Antioxidant activity of liver growth factor, a bilirubin covalently bound to albumin

Free Radical Biology and Medicine

Volumn 46, Issue 5, 2009, Pages 656-662

  Condezo Hoyos, Luis ^a   Abderrahim, Fatima ^a   Conde, M Victoria ^a   Susín, Cristina ^a   Díaz Gil, Juan J ^b   González, M Carmen ^a   Arribas, Silvia M ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

Antioxidant; Arteries; Free radicals; Liver growth factor; Nitric oxide; Reactive oxygen species

Indexed keywords

ALBUMIN; ANTIOXIDANT; BILIRUBIN; FREE RADICAL; LIVER GROWTH FACTOR; SUPEROXIDE DISMUTASE; TIRON; TROLOX C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; COVALENT BOND; DEGRADATION; DRUG MECHANISM; IN VITRO STUDY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIOXIDANTS; BENZOTHIAZOLES; BILIRUBIN; BLOOD PRESSURE DETERMINATION; CAROTID ARTERIES; CHROMANS; ENDOTHELIAL CELLS; FIBROSIS; HYDROXYL RADICAL; HYPERTENSION; MALE; NITRIC OXIDE; OXIDATIVE STRESS; PEROXIDES; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN; SERUM ALBUMIN, BOVINE; SULFONIC ACIDS;

RATTUS;

EID: 59249109048     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.12.002     Document Type: Article

References (56)

1. Genestra M. Oxy radicals, redox-sensitive signalling cascades and antioxidants. Cell. Signalling 19 (2007) 1807-1819
2. Valko M., Leibfritz D., Moncol J., Cronin M.T.D., Mazur M., and Telser J. Free radicals and antioxidant in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007) 44-84
3. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2000) 47-95
4. Cai H., and Harrison D.G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87 (2000) 840-844
5. Harrison D.G., Gongora M.C., Guzik T.J., and Widder J. Oxidative stress and hypertension. J. Am. Soc. Hypertens. 1 (2007) 30-44
6. Rush J.W., and Ford R.J. Nitric oxide, oxidative stress and vascular endothelium in health and hypertension. Clin. Hemorheol. Microcirc. 37 (2007) 185-192
7. Graham I., Atar D., Borch-Jhonsen K., Boysen G., Burell G., Cifkova R., Dallongeville J., De Backer G., Ebrahim S., Gjelsvik B., Herrmann-Lingen C., Hoes A., Humphries S., Knapton M., Perk J., Priori S.G., Pyorala K., Reiner Z., Ruilope L., Sans-Menendez S., Op Reimer W., Weissberg P., Wood D., Yarnell J., and Zamorano J.L. European guidelines on cardiovascular disease prevention in clinical practice: executive summary. Atherosclerosis 194 (2007) 1-45
8. Paravicini T.M., and Touyz R.M. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care Suppl. 2 (2008) S170-180
9. Mayer M. Association of serum bilirubin concentration with risk of coronary artery disease. Clin. Chem. 46 (2000) 1723-1727
10. Perlstein T.S., Pande R.L., Beckman J.A., and Creager M.A. 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 (2008) 166-172
11. Neuzil J., and Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J. Biol. Chem. 269 (1994) 16712-16719
12. Stocker R. Antioxidant activities of bile pigments. Antioxid. Redox Signaling 6 (2004) 841-849
13. MacLean P.D., Drake E.C., Ross L., and Barclay C. Bilirubin as an antioxidant in micelles and lipid bilayers: its contribution to the total antioxidant capacity of human blood plasma. Free Radic. Biol. Med. 43 (2007) 600-609
14. Yoshida H., Inagaki T., Hiranot M., and Sugimoto T. Analyses of azopigments obtained from the delta fraction of bilirubin from mammalian plasma (mammalian biliprotein). Biochem. J. 248 (1987) 79-84
15. Stocker R., Glazer A.N., and Ames B.N. Antioxidant activity of albumin-bound bilirubin. Proc. Natl. Acad. Sci. USA 84 (1987) 5918-5922
16. Chepelev L.L., Beshara C.S., MacLean P.D., Hatfield G.L., Rand A.A., Thompson A., Wright J.M., and Barclay L.R.C. Polypyrroles as antioxidants: kinetic studies on reactions of bilirubin and biliverdin dimethyl esters and synthetic model compounds with peroxyl radicals in solution. Chemical calculations on selected typical structures. J. Org. Chem. 71 (2006) 22-30
17. Wu T.W., Wu J., Li R.K., Mickle D., and Carey D. Albumin-bound bilirubins protect human ventricular myocytes against oxyradical damage. Biochem. Cell Biol. 69 (1991) 638-688
18. Wu T.W., Carey D., Wu J., and Sugiyama H. The cytoprotective effects of bilirubin and biliverdin on rat hepatocytes and human erythrocytes and the impact of albumin. Biochem. Cell Biol. 69 (1991) 828-834
19. Díaz-Gil J.J., Gavilanes J.G., Sánchez G., García-Canero R., García-Segura J.M., and Santamaría L. Identification of a liver growth factor as an albumin-bilirubin complex. Biochem. J. 234 (1987) 443-448
20. Díaz-Gil J.J., Sánchez G., Trilla C., and Escartín P. Identification of biliprotein as a liver growth factor. Hepatology 8 (1988) 484-486
21. Díaz-Gil J.J., Muñoz J., Albillos A., Rúa C., Machín C., García-Cañero R., Cereceda R.M., Guijarro M.C., Trilla C., and Escartín P. Improvement in liver fibrosis, functionality and hemodynamics in CCI4-cirrhotic rats after injection of the liver growth factor. J. Hepatol. 30 (1999) 1065-1072
22. Reimers D., Herranz A.S., Díaz-Gil J.J., Lobo M.V., Paíno C.L., Alonso R., Asensio M.J., Gonzalo-Gobernado R., and Bazán E. Intrastriatal infusion of liver growth factor stimulates dopamine terminal sprouting and partially restores motor function in 6-hydroxydopamine-lesioned rats. J. Histochem. Cytochem. 54 (2006) 457-465
23. Somoza B., Abderrahim F., González J.M., Conde M.V., Arribas S.M., Starcher B., Regadera J., Fernández-Alonso M.S., Díaz-Gil J.J., and González M.C. Short-term treatment of spontaneously hypertensive rats with liver growth factor reduces carotid artery fibrosis, improves vascular function, and lowers blood pressure. Cardiovasc. Res. 69 (2006) 764-771
24. Díaz-Gil J.J., Sánchez G., Santamaría L., Trilla C., Esteban P., and Escartín P. Liver DNA synthesis promoter activity detected in human plasma from subjects with hepatitis. Hepatology 6 (1986) 658-661
25. Díaz-Gil J.J., Rúa C., Machín C., Cereceda R.M., García-Canero R., and de Foronda M. Hepatic growth induced by injection of the liver growth factor into normal rats. Growth Regul. 4 (1994) 113-122
26. Re R., Pellegrini N., Proteggente A., Pannala A., Yand M., and Rice-Evans C. Antioxidant activity applying and improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26 (1999) 1231-1237
27. Davalos A., Gómez-Cordovés C., and Bartolomé B. Extending applicability of oxygen radical absorbance capacity (ORAC-fluorescein) assay. J. Agric. Food Chem. 52 (2004) 48-54
28. Halliwell B., Gutteridge J.M.C., and Aruoma O.I. The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 165 (1987) 210-215
29. Cheng Z., Yan G., Li Y., and Chang W. Determination of antioxidant activity of phenolic antioxidants in a Fenton-type reaction system by chemiluminescence assay. Anal. Bioanal. Chem. 375 (2003) 376-380
30. Conde M.V., Marín J., Fernandez-Criado C., and Balfagón G. Regulation of beta-adrenoceptor-mediated relaxation of the rat aorta is modulated by endogenous ovarian hormones. Clin. Sci. (London) 98 (2000) 381-387
31. Marklund S., and Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47 (1974) 469-474
32. Halliwell B., and Gutteridge J.M.C. The antioxidants of human extracellular fluids. Arch. Biochem. Biophys. 280 (1990) 1-8
33. Roche M., Rondeau P., Singh N.R., Tarnus E., and Bourdon E. The antioxidant properties of serum albumin. FEBS Lett. 582 (2008) 1783-1787
34. Bompadre S., Leone L., Politi A., and Batino M. Improved FIA-ABTS method for antioxidant capacity determination in different biological samples. Free Radic. Res. 38 (2004) 831-838
35. Arts M.J., Haenen G.R., Voss H.P., and Bast A. Antioxidant capacity of reaction products limits the applicability of the trolox equivalent antioxidant capacity (TEAC) assay. Food Chem. Toxicol. 42 (2004) 45-49
36. {radical dot}+) with amino acid: kinetics and mechanism. Can. J. Chem. 78 (2000) 1052-1059
37. Laguerre M., Lecomte J., and Villeneuve P. Evaluation of the ability of antioxidants to counteract lipid oxidation: existing methods, new trends and challenges. Prog. Lipid Res. 46 (2007) 244-282
38. Huìe R.E., and Neta P. Chemistry of Reactive Oxygen Species: Reactive Oxygen Species in Biological Systems. In: Gilbert D.L., and Colton C.A. (Eds). An Interdisciplinary Approach (1999), Kluwer Academic, New York 33-63
39. Deshmukh A.J., Patel N.J., and Patel R.J. Hydroxyl radical mediates the augmented angiotensin II responses in thoracic aorta of spontaneously hypertensive rats. Pharmacology 79 (2007) 122-128
40. Hamilton C. Nitric oxide, oxidative stress and hypertension: a complex equation. J. Hypertens 20 (2002) 1055-1056
41. Taniyama Y., and Griendling K.K. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42 (2003) 1075-1081
42. Hogg N., and Kalyanaraman B. Nitric oxide and lipid peroxidation. Biochim. Biophys. Acta 1411 (1999) 378-384
43. Rees D.D., Palmer R.M., Schulz R., Hodson H.F., and Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br. J. Pharmacol. 101 (1990) 746-752
44. Reyes-Toso C.F., Linares L.M., Witriw A., Vázquez M.B., Ricci C.R., and Cardinali D.P. Antioxidants restore aortic ring relaxation in pancreatectomized rats. Life Sci. 81 (2007) 1467-1472
45. Vuong T.D., de Kimpe S., de Roos R., Rabelink T.J., Koomans H.A., and Joles J.A. Albumin restores lysophosphatidylcholine-induced inhibition of vasodilation in rat aorta. Kidney Int. 60 (2001) 1088-1096
46. Pflueger A., Croatt A.J., Peterson T.E., Smith L.A., d'Uscio L.V., Katusic Z.S., and Nath K.A. The hyperbilirubinemic Gunn rat is resistant to the pressor effects of angiotensin II. Am. J. Physiol. Renal Physiol. 288 (2005) F552-F558
47. Online at http://www.rcsb.org/pdb/home/home.dol, October 15, 2008.
48. Dufour C., Loonis M., and Dangles O. Inhibition of the peroxidation of linoleic acid by the flavonoid quercetin within their complex with human serum albumin. Free Radic. Biol. Med. 43 (2007) 241-252
49. Carter D.C., and Ho J.X. Structure of serum albumin. Adv. Protein Chem. 44 (1994) 153-203
50. Schnitzer J.E., Sung A., Horvat R., and Bravo J. Preferential interaction of albumin-binding proteins, gp30 and gp18, with conformationally modified albumins. J. Biol. Chem. 267 (1992) 24544-24553
51. Pain R. Determining the CD spectrum of a protein. Current Protocols in Protein Science, Chap. 7, Unit 7.6. Wiles Interscience City: Hoboken, NJ. (2005)
52. Kanakis C.D., Tarantilis P.A., Tajmir-Riahi H.A., and Polissiou M.G. Crocetin, dimethylcrocetin, and safranal bind human serum albumin: stability and antioxidative properties. J. Agric. Food Chem. 55 (2007) 970-977
53. Mancuso C., Bonsignore A., Capone C., Di stasio E., and Pani G. Albumin-bound bilirubin interacts with nitric oxide by a redox mechanism. Antioxid. Redox Signaling 8 (2006) 487-493
54. Weiss J.S., Gautam A., Lauff J.J., Sundberg M.W., Jatlow P., Boyer J.L., and Seligson D. The clinical importance of a protein-bound fraction of serum bilirubin in patients with hyperbilirubinemia. N. Engl. J. Med. 309 (1983) 147-150
55. Trauner M., Fickert P., and Stauber R.E. Inflammation-induced cholestasis. J. Gastroenterol. Hepatol. 14 (1999) 946-959
56. -/- mice and the Gunn rat. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H333-342