S.H., and Ferris C.D.A. mammalian iron ATPase induced by iron. J. Biol. Chem. 275 (2000) 15166-15173
168. Choi B.M., Pae H.O., Jeong Y.R., Oh G.S., Jun C.D., Kim B.R., Kim Y.M., and Chung H.T. Overexpression of heme oxygenase (HO)-1 renders Jurkat T cells resistant to fas-mediated apoptosis: involvement of iron released by HO-1. Free Radic. Biol. Med. 36 (2004) 858-871
169. Mishra S., Fujita T., Lama V.N., Nam D., Liao H., Okada M., Minamoto K., Yoshikawa Y., Harada H., and Pinsky D.J. Carbon monoxide rescues ischemic lungs by interrupting MAPK-driven expression of early growth response 1 gene and its downstream target genes. Proc. Natl. Acad. Sci. USA 13 (2006) 5191-5196
170. Zhang X., Shan P., Jiang D., Noble P.W., Abraham N.G., Kappas A., and Lee P.J. Small interfering RNA targeting heme oxygenase-1 enhances ischemia-reperfusion-induced lung apoptosis. J. Biol. Chem. 279 (2004) 10677-10684
171. Parks D.A., and Granger D.N. Contributions of ischemia and reperfusion to mucosal lesion formation. Am. J. Physiol. 250 (1986) G749-G753
172. Katori M., Buelow R., Ke B., Ma J., Coito A.J., Iyer S., Southard D., Busuttil R.W., and Kupiec-Weglinski J.W. Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an anti-apoptotic pathway. Transplantation 73 (2002) 287-292
173. Amersi F., Buelow R., Kato H., Ke B., Coito A.J., Shen X.D., Zhao D., Zaky J., Melinek J., Lassman C.R., Kolls J.K., Alam J., Ritter T., Volk H.D., Farmer D.G., Ghobrial R.M., Busuttil R.W., and Kupiec-Weglinski J.W. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J. Clin. Invest. 104 (1999) 1631-1639
174. Blydt-Hansen T., Katori M., Lassman C., Ke B., Coito A.J., Iyer S., Buelow R., Ettenger R., Busuttil R.W., and Kupiec-Weglinski J.W. Gene transfer-induced local heme oxygenase-1 overexpression protects rat kidneys from ischemia/reperfusion injury. J. Am. Soc. Nephrol. 14 (2002) 745-754
175. Squiers E., Bruch D., Buelow R., and Tice D. Pretreatment of small bowel isograft donors with cobalt-protoporphyrin decreases preservation injury. Transplant. Proc. 31 (1999) 585-586
176. Pileggi A., Molano R., Berney T., Cattan P., Vizzardelli C., Oliver R., Fraker C., Ricordi C., Pastori R.L., Bach F.H., and Inverardi L. Heme oxygenase-1 induction in islet cells results in protection from apoptosis and improved in vivo function after transplantation. Diabetes 50 (2001) 1983-1991
177. Rucker M., Schafer T., Roesken F., Spitzer W., Bauer M., and Menger M. Local heat-shock priming-induced improvement in microvascular perfusion in osteomyocutaneous flaps is mediated by heat-shock protein 32. Br. J. Surg. 88 (2001) 450-457
178. Ozaki K.S., Marques G.M., Nogueira E., Feitoza R.Q., Cenedeze M.A., Franco M.F., Mazzali M., Soares M.P., Pacheco-Silva A., and Câmara N.O. Improved renal function after kidney transplantation is associated with heme oxygenase-1 polymorphism. Clin. Transplant. 22 (2008) 609-616
179. Nath K., Balla G., Vercellotti G., Balla J., Jacob H., and Levitt M. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J. Clin. Invest. 90 (1992) 267-270
180. Brune B., and Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32 (1987) 497-504
181. Sato K., Balla J., Otterbein L., Smith R.N., Brouard S., Lin Y., Csizmadia E., Sevigny J., Robson S.C., Vercellotti G., Choi A.M., Bach F.H., and Soares M.P. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol. 166 (2001) 4185-4194
182. Otterbein L.E., Zuckerbraun B.S., Haga M., Liu F., Song R., Usheva A., Stachulak C., Bodyak N., Smith R.N., Csizmadia E., Tyagi S., Akamatsu Y., Flavell R.J., Billiar T.R., Tzeng E., Bach F.H., Choi A.M., and Soares M.P. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat. Med. 9 (2003) 183-190
183. Nakao A., Kimizuka K., Stolz D.B., Seda Neto J., Kaizu T., Choi A.M., Uchiyama T., Zuckerbraun B.S., Bauer A.J., Nalesnik M.A., Otterbein L.E., Geller D.A., and Murase N. Protective effect of carbon monoxide inhalation for cold-preserved small intestinal grafts. Surgery 134 (2003) 285-292
184. Faleo G., Neto J.S., Kohmoto J., Tomiyama K., Shimizu H., Takahashi T., Wang Y., Sugimoto R., Choi A.M., Stolz D.B., Carrieri G., McCurry K.R., Murase N., and Nakao A. Carbon monoxide ameliorates renal cold ischemia-reperfusion injury with an upregulation of vascular endothelial growth factor by activation of hypoxia-inducible factor. Transplantation 85 (2008) 1833-1840
185. Kaizu T., Nakao A., Tsung A., Toyokawa H., Sahai R., Geller D.A., and Murase N. Carbon monoxide inhalation ameliorates cold ischemia/reperfusion injury after rat liver transplantation. Surgery 138 (2005) 229-235
186. Song R., Kubo M., Morse D., Zhou Z., Zhang X., Dauber J.H., Fabisiak J., Alber S.M., Watkins S.C., Zuckerbraun B.S., Otterbein L.E., Ning W., Oury T.D., Lee P.J., McCurry K.R., and Choi A.M. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am. J. Pathol. 163 (2003) 231-242
187. Nakao A., Toyokawa H., Tsung A., Nalesnik M.A., Stolz D.B., Kohmoto J., Ikeda A., Tomiyama K., Harada T., Takahashi T., Yang R., Fink M.P., Morita K., Choi A.M., and Murase N. Ex vivo application of carbon monoxide in University of Wisconsin solution to prevent intestinal cold ischemia/reperfusion injury. Am. J. Transplant. 6 (2006) 2243-2255
188. Musameh M.D., Green C.J., Mann B.E., Fuller B.J., and Motterlini R. Improved myocardial function after cold storage with preservation solution supplemented with a carbon monoxide-releasing molecule (CORM-3). J. Heart Lung Transplant. 26 (2007) 1192-1198
189. Gunther L., Berberat P.O., Haga M., Brouard S., Smith R.N., Soares M.P., Bach F.H., and Tobiasch E. Carbon monoxide protects pancreatic β-cells from apoptosis and improves islet function/survival after transplantation. Diabetes 51 (2002) 994-999
190. Nakao A., Kimizuka K., Stolz D.B., Neto J.S., Kaizu T., Choi A.M., Uchiyama T., Zuckerbraun B.S., Nalesnik M.A., Otterbein L.E., and Murase N. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am. J. Pathol. 163 (2003) 1587-1598
191. Akamatsu Y., Haga M., Tyagi S., Yamashita K., Graca-Souza A.V., Ollinger R., Czismadia E., May G.A., Ifedigbo E., Otterbein L.E., Bach F.H., and Soares M.P. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J. 18 (2004) 771-772
192. Pannen B.H.J., Köhler N., Hole B., Bauer M., Clemens M.G., and Geiger K.K. Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J. Clin. Invest. 102 (1998) 1220-1228
193. Amersi F., Shen X.D., Anselmo D., Melinek J., Iyer S., Southard D.J., Katori M., Volk H.D., Busuttil R.W., Buelow R., and Kupiec-Weglinski J. W. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 35 (2002) 815-823
194. Fondevila C., Shen X.D., Tsuchiyashi S., Yamashita K., Csizmadia E., Lassman C., Busuttil R.W., Kupiec-Weglinski J.W., and Bach F.H. Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 40 (2004) 1333-1341
195. Adin C.A., Croker B.P., and Agarwal A. Protective effects of exogenous bilirubin on ischemia-reperfusion injury in the isolated, perfused rat kidney. Am. J. Physiol., Renal Physiol. 288 (2005) F778-F784
196. Yamashita K., McDaid J., Ollinger R., Tsui T.Y., Berberat P.O., Usheva A., Csizmadia E., Smith R.N., Soares M.P., and Bach F.H. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J. 18 (2004) 765-767
197. Nakao A., Neto J.S., Kanno S., Stolz D.B., Kimizuka K., Liu F., Bach F.H., Billiar T.R., Choi A.M., Otterbein L.E., and Murase N. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am. J. Transplant. 5 (2005) 282-291
198. Otterbein L.E., Mantell L.L., and Choi A.M. Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol. 276 (1999) L688-L694
199. Otterbein L.E., Bach F.H., Alam J., Soares M., Tao Lu H., Wysk M., Davis R.J., Flavell R.A., and Choi A.M. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6 (2000) 422-428
200. Motterlini R., Mann B.E., and Foresti R. Therapeutic applications of carbon monoxide-releasing molecules. Expert Opin. Invest. Drugs 14 (2005) 1305-1318