Evaluating the beneficial and detrimental effects of bile pigments in early and later life

Frontiers in Pharmacology

Volumn 3 JUN, Issue , 2012, Pages 1-5

  Dennery, Phyllis A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Antioxidant; Kernicterus; Neonatal jaundice; Polymorphisms; UDP glucuronyltransferase

Indexed keywords

BILE PIGMENT; BILIRUBIN; BILIRUBIN DERIVATIVE; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; BILIRUBIN BLOOD LEVEL; CELL PROTECTION; DNA POLYMORPHISM; DRUG MECHANISM; ENZYME INHIBITION; GENE; GENE ACTIVITY; GENETIC ASSOCIATION; GRAFT REJECTION; HUMAN; KERNICTERUS; LIVER TOXICITY; NEWBORN JAUNDICE; NONHUMAN; PHOTOTHERAPY; UGTA1 GENE;

EID: 84866175674     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00115     Document Type: Article

References (56)

1. Ahlfors, C. E., Amin, S. B., and Parker, A. E. (2009). Unbound bilirubin predicts abnormal automated auditory brainstem response in a diverse newborn population. J. Perinatol. 29, 305-309.
2. Akin, E., Clower, B., Tibbs, R., Tang, J., and Zhang, J. (2002). Bilirubin produces apoptosis in cultured bovine brain endothelial cells. Brain Res. 931, 168-175.
3. Bartlett, M. G., and Gourley, G. R. (2011). Assessment of UGT polymorphisms and neonatal jaundice. Semin. Perinatol. 35, 127-133.
4. Basiglio, C. L., Arriaga, S. M., Pelusa, E, Almara, A. M., Kapitulnik, J., andMottino, A. D. (2010). Complement activation and disease: protective effects of hyperbilirubinaemia. Clin. Sci. 118, 99-113.
5. Bhutani, V. K., Johnson, L. H., and Sivieri, E. M. (1999). Predictive ability of a predischarge hour-specific serum bilirubin for subsequent significant hyperbilirubine-mia in healthy term and near-term newborns. Pediatrics 103, 6-14.
6. Bratlid, D. (1990). How bilirubin gets into the brain. Clin. Perinatol. 17, 449-465.
7. Brites, D., Silva, R., and Brito, A. (1997). Effect of bilirubin on erythrocyte shape and haemolysis, under hypotonic, aggregating or non-aggregating conditions, and correlation with cell age. Scand. J. Clin. Lab. Invest. 57, 337-349.
8. Brito, M. A., Lima, S., Fernandes, A., Falcao, A. S., Silva, R. F., Butter-field, D. A., and Brites, D. (2008). Bilirubin injury to neurons: contribution of oxidative stress and rescue by glycoursodeoxycholic acid. Neurotoxicology 29, 259-269.
9. Calligaris, R., Bellarosa, C., Foti, R., Roncaglia, P., Giraudi, P., Krmac, H., Tiribelli, C., and Gustincich, S. (2009). A transcriptome analysis identifies molecular effectors of unconjugated bilirubin in human neuroblastoma SH-SY5Y cells. BMC Genomics 10, 543. doi:10. 1186/1471-2164-10-543.
10. Chang, E. F., Claus, C. P., Vreman, H. J., Wong, R. J., and Noble-Haeusslein, L. J. (2005). Heme regulation in traumatic brain injury: relevance to the adult and developing brain. J. Cereb. Blood Flow Metab. 25, 1401-1417.
11. Chuniaud, L., Dessante, M., Chantoux, E, Blondeau, J. P., Francon, J., and Trivin, F. (1996). Cytotoxicity of bilirubin for human fibroblasts and rat astrocytes in culture. Effect of the ratio of bilirubin to serum albumin. Clin. Chim. Acta 256, 103-114.
12. de Vries, H. S., Te Morsche, R. H., Jenniskens, K., Peters, W. H., and De Jong, D. J. (2012). A functional polymorphism in UGT1A1 related to hyperbilirubinemia is associated with a decreased risk for Crohn's disease. J. Crohns Colitis. 6, 597-602.
13. 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.
14. Dennery, P. A., Seidman, D. S., and Stevenson, D. K. (2001). Neonatal hyperbilirubinemia. N. Engl. J. Med. 344, 581-590.
15. Dura, P., Salomon, J., Te Morsche, R. H., Roelofs, H. M., Kristins-son, J. O., Wobbes, T., Witteman, B. J., Tan, A. C., Drenth, J. P., and Peters, W. H. (2012). High enzyme activity UGT1A1 or low activity UGT1A8 and UGT2B4 genotypes increase esophageal cancer risk. Int. J. Oncol. 40, 1789-1796.
16. Ekblom, K., Marklund, S. L., Johansson, L., Osterman, P., Hallmans, G., Weinehall, L., Wiklund, P. G., and Hultdin, J. (2010). Bilirubin and UGT1A1*28 are not associated with lower risk for ischemic stroke in a prospective nested case-referent setting. Cerebrovasc. Dis. 30, 590-596.
17. Gennuso, F., Fernetti, C., Tirolo, C., Testa, N., L'Episcopo, F., Caniglia, S., Morale, M. C., Ostrow, J. D., Pascolo, L., Tiribelli, C., and Marchetti, B. (2004). Bilirubin protects astrocytes from its own toxicity by inducing up-regulation and translocation ofmultidrugresistance-associated protein 1 (Mrp1). Proc. Natl. Acad. Sci. U. S. A. 101, 2470-2475.
18. Gibbs, P. E., Tudor, C., and Maines, M. D. (2012). Biliverdin reduc-tase: more than a namesake - the reductase, its Peptide fragments, and biliverdin regulate activity of the three classes of protein kinase C. Front. Pharmacol. 3:31. doi:10.3389/fphar.2012.00031.
19. Granato, A., Gores, G., Vilei, M. T., Tolando, R., Ferraresso, C., and Muraca, M. (2003). Bilirubin inhibits bile acid induced apop-tosis in rat hepatocytes. Gut 52, 1774-1778.
20. Johnston, M. V., and Hoon, A. H. Jr. (2000). Possible mechanisms in infants for selective basal ganglia damage from asphyxia, kernicterus, or mitochondrial encephalopathies. J. Child Neurol. 15, 588-591.
21. Karatzas, A., Giannatou, E., Tzortzis, V., Gravas, S., Aravantinos, E., Mout-zouris, G., Melekos, M., and Tsezou, A. (2010). Genetic polymorphisms in the UDP-glucuronosyltransferase 1A1 (UGT1A1) gene and prostate cancer risk in Caucasian men. Cancer Epidemiol. 34, 345-349.
22. Lerner-Marmarosh, N., Miralem, T., Gibbs, P. E., and Maines, M. D. (2008). Human biliverdin reductase is an ERK activator; hBVR is an ERK nuclear transporter and is required for MAPK signaling. Proc. Natl. Acad. Sci. U. S. A. 105, 6870-6875.
23. Lu, P. H., Chen, M. B., Wu, X. Y., Gu, J. H., Liu, Y., and Gu, R. M. (2011). Genetic polymorphisms of UGT1A7 and cancer risk: evidence from 21 case-control studies. Cancer Invest. 29, 645-654.
24. Maines, M. D. (1988). Heme oxyge-nase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEBJ. 2, 2557-2568.
25. Maines, M. D., Trakshel, G. M., and Kutty, R. K. (1986). Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J. Biol Chem. 261, 411-419.
26. Maisels, M. J., and Newman, T. B. (2007). Kernicterus, the Daubert decision, and evidence-based medicine. Pediatrics 119, 1038; author reply 1038-1039.
27. Mayer, M. (2000). Association of serum bilirubin concentration with risk of coronary artery disease. Clin. Chem. 46, 1723-1727.
28. McDonagh, A. F. (1990). Is bilirubin good for you? Clin. Perinatol. 17, 359-369.
29. Mireles, L. C., Lum, M. A., and Dennery, P. A. (1999). Antioxidant and cyto-toxic effects of bilirubin on neonatal erythrocytes. Pediatr. Res. 45, 355-362.
30. Ngai, K. C., Yeung, C. Y., and Leung, C. S. (2000). Difference in susceptibilities of different cell lines to bilirubin damage. J. Paediatr. Child Health 36, 51-55.
31. Nolting, P. R., Kusters, D. M., Hutten, B. A., and Kastelein, J. J. (2011). Serum bilirubin levels in familial hypercho-lesterolemia: a new risk marker for cardiovascular disease? J. Lipid Res. 52, 1755-1759.
32. Nowis, D., Legat, M., Grzela, T., Niderla, J., Wilczek, E., Wilczynski, G. M., Glodkowska, E., Mrowka, P., Issat, T., Dulak, J., Jozkowicz, A., Was, H., Adamek, M., Wrzosek, A., Nazarewski, S., Makowski, M., Stok-losa, T., Jakobisiak, M., and Golab, J. (2006). Heme oxygenase-1 protects tumor cells against photody-namic therapy-mediated cytotoxic-ity. Oncogene 25, 3365-3374.
33. Oakes, G. H., and Bend, J. R. (2005). Early steps in bilirubin-mediated apoptosis in murine hepatoma (Hepa 1c1c7) cells are characterized by aryl hydrocarbon receptor-independent oxidative stress and activation of the mitochondrial pathway. J. Biochem. Mol. Toxicol. 19, 244-255.
34. Ohrui, T., Higuchi, M., Kanda, A., Mat-sui, T., Sato, E., and Sasaki, H. (2001). A patient with exacerbation of idio-pathic pulmonary fibrosis which was resolved probably due to the coexisting hyperbilirubinemia? Tohoku J. Exp. Med. 193, 245-249.
35. Ollinger, R., Wang, H., Yamashita, K., Wegiel, B., Thomas, M., Margre-iter, R., and Bach, F. H. (2007). Therapeutic applications of bilirubin and biliverdin in transplantation. Antioxid. Redox Signal. 9, 2175-2185.
36. Oren, D. A. (1997). Bilirubin, REM sleep, and phototransduction of environmental time cues. A hypothesis. Chronobiol. Int. 14, 319-329.
37. Rocuts, F., Zhang, X., Yan, J., Yue, Y., Thomas, M., Bach, F. H., Czismadia, E., and Wang, H. (2010). Bilirubin promotes de novo generation of T regulatory cells. Cell Transplant. 19, 443-451.
38. Rodrigues, C. M., Sola, S., and Brites, D. (2002a). Bilirubin induces apoptosis via the mitochondrial pathway in developing rat brain neurons. Hepatology 35, 1186-1195.
39. Rodrigues, C. M., Sola, S., Brito, M. A., Brites, D., and Moura, J. J. (2002b). Bilirubin directly disrupts membrane lipid polarity and fluidity, protein order, and redox status in rat mitochondria. J. Hepatol. 36, 335-341.
40. Rodrigues, C. M., Sola, S., Silva, R. F., and Brites, D. (2002c). Aging confers different sensitivity to the neurotoxic properties of unconjugated bilirubin. Pediatr. Res. 51, 112-118.
41. Rodrigues, C. M., Sola, S., Silva, R., and Brites, D. (2000). Bilirubin and amyloid-beta peptide induce cytochrome c release through mitochondrial membrane permeabiliza-tion. Mol. Med. 6, 936-946.
42. Rosenstein, B. S., Ducore, J. M., and Cummings, S. W (1983). The mechanism of bilirubin-photosensitized DNA strand breakage in human cells exposed to phototherapy light. Mutat. Res. 112, 397-406.
43. Ryter, S. W., and Tyrrell, R. M. (2000). The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28, 289-309.
44. Shapiro, S. M., and Nakamura, H. (2001). Bilirubin and the auditory system. J. Perinatol. 21(Suppl. 1), S52-S55; discussion S59-S62.
45. Stocker, R., McDonagh, A. F., Glazer, A. N., and Ames, B. N. (1990). Antioxidant activities of bile pigments: biliverdin and bilirubin. Meth. Enzy-mol. 186, 301-309.
46. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N., and Ames, B. N. (1987). Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046.
47. Strauss, K. A., Robinson, D. L., Vre-man, H. J., Puffenberger, E. G., Hart, G., and Morton, D. H. (2006). Management of hyperbilirubinemia and prevention of kernicterus in 20 patients with Crigler-Najjar disease. Eur. J. Pediatr. 165, 306-319.
48. Suttner, D. M., and Dennery, P. A. (1999). Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEBJ. 13, 1800-1809.
49. Tang, W., Fu, Y. P., Figueroa, J. D., Malats, N., Garcia-Closas, M., Chat-terjee, N., Kogevinas, M., Baris, D., Thun, M., Hall, J. L., De Vivo, I., Albanes, D., Porter-Gill, P., Purdue, M. P., Burdett, L., Liu, L., Hutchin-son, A., Myers, T., Tardon, A., Serra, C., Carrato, A., Garcia-Closas, R., Lloreta, J., Johnson, A., Schwenn, M., Karagas, M. R., Schned, A., Black, A., Jacobs, E. J., Diver, W R., Gap-stur, S. M., Virtamo, J., Hunter, D. J., Fraumeni, J. F. Jr., Chanock, S. J., Silverman, D. T., Rothman, N., and Prokunina-Olsson, L. (2012). Mapping of the UGT1A locus identifies an uncommon coding variant that affects mRNA expression and protects from bladder cancer. Hum. Mol. Genet. 21, 1918-1930.
50. 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.
51. Van Molle, W., and Libert, C. (2003). Bilirubin release induced by tumor necrosis factor in combination with galactosamine is toxic to mice. Cytokine 23, 94-100.
52. Vitek, L., Jirsa, M., Brodanova, M., Kalab, M., Marecek, Z., Danzig, V., Novotny, L., and Kotal, P. (2002). Gilbert syndrome and ischemic heart disease: a protective effect of elevated bilirubin levels. Atherosclerosis 160, 449-456.
53. Wang, J., Zhou, H. C., Pan, P., Zhang, N., and Li, W Z. (2010). Exogenous biliverdin improves the function of lung grafts from brain dead donors in rats. Transplant. Proc. 42, 1602-1609.
54. Watchko, J. F., and Oski, F. A. (1983). Bilirubin 20 mg/dL = vigintiphobia. Pediatrics 71, 660-663.
55. Wegiel, B., Gallo, D., Csizmadia, E., Roger, T., Kaczmarek, E., Harris, C., Zuckerbraun, B. S., and Otter-bein, 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.
56. Zhang, Z. Y., Bian, L. Q., Kim, S. J., Zhou, C. C., and Choi, Y H. (2012). Inverse relation of total serum bilirubin to coronary artery calcification score detected by multidetector computed tomography in males. Clin. Cardiol. 35, 301-306.