Bile pigments in pulmonary and vascular disease

Frontiers in Pharmacology

Volumn 3 MAR, Issue , 2012, Pages

  Ryter, Stefan W ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

Author keywords

Antioxidant; Bilirubin; Biliverdin; Cardiovascular disease; Pulmonary disease

Indexed keywords

BILIRUBIN; BILIVERDIN; C REACTIVE PROTEIN; HEME OXYGENASE 1; HEME OXYGENASE 2; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ACUTE GRAFT REJECTION; ANTIANGIOGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CARDIAC GRAFT REJECTION; CARDIOVASCULAR DISEASE; CELL PROLIFERATION; CELL PROTECTION; CEREBROVASCULAR ACCIDENT; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFICACY; DRUG STRUCTURE; FRAMINGHAM RISK SCORE; GENE; GENETIC ASSOCIATION; GRAFT SURVIVAL; HEART INFARCTION; HEART PROTECTION; HUMAN; IMMUNOMODULATION; INTRACELLULAR SIGNALING; ISCHEMIC HEART DISEASE; LIVER GRAFT REJECTION; LIVER INJURY; LIVER ISCHEMIA; LUNG DISEASE; LUNG FIBROSIS; LUNG GRAFT REJECTION; LUNG INJURY; NEOINTIMA; NEUROTOXICITY; NEWBORN JAUNDICE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN FUNCTION; REPERFUSION INJURY; RISK FACTOR; TISSUE INJURY; TREATMENT OUTCOME; UGT1A1 GENE;

EID: 84865998135     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00039     Document Type: Article

References (104)

1. Abraham, N. G., Asija, A., Drummond, G., and Peterson, S. (2007). Heme oxygenase-1 gene therapy: recent advances and therapeutic applications. Curr. Gene Ther. 7, 89-108.
2. Adin, C. A., Croker, B. P., and Agarwal, A. (2005). Protective effects of exogenous bilirubin on ischemiareperfusion injury in the isolated, perfused rat kidney. Am. J. Physiol. Renal Physiol. 288, F778-F784.
3. Ajja, R., Lee, D. C., Sui, X., Church, T. S., and Steven, N. B. (2011). Usefulness of serum bilirubin and cardiorespiratory fitness as predictors of mortality in men. Am. J. Cardiol. 108, 1438-1442.
4. Baranano, D. E., Rao, M., Ferris, C. D., and Snyder, S. H. (2002). Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. U.S.A. 99, 16093-16098.
5. Blanckaert, N., and Fevery, J. (1990). " Physiology and pathophysiology of bilirubin metabolism," in Hepatology. A Textbook of Liver Disease, 2nd Edn, Vol. 1, eds D. Zakim and T. D. Boyer (Philadelphia: W. D. Saunders), 254-302.
6. Breimer, L. H., Spyropolous, K. A., Winder, A. F., Mikhailidis, D. P., and Hamilton, G. (1994). Is bilirubin protective against coronary artery disease. Clin. Chem. 40, 1987-1988.
7. Breimer, L. H., Wannamethee, G., Ebrahim, S., and Shaper, A. G. (1995). Serum bilirubin and risk of ischemic heart disease in middleaged British men. Clin. Chem. 41, 1504-1508.
8. Brito, M. A., Lima, S., Fernandes, A., Falcão, A. S., Silva, R. F., Butterfield, D. A., and Brites, D. (2008). Bilirubin injury to neurons: contribution of oxidative stress and rescue by glycoursodeoxycholic acid. Neurotoxicology 29, 259-269.
9. Bulmer, A. C., Blanchfield, J. T., Toth, I., Fassett, R. G., and Coombes, J. S. (2008). Improved resistance to serum oxidation in Gilbert's syndrome: a mechanism for cardiovascular protection. Atherosclerosis 199, 390-396.
10. Cheriyath, P., Gorrepati, V. S., Peters, I., Nookala, V., Murphy, M. E., Srouji, N., and Fischman, D. (2010). High total bilirubin as a protective factor for diabetes mellitus: an analysis of NHANES data from 1999-2006. J. Clin. Med. Res. 2, 201-216.
11. Chowdhury, J. R., and Chowdhury, N. R. (1983). Conjugation and excretion of bilirubin. Semin. Liver Dis. 3, 11-23.
12. Chowdhury, J. R., Chowdhury, N. R., Bhargava, M. M., and Arias, I. M. (1979). Purification and partial characterization of rat liver bilirubin glucuronoside glucuronosyltransferase. J. Biol. Chem. 254, 8336-8339.
13. Clark, J. E., Foresti, R., Green, C. J., and Motterlini, R. (2000a). Dynamics of haem oxygenase-1expression and bilirubin production in cellular protection against oxidative stress. Biochem. J. 348, 615-619.
14. Clark, J. E., Foresti, R., Sarathchandra, P., Kaur, H., Green, C. J., and Motterlini, R. (2000b). Heme oxygenase-1derived bilirubin ameliorates postischemic myocardial dysfunction. Am. J. Physiol. 278, H643-H651.
15. Cui, Y., König, J., Leier, I., Buchholz, U., and Keppler, D. (2001). Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J. Biol. Chem. 276, 9626-9630.
16. Davies, K. J. (1995). Oxidative stress: the paradox of aerobic life. Biochem. Soc. Symp. 61, 1-31.
17. Davies, K. J. (2000). Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50, 279-289.
18. Dennery, P. A., McDonagh, A. F., Spitz, D. R., Rodgers, P. A., and Stevenson, D. K. (1995). Hyperbilirubinemia results in reduced oxidative injury in neonatal Gunn rats exposed to hyperoxia. Free Radic. Biol. Med. 19, 395-404.
19. Djousse, L., Levy, D., Cupples, L. A., Evans, J. C., D'Agostino, R. B., and Ellison, R. C. (2001). Total serum bilirubin and risk of cardiovascular disease in the Framingham Offspring Study. Am. J. Cardiol. 87, 1196-1200.
20. Djoussé, L., Rothman, K. J., Cupples, L. A., Levy, D., and Ellison, R. C. (2003). Effect of serum albumin and bilirubin on the risk of myocardial infarction (the Framingham Offspring Study). Am. J. Cardiol. 91, 485-488.
21. Doré, S., Takahashi, M., Ferris, C. D., Zakhary, R., Hester, L. D., Guastella, D., and Snyder, S. H. (1999). Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl. Acad. Sci. U.S.A. 96, 2445-2450.
22. Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
23. Erdogan, D., Gullu, H., Yildirim, E., Tok, D., Kirabas, I., Ciftci, O., Baycan, S. T., and Muderrisoglu, H. (2005). Low serum bilirubin levels are independently and inversely related to impaired flow-mediated vasodilation and increased carotid intima-media thickness in both men and women. Atherosclerosis 184, 431-437.
24. Fondevila, C., Shen, X. D., Tsuchiyashi, S., Yamashita, K., Csizmadia, E., Lassman, C., Busuttil, R. W., Kupiec Weglinski, J. W., and Bach, F. H. (2004). Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 40, 1333-1341.
25. Foresti, R., Green, C. J., and Motterlini, R. (2004). Generation of bile pigments by haem oxygenase: a refined cellular strategy in response to stressful insults. Biochem. Soc. Symp. 71, 177-192.
26. Forman, H. J., Maiorino, M., and Ursini, F. (2010). Signaling functions of reactive oxygen species. Biochemistry 49, 835-842.
27. Franchini, M., Targher, G., and Lippi, G. (2010). Serum bilirubin levels and cardiovascular disease risk: a Janus Bifrons? Adv. Clin. Chem. 50, 47-63.
28. Fujii, M., Inoguchi, T., Sasaki, S., Maeda, Y., Zheng, J., Kobayashi, K., and Takayanagi, R. (2010). Bilirubin and biliverdin protect rodents against diabetic nephropathy by downregulating NAD(P)H oxidase. Kidney Int. 78, 905-919.
29. Fukui, M., Tanaka, M., Shiraishi, E., Harusato, I., Hosoda, H., Asano, M., Hasegawa, G., and Nakamura, N. (2008). Relationship between serum bilirubin and albuminuria in patients with type 2 diabetes. Kidney Int. 74, 1197-1201.
30. Fukui, M., Tanaka, M., Yamazaki, M., Hasegawa, G., Nishimura, M., Iwamoto, N., Ono, T., Imai, S., and Nakamura, N. (2011). Low serum bilirubin concentration in haemodialysis patients with Type 2 diabetes. Diabet. Med. 28, 96-99.
31. García-Lafuente, A., Guillamón, E., Villares, A., Rostagno, M. A., and Martínez, J. A. (2009). Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflamm. Res. 58, 537-552.
32. Ghersi-Egea, J. F., Gazzin, S., and Strazielle, N. (2009). Blood-brain interfaces and bilirubin-induced neurological diseases. Curr. Pharm. Des. 15, 2893-2907.
33. Gullu, H., Erdogan, D., Tok, D., Topcu, S., Caliskan, M., Ulus, T., and Muderrisoglu, H. (2005). High serum bilirubin concentrations preserve coronary flow reserve and coronary microvascular functions. Arterioscler. Thromb. Vasc. Biol. 25, 2289-2294.
34. Halliwell, B., and Gutteridge, J. M. C. (1999). Free Radicals in Biology and Medicine. New York, NY: Oxford University Press.
35. Hopkins, P. N., Wu, L. L., Hunt, S. C., James, B. C., Vincent, G. M., and Williams, R. R. (1996). Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 16, 250-255.
36. Horsfall, L. J., Rait, G., Walters, K., Swallow, D. M., Pereira, S. P., Nazareth, I., and Petersen, I. (2011). Serum bilirubin and risk of respiratory disease and death. JAMA 305, 691-697.
37. Hwang, H. J., Lee, S. W., and Kim, S. H. (2011). Relationship between bilirubin and C-reactive protein. Clin. Chem. Lab. Med. 49, 1823-1828.
38. Ishizaka, N., Ishizaka, Y., Takahashi, E., Yamakado, M., and Hashimoto, H. (2001). High serum bilirubin level is inversely associated with the presence of carotid plaque. Stroke 32, 580-583.
39. Jo, J., Yun, J. E., Lee, H., Kimm, H., and Jee, S. H. (2011). Total, direct, and indirect serum bilirubin concentrations and metabolic syndrome among the Korean population. Endocrine 39, 182-189.
40. Kaliora, A. C., Dedoussis, G. V., and Schmidt, H. (2006). Dietary antioxidants in preventing atherogenesis. Atherosclerosis 187, 1-17.
41. Kamisako, T., Kobayasi, Y., Takeuchi, K., Ishihara, T., Higuchi, K., Tanaka, Y., Gabazza, E. C., and Adachi, Y. (2000). Recent advances in bilirubin metabolism research: the molecular mechanism of hepatocyte bilirubin transport and its clinical relevance. J. Gastroenterol. 35, 659-664.
42. Kapitulnik,J.,and Maines,M. D. (2009). Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol. Sci. 30, 129-137.
43. Kaur, H., Hughes, M. N., Green, C. J., Naughton, P., Foresti, R., and Motterlini, R. (2003). Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett. 543, 113-119.
44. Ko, G. T., Chan, J. C., Woo, J., Lau, E., Yeung, V. T., Chow, C. C., Li, J. K., So, W. Y., and Cockram, C. S. (1996). Serum bilirubin and cardiovascular risk factors in a Chinese population. J. Cardiovasc. Risk 3, 459-463.
45. Kwon, K. M., Kam, J. H., Kim, M. Y., Kim, M. Y., Chung, C. H., Kim, J. K., Linton, J. A., Eom, A., Koh, S. B., and Kang, H. T. (2011). Inverse association between total bilirubin and metabolic syndrome in rural korean women. J. Womens Health (Larchmt) 20, 963-969.
46. Lee, S. S., Gao, W., Mazzola, S., Thomas, M. N., Csizmadia, E., Otterbein, L. E., Bach, F. H., and Wang, H. (2007). Heme oxygenase-1, carbon monoxide, and bilirubin induce tolerance in recipients toward islet allografts by modulating T regulatory cells. FASEB J. 21, 3450-3457.
47. Levinson, S. S. (1997). Relationship between bilirubin, apolipoprotein B, and coronary artery disease. Ann. Clin. Lab. Sci. 27, 185-192.
48. Lin, J. P., O'Donnell, C. J., Schwaiger, J. P., Cupples, L. A., Lingenhel, A., Hunt, S. C., Yang, S., and Kronenberg, F. (2006). Association between the UGT1A1*28 allele, bilirubin levels, and coronary heart disease in the Framingham Heart Study. Circulation 114, 1476-1481.
49. Lin, J. P., Schwaiger, J. P., Cupples, L. A., O'Donnell, C. J., Zheng, G., Schoenborn, V., Hunt, S. C., Joo, J., and Kronenberg, F. (2009). Conditional linkage and genome-wide association studies identify UGT1A1 as a major gene for anti-atherogenic serum bilirubin levels-the Framingham Heart Study. Atherosclerosis 206, 228-233.
50. Litwack, G., Ketterer, B., and Arias, I. M. (1971). Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of exogenous organic anions. Nature 234, 466-467.
51. Maghzal,G. J.,Leck,M. C.,Collinson,E., Li, C., and Stocker, R. (2009). Limited role for the bilirubin-biliverdin redox amplification cycle in the cellular antioxidant protection by biliverdin reductase. J. Biol. Chem. 284, 29251-29259.
52. Maines, M. D. (1997). The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554.
53. Mancuso, C., Bonsignore, A., Di Stasio, E., Mordente, A., and Motterlini, R. (2003). Bilirubin and S-nitrosothiols interaction: evidence for a possible role of bilirubin as a scavenger of nitric oxide. Biochem. Pharmacol. 66, 2355-2363.
54. Mazzone, G. L., Rigato, I., Ostrow, J. D., Bossi, F., Bortoluzzi, A., Sukowati,C. H.,Tedesco,F.,and Tiribelli, C. (2009). Bilirubin inhibits the TNFalpha-related induction of three endothelial adhesion molecules. Biochem. Biophys. Res. Commun. 386, 338-344.
55. Meister,A., and Anderson, M. E. (1983). Glutathione.Annu. Rev. Biochem. 52, 711-760.
56. Miralem, T., Hu, Z., Torno, M. D., Lelli, K. M., and Maines, M. D. (2005). Small interference RNAmediated 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, 17084-17092.
57. Nakao, A., Murase, N., Ho, C., Toyokawa, H., Billiar, T. R., and Kanno, S. (2005). Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation 112, 587-591.
58. 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. (2000). Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am. J. Transplant. 5, 282-291.
59. Neuzil, J., and Stocker, R. (1993). Bilirubin attenuates radical-mediated damage to serum albumin. FEBS Lett. 331, 281-284.
60. Neuzil, J., and Stocker, R. (1994). Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J. Biol. Chem. 269, 16712-16719.
61. Noguchi, M., Yoshida, T., and Kikuchi, G. (1979). Specific requirement of NADPH-cytochrome c reductase for the microsomal heme oxygenase reaction yielding biliverdin IX alpha. FEBS Lett. 98, 281-284.
62. Nolting, P. R., Kusters, D. M., Hutten, B. A., Kastelein, J. J., and ExPRESS study group. (2011). Serum bilirubin levels in familial hypercholesterolemia: a new risk marker for cardiovascular disease? J. Lipid Res. 52, 1755-1759.
63. Novotný, L., and Vítek, L. (2003). Inverse relationship between serum bilirubin and atherosclerosis in men: a meta-analysis of published studies. Exp. Biol. Med. (Maywood) 228, 568-571.
64. 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. (2005). Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 112, 1030-1039.
65. Ollinger, R., Wang, H., Yamashita, K., Wegiel, B., Thomas, M., Margreiter, R., and Bach, F. H. (2007). Therapeutic applications of bilirubin and biliverdin in transplantation. Antioxid. Redox Signal. 9, 2175-2185.
66. Papez, M. J., Civalier, C. J., Thorne, L. B., and Gulley, M. L. (2009). UGT1A1 promoter genotype is not strongly associated with severity of coronary artery disease. Diagn. Mol. Pathol. 18, 226-231.
67. Pedersen, A. O., Shonheyder, F., and Broderson, R. (1977). Photooxidation of human serum albumin and its complex with bilirubin. Eur. J. Biochem. 72, 213-221.
68. Perlstein, T. S., Pande, R. L., Beckman, J. A., and Creager, M. A. (2008a). Serum total bilirubin level and prevalent lower-extremity peripheral arterial disease: National Health and Nutrition Examination Survey (NHANES) 1999 to 2004. Arterioscler. Thromb. Vasc. Biol. 28, 166-172.
69. Perlstein, T. S., Pande, R. L., Creager, M. A., Weuve, J., and Beckman, J. A. (2008b). Serum total bilirubin level, prevalent stroke, and stroke outcomes: NHANES 1999-2004. Am. J. Med. 121, 781-788.
70. Rantner, B., Kollerits, B., Anderwald Stadler, M., Klein-Weigel, P., Gruber, I., Gehringer, A., Haak, M., Schnapka-Köpf, M., Fraedrich, G., and Kronenberg, F. (2008). Association between the UGT1A1 TArepeat polymorphism and bilirubin concentration in patients with intermittent claudication: results from the CAVASIC study. Clin. Chem. 54, 851-857.
71. Rodella, L., Lamon, B. D., Rezzani, R., Sangras, B., Goodman, A. I., Falck, J. R., and Abraham, N. G. (2006). Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radic. Biol. Med. 40, 2198-2205.
72. Roy-Chowdhury, J. (1996). " Bilirubin metabolism and its disorders," in Hepatology. A Textbook of Liver Disease, 3rd Edn, Vol. 1, eds D. Zakim and T. D. Boyer (Philadelphia: W. D. Saunders), 323-361.
73. Roy-Chowdhury, N., Lu, Y., and Roy Chowdhury, J. (2008) " Bilirbuin metabolism," in Textbook of Hepatology: From Basic Science to Clinical Practice, 3rd Edn, eds J. Rodés, J. P. Benhamou,A. T. Blei, J. Reichen, and M. Rizzetto (Hoboken, NJ: Wiley), 165-174.
74. Ryter, S. W., Morse, D., and Choi, A. M. (2007). Carbon monoxide and bilirubin: potential therapies for pulmonary/vascular injury and disease. Am. J. Respir. Cell Mol. Biol. 36, 175-182.
75. Sarady-Andrews, J. K., Liu, F., Gallo, D., Nakao, A., Overhaus, M., Ollinger, R., Choi, A. M., and Otterbein, L. E. (2005). Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L1131-L1137.
76. Schwertner, H. A., Jackson, W. G., and Tolan, G. (1994). Association of low serum concentration of bilirubin with increased risk of coronary artery disease. Clin. Chem. 40, 18-23.
77. Schwertner, H. A., and Vítek, L. (2008). Gilbert syndrome, UGT1A1*28 allele, and cardiovascular disease risk: possible protective effects and therapeutic applications of bilirubin. Atherosclerosis 198, 1-11.
78. Sedlak, T. W., and Snyder, S. H. (2009). Cycling the wagons for biliverdin reductase. J. Biol. Chem. 284, 1-11.
79. Stevens, B., and Small, R. D. (1976). The photoperoxidation of unsaturated organic molecules-XV. O2 1Δg quenching by bilirubin and biliverdin. Photochem. Photobiol. 23, 33-36.
80. Stocker, R., and Ames, B. (1987). Potential role of conjugated bilirubin and copper in the metabolism of lipid peroxides in the bile. Proc. Natl. Acad. Sci. U.S.A. 84, 8130-8134.
81. Stocker, R., and Maghzal, G. J. (2009). Reply to Sedlak and Snyder: the little bighorn of the biliverdin reductase amplification cycle. J. Biol. Chem. 284, l-12.
82. Stocker, R., and Peterhans, E. (1989a). Synergistic interaction between vitamin E and the bile pigments bilirubin and biliverdin. Biochim. Biophys. Acta 1002, 238-244.
83. Stocker, R., and Peterhans, E. (1989b). Antioxidant properties of conjugated bilirubin and biliverdin: relevant scavenging of hypochlorous acid. Free Radic. Res. Commun. 6, 57-66.
84. Stocker, R., Yamamoto, Y., McDonagh, A., Glazer, A., and Ames, B. N. (1987a). Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1045.
85. Stocker, R., Glazer, A. N., and Ames, B. N. (1987b). Antioxidant activity of albumin-bound bilirubin. Proc. Natl. Acad. Sci. U.S.A. 84, 5918-5922.
86. Sugamura, K., and Keaney, J. F. Jr. (2011). Reactive oxygen species in cardiovascular disease. Free Radic. Biol. Med. 51, 978-992.
87. Tapan, S., Karadurmus, N., Dogru, T., Ercin, C. N., Tasci, I., Bilgi, C., Kurt, I., and Erbil, M. K. (2011). Decreased small dense LDL levels in Gilbert's syndrome. Clin. Biochem. 44, 300-303.
88. Tell, G., and Gustincich, S. (2009). Redox state, oxidative stress, and molecular mechanisms of protective and toxic effects of bilirubin on cells. Curr. Pharm. Des.15, 2908-2914.
89. Temme, E. H. M., Zhang, J. J., Schouten, E. G., and Kesteloot, H. (2001). Serum bilirubin and 10-year mortality risk in a Belgian population. Cancer Causes Control 12, 887-894.
90. Tenhunen, R., Marver, H. S., and Schmid, R. (1969). Microsomal heme oxygenase. Characterization of the enzyme. J. Biol. Chem. 244, 6388-6394.
91. Tenhunen, R., Ross, M. E., Marver, H. S., and Schmid, R. (1970). Reduced nicotinamide-adenine dinucleotide phosphate dependent biliverdin reductase: partial purification and characterization. Biochemistry 9, 298-303.
92. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40.
93. Vítek, L., Jirsa, M., Brodanová, M., Kaláb, M., Mareček, Z., Danzig, V., Novotný, L., and Kotal, P. (2002). Gilbert syndrome and ischemic heart disease: a protective effect of elevated bilirubin levels. Atherosclerosis 160, 449-456.
94. Vitek, L., and Ostrow, J. D. (2009). Bilirubin chemistry and metabolism; harmful and protective aspects. Curr. Pharm. Des. 15, 2869-2883.
95. Wang, H. D., Yamaya, M., Okinaga, S., Jia, Y. X., Kamanaka, M., Takahashi, H., Guo, L. Y., Ohrui, T., and Sasaki, H. (2002). Bilirubin ameliorates bleomycin-induced pulmonary fibrosis in rats. Am. J. Respir. Crit. Care Med. 165, 406-411.
96. Wang, X., Chowdhury, J. R., and Chowdhury, N. R. (2006a). Bilirubin metabolism: applied physiology. Curr. Pediatr. 16, 70-74.
97. Wang, H., Lee, S. S., Dell'Agnello, C., Tchipashvili, V., d'Avila, J. C., Czismadia, E., Chin, B. Y., and Bach, F. H. (2006b). Bilirubin can induce tolerance to islet allografts. Endocrinology 147, 762-768.
98. Wegiel, B., Gallo, D., Csizmadia, E., Roger, T., Kaczmarek, E., Harris, C., Zuckerbraun, B. S., and Otterbein, L. E. (2011). Biliverdin inhibits Toll-like receptor-4 (TLR4) expression through nitric oxide-dependent nuclear translocation of biliverdin reductase. Proc. Natl. Acad. Sci. U.S.A. 108, 18849-18854.
99. 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. (2004). Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J. 18, 765-767.
100. Yoshida, T., and Kikuchi, G. (1974). Sequence of the reaction of heme catabolism catalyzed by the microsomal heme oxygenase system. FEBS Lett. 48, 256-261.
101. Yoshida, T., Noguchi, M., and Kikuchi, G. (1980). Oxygenated form of heme heme oxygenase complex and requirement for second electron to initiate heme degradation from the oxygenated complex. J. Biol. Chem. 255, 4418-4420.
102. Yoshino, S., Hamasaki, S., Ishida, S., Kataoka, T., Yoshikawa, A., Oketani, N.,Saihara,K.,Okui,H.,Shinsato,T., Ichiki, H., Kubozono, T., Kuwahata, S.,Fujita,S.,Kanda,D.,Nakazaki,M., Miyata, M., and Tei, C. (2011). Relationship between bilirubin concentration, coronary endothelial function, and inflammatory stress in overweight patients. J. Atheroscler. Thromb. 18, 403-412.
103. Zhou,H.,Qian,H.,Liu,J.,Zhu,D.,Ding, W., Pan, P., Jin, D., Wang, J., and Li, W. (2011). Protection against lung graft injury from brain-dead donors with carbon monoxide,biliverdin,or both. J. Heart Lung Transplant. 30, 460-466.
104. Zhu, H., Wang, J., Jiang, H., Ma, Y., Pan, S., Reddy, S., and Sun, X. (2010). Bilirubin protects graftsagainst non-specific inflammationinduced injury in syngeneic intraportal islet transplantation. Exp. Mol. Med. 42, 739-748.