Biliverdin reductase isozymes in metabolism

Trends in Endocrinology and Metabolism

Volumn 26, Issue 4, 2015, Pages 212-220

  O'Brien, Luke ^a   Hosick, Peter A ^b   John, Kezia ^a   Stec, David E ^c   Hinds, Terry D ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b MONTCLAIR STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Bilirubin; Biliverdin reductase; BVRA; BVRB; Diabetes; Heme oxygenase; Obesity

Indexed keywords

BILIRUBIN; BILIVERDIN; BILIVERDIN REDUCTASE ISOZYME; INSULIN; INSULIN RECEPTOR KINASE; INSULIN RECEPTOR SUBSTRATE; OXIDOREDUCTASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; ADIPOCYTOKINE; BILIVERDIN REDUCTASE; ISOENZYME;

BILIRUBIN BLOOD LEVEL; ENZYME STRUCTURE; HUMAN; INFLAMMATION; METABOLIC DISORDER; METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ABDOMINAL OBESITY; ADIPOSE TISSUE; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; BLOOD; CHEMISTRY; ENERGY METABOLISM; ENZYMOLOGY; GENETICS; HYPERTRIGLYCERIDEMIA; IMMUNOLOGY; INSULIN RESISTANCE; PROTEIN CONFORMATION; SECRETION (PROCESS);

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; BILIRUBIN; BINDING SITES; ENERGY METABOLISM; HUMANS; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; ISOENZYMES; MODELS, BIOLOGICAL; OBESITY, ABDOMINAL; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EID: 84933673406     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2015.02.001     Document Type: Review

References (76)

1. Nakamura K., et al. Adipokines: a link between obesity and cardiovascular disease. J. Cardiol. 2014, 63:250-259.
2. Hinds T.D., et al. Increased HO-1 levels ameliorate fatty liver development through a reduction of heme and recruitment of FGF21. Obesity (Silver Spring) 2013, 22:705-712.
3. Vanella L., et al. Increased heme-oxygenase 1 expression in mesenchymal stem cell-derived adipocytes decreases differentiation and lipid accumulation via upregulation of the canonical Wnt signaling cascade. Stem Cell Res. Ther. 2013, 4:28.
4. Li M., et al. Interdiction of the diabetic state in NOD mice by sustained induction of heme oxygenase: possible role of carbon monoxide and bilirubin. Antioxid. Redox Signal. 2007, 9:855-863.
5. Nicolai A., et al. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension 2009, 53:508-515.
6. Ndisang J.F. The heme oxygenase system selectively modulates proteins implicated in metabolism, oxidative stress and inflammation in spontaneously hypertensive rats. Curr. Pharm. Des. 2014, 20:1318-1327.
7. Ndisang J.F., et al. The heme oxygenase system suppresses perirenal visceral adiposity, abates renal inflammation and ameliorates diabetic nephropathy in Zucker diabetic fatty rats. PLoS ONE 2014, 9:e87936.
8. Gibbs P.E., et al. Human biliverdin reductase-based peptides activate and inhibit glucose uptake through direct interaction with the kinase domain of insulin receptor. FASEB J. 2014, 28:2478-2491.
9. Wu Y., et al. Low serum total bilirubin concentrations are associated with increased prevalence of metabolic syndrome in Chinese. J. Diabetes 2011, 3:217-224.
10. Fu G., et al. Molecular modeling to provide insight into the substrate binding and catalytic mechanism of human biliverdin-IXα reductase. J. Phys. Chem. B 2012, 116:9580-9594.
11. Tudor C., et al. Biliverdin reductase is a transporter of haem into the nucleus and is essential for regulation of HO-1 gene expression by haematin. Biochem. J. 2008, 413:405-416.
12. Ahmad Z., et al. Human biliverdin reductase is a leucine zipper-like DNA-binding protein and functions in transcriptional activation of heme oxygenase-1 by oxidative stress. J. Biol. Chem. 2002, 277:9226-9232.
13. Fuchs S.Y., Ronai Z. Ubiquitination and degradation of ATF2 are dimerization dependent. Mol. Cell. Biol. 1999, 19:3289-3298.
14. Kravets A., et al. Biliverdin reductase, a novel regulator for induction of activating transcription factor-2 and heme oxygenase-1. J. Biol. Chem. 2004, 279:19916-19923.
15. van Dam H., et al. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 1995, 14:1798-1811.
16. Srebrow A., et al. The CRE-binding factor ATF-2 facilitates the occupation of the CCAAT box in the fibronectin gene promoter. FEBS Lett. 1993, 327:25-28.
17. Kietzmann T., et al. Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J. Biol. Chem. 2003, 278:17927-17936.
18. Lerner-Marmarosh N., et al. 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. 2008, 105:6870-6875.
19. Gibbs P.E., Maines M.D. Biliverdin inhibits activation of NF-κB: reversal of inhibition by human biliverdin reductase. Int. J. Cancer 2007, 121:2567-2574.
20. Lerner-Marmarosh N., et al. Human biliverdin reductase: a member of the insulin receptor substrate family with serine/threonine/tyrosine kinase activity. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7109-7114.
21. Li W., et al. Activation of Nrf2-antioxidant signaling attenuates NFκB-inflammatory response and elicits apoptosis. Biochem. Pharmacol. 2008, 76:1485-1489.
22. Surh Y.J., et al. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 2008, 74:1526-1539.
23. 2-induced PC12 cell death by a metabolite of sesamin contained in sesame seeds. Bioorg. Med. Chem. 2011, 19:1959-1965.
24. Reddy N.M., et al. Disruption of Nrf2 impairs the resolution of hyperoxia-induced acute lung injury and inflammation in mice. J. Immunol. 2009, 182:7264-7271.
25. Blumenthal S.G., et al. Changes in bilirubins in human prenatal development. Biochem. J. 1980, 186:693-700.
26. Komuro A., et al. Cloning and characterization of the cDNA encoding human biliverdin-IXα reductase. Biochim. Biophys. Acta 1996, 1309:89-99.
27. Pereira P.J., et al. Structure of human biliverdin IXβ reductase, an early fetal bilirubin IXβ producing enzyme. Nat. Struct. Biol. 2001, 8:215-220.
28. Cunningham O., et al. Initial-rate kinetics of the flavin reductase reaction catalysed by human biliverdin-IXβ reductase (BVR-B). Biochem. J. 2000, 345:393-399.
29. Zucker S.D., et al. Unconjugated bilirubin exhibits spontaneous diffusion through model lipid bilayers and native hepatocyte membranes. J. Biol. Chem. 1999, 274:10852-10862.
30. Choi S.H., et al. Relationships between serum total bilirubin levels and metabolic syndrome in Korean adults. Nutr. Metab. Cardiovasc. Dis. 2011, 23:31-37.
31. Torgerson J.S., et al. Are elevated aminotransferases and decreased bilirubin additional characteristics of the metabolic syndrome?. Obes. Res. 1997, 5:105-114.
32. Cüre E., et al. The evaluation of relationship between adiponectin levels and epicardial adipose tissue thickness with low cardiac risk in Gilbert's syndrome: an observational study. Anadolu Kardiyol. Derg. 2013, 13:791-796.
33. Andersson C., et al. Acute effect of weight loss on levels of total bilirubin in obese, cardiovascular high-risk patients: an analysis from the lead-in period of the Sibutramine Cardiovascular Outcome trial. Metab. Clin. Exp. 2009, 58:1109-1115.
34. Dong H., et al. Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinology 2014, 155:818-828.
35. Jais A., et al. Heme oxygenase-1 drives metaflammation and insulin resistance in mouse and man. Cell 2014, 158:25-40.
36. Ito T., et al. Mesobiliverdin IXα enhances rat pancreatic islet yield and function. Front. Pharmacol. 2013, 4:50.
37. Stechschulte L.A., et al. Glucocorticoid receptor beta stimulates Akt1 growth pathway by attenuation of PTEN. J. Biol. Chem. 2014, 289:17885-17894.
38. Kandel E.S., Hay N. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp. Cell Res. 1999, 253:210-229.
39. Pachori A.S., et al. Heme-oxygenase-1-induced protection against hypoxia/reoxygenation is dependent on biliverdin reductase and its interaction with PI3K/Akt pathway. J. Mol. Cell. Cardiol. 2007, 43:580-592.
40. Wegiel B., et al. Cell surface biliverdin reductase mediates biliverdin-induced anti-inflammatory effects via phosphatidylinositol 3-kinase and Akt. J. Biol. Chem. 2009, 284:21369-21378.
41. Zeng R., et al. Biliverdin reductase mediates hypoxia-induced EMT via PI3-kinase and Akt. J. Am. Soc. Nephrol. 2008, 19:380-387.
42. Mo L., et al. PI3K/Akt signaling pathway-induced heme oxygenase-1 upregulation mediates the adaptive cytoprotection of hydrogen peroxide preconditioning against oxidative injury in PC12 cells. Int. J. Mol. Med. 2012, 30:314-320.
43. Butler M., et al. Specific inhibition of PTEN expression reverses hyperglycemia in diabetic mice. Diabetes 2002, 51:1028-1034.
44. Young S.C., et al. Inhibition of biliverdin reductase increases ANG II-dependent superoxide levels in cultured renal tubular epithelial cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R1546-R1553.
45. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004, 75:639-653.
46. Gibbs P.E., et al. Formation of ternary complex of human biliverdin reductase-protein kinase Cδ-ERK2 protein is essential for ERK2-mediated activation of Elk1 protein, nuclear factor-κB, and inducible nitric-oxidase synthase (iNOS). J. Biol. Chem. 2012, 287:1066-1079.
47. Wegiel B., et al. Biliverdin inhibits Toll-like receptor-4 (TLR4) expression through nitric oxide-dependent nuclear translocation of biliverdin reductase. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:18849-18854.
48. Ding B., et al. The coordinated increased expression of biliverdin reductase and heme oxygenase-2 promotes cardiomyocyte survival: a reductase-based peptide counters beta-adrenergic receptor ligand-mediated cardiac dysfunction. FASEB J. 2011, 25:301-313.
49. Hers I., et al. Akt signalling in health and disease. Cell. Signal. 2011, 23:1515-1527.
50. Goswami A., et al. The phosphoinositide 3-kinase/Akt1/Par-4 axis: a cancer-selective therapeutic target. Cancer Res. 2006, 66:2889-2892.
51. De Fea K., Roth R.A. Modulation of insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. J. Biol. Chem. 1997, 272:31400-31406.
52. Lee Y.H., et al. c-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade. J. Biol. Chem. 2003, 278:2896-2902.
53. Backer J.M., et al. Phosphatidylinositol 3'-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 1992, 11:3469-3479.
54. Liu Y.F., et al. Serine phosphorylation proximal to its phosphotyrosine binding domain inhibits insulin receptor substrate 1 function and promotes insulin resistance. Mol. Cell. Biol. 2004, 24:9668-9681.
55. Gual P., et al. Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 2005, 87:99-109.
56. Yin W., et al. Oxidative stress inhibits insulin-like growth factor-I induction of chondrocyte proteoglycan synthesis through differential regulation of phosphatidylinositol 3-kinase-Akt and MEK-ERK MAPK signaling pathways. J. Biol. Chem. 2009, 284:31972-31981.
57. Maines M.D., et al. Human biliverdin reductase, a previously unknown activator of protein kinase C βII. J. Biol. Chem. 2007, 282:8110-8122.
58. Liberman Z., et al. Coordinated phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 and protein kinase C βII in the diabetic fat tissue. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E1169-E1177.
59. Jaishy B., et al. Lipid-induced NOX2 activation inhibits autophagic flux by impairing lysosomal enzyme activity. J. Lipid Res. 2014, Published online December 21, 2014. http://dx.doi.org/10.1194/jlr.M055152.
60. Miralem T., et al. The human biliverdin reductase-based peptide fragments and biliverdin regulate protein kinase Cδ activity: the peptides are inhibitors or substrate for the protein kinase C. J. Biol. Chem. 2012, 287:24698-24712.
61. Lerner-Marmarosh N., et al. Regulation of TNF-α-activated PKC-ζ signaling by the human biliverdin reductase: identification of activating and inhibitory domains of the reductase. FASEB J. 2007, 21:3949-3962.
62. Marino J.S., et al. Suppression of protein kinase C theta contributes to enhanced myogenesis in vitro via IRS1 and ERK1/2 phosphorylation. BMC Cell Biol. 2013, 14:39.
63. Maines M.D. Biliverdin reductase: PKC interaction at the cross-talk of MAPK and PI3K signaling pathways. Antioxid. Redox Signal. 2007, 9:2187-2195.
64. Kapitulnik J., Maines M.D. Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol. Sci. 2009, 30:129-137.
65. Hotamisligil G.S., et al. Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J. Clin. Invest. 1995, 95:2409-2415.
66. Singh A.K., Jiang Y. Lipopolysaccharide (LPS) induced activation of the immune system in control rats and rats chronically exposed to a low level of the organothiophosphate insecticide, acephate. Toxicol. Ind. Health 2003, 19:93-108.
67. Florczyk U., et al. Overexpression of biliverdin reductase enhances resistance to chemotherapeutics. Cancer Lett. 2011, 300:40-47.
68. Melle C., et al. Identification of specific protein markers in microdissected hepatocellular carcinoma. J. Proteome Res. 2007, 6:306-315.
69. Pallua J.D., et al. MALDI-MS tissue imaging identification of biliverdin reductase B overexpression in prostate cancer. J. Proteomics 2013, 91:500-514.
70. Lemberg R., Wyndham R.A. Reduction of biliverdin to bilirubin in tissues. Biochem. J. 1936, 30:1147-1170.
71. Singleton J.W., Laster L. Biliverdin reductase of guinea pig liver. J. Biol. Chem. 1965, 240:4780-4789.
72. Yamaguchi T., et al. Biliverdin-IX alpha reductase and biliverdin-IX beta reductase from human liver. Purification and characterization. J. Biol. Chem. 1994, 269:24343-24348.
73. Saito F., et al. Mapping of the newly identified biliverdin-IX beta reductase gene (BLVRB) to human chromosome 19q13.13→q13.2 by fluorescence in situ hybridization. Cytogenet. Cell Genet. 1995, 71:179-181.
74. Parkar M., et al. Confirmation of the assignment of human biliverdin reductase to chromosome 7. Ann. Hum. Genet. 1984, 48:57-60.
75. Mizukami Y., et al. Nuclear mitogen-activated protein kinase activation by protein kinase Cζ during reoxygenation after ischemic hypoxia. J. Biol. Chem. 2000, 275:19921-19927.
76. Jacobs D., et al. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 1999, 13:163-175.