Astaxanthin ameliorates the redox imbalance in lymphocytes of experimental diabetic rats

Chemico-Biological Interactions

Volumn 186, Issue 3, 2010, Pages 306-315

  Otton, Rosemari ^a   Marin, Douglas Popp ^a   Bolin, Anaysa Paola ^a   Santos, Rita de Cássia Macedo dos ^a   Polotow, Tatiana Geraldo ^a   Sampaio, Sandra Coccuzzo ^b   de Barros, Marcelo Paes ^a  

^a UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

Apoptosis; Astaxanthin; Carotenoid; Diabetes; Lymphocyte; Oxidative stress

Indexed keywords

ALLOXAN; ANTIOXIDANT; ASTAXANTHIN; CALCIUM ION; CATALASE; CHOLESTEROL; GLUCOSE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; LIPID; NITRIC OXIDE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; DRUG MECHANISM; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; IMMUNOCOMPETENT CELL; IMMUNOPATHOLOGY; LIPID OXIDATION; LYMPHOCYTE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MALE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN ANALYSIS; RAT; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; ANTIOXIDANTS; CALCIUM; CELL PROLIFERATION; DIABETES MELLITUS; HYDROGEN PEROXIDE; LYMPHOCYTES; MALE; NITRIC OXIDE; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; XANTHOPHYLLS;

DECAPODA (CRUSTACEA); RATTUS; RATTUS NORVEGICUS;

EID: 77954384760     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2010.05.011     Document Type: Article

References (47)

1. Stephens J.W., Khanolkar M.P., Bain S.C. The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis 2009, 202:321-329.
2. Marhoffer W., Stein M., Maeser E.F., Federlin K. Impairment of polymorphonuclear leukocyte function and metabolic control of diabetes. Diabetes Care 1992, 15:256-260.
3. Dolkart R.E., Halpern B., Perlman J. Comparison of antibody responses in normal and alloxan diabetic mice. Diabetes 1971, 20:162-167.
4. Newsholme P., Haber E.P., Hirabara S.M., Rebelato E.L., Procopio J., Morgan D., Oliveira-Emilio H.C., Carpinelli A.R., Curi R. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J. Physiol. 2007, 583:9-24.
5. Otton R., Carvalho C.R., Mendonca J.R., Curi R. Low proliferation capacity of lymphocytes from alloxan-diabetic rats: involvement of high glucose and tyrosine phosphorylation of Shc and IRS-1. Life Sci. 2002, 71:2759-2771.
6. Otton R., Soriano F.G., Verlengia R., Curi R. Diabetes induces apoptosis in lymphocytes. J. Endocrinol. 2004, 182:145-156.
7. Arnlov J., Zethelius B., Riserus U., Basu S., Berne C., Vessby B., Alfthan G., Helmersson J. Serum and dietary beta-carotene and alpha-tocopherol and incidence of type 2 diabetes mellitus in a community-based study of Swedish men: report from the Uppsala Longitudinal Study of Adult Men (ULSAM) study. Diabetologia 2009, 52:97-105.
8. Sugiura M., Nakamura M., Ikoma Y., Yano M., Ogawa K., Matsumoto H., Kato M., Ohshima M., Nagao A. Serum carotenoid concentrations are inversely associated with serum aminotransferases in hyperglycemic subjects. Diabetes Res. Clin. Pract. 2006, 71:82-91.
9. 2+-loaded liposomes: scavenging oxyradicals or changing membrane permeability?. Biochem. Biophys. Res. Commun. 2001, 288:225-232.
10. Chew B.P. A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res. 1999, 19:1849-1854.
11. Pashkow F.J., Watumull D.G., Campbell C.L. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am. J. Cardiol. 2008, 101:58D-68D.
12. Guerin M., Huntley M.E., Olaizola M. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 2003, 21:210-216.
13. Jyonouchi H., Hill R.J., Tomita Y., Good R.A. Studies of immunomodulating actions of carotenoids. I. Effects of beta-carotene and astaxanthin on murine lymphocyte functions and cell surface marker expression in in vitro culture system. Nutr. Cancer 1991, 16:93-105.
14. Jyonouchi H., Zhang L., Tomita Y. Studies of immunomodulating actions of carotenoids. II. Astaxanthin enhances in vitro antibody production to T-dependent antigens without facilitating polyclonal B-cell activation. Nutr. Cancer 1993, 19:269-280.
15. Jyonouchi H., Sun S., Gross M. Effect of carotenoids on in vitro immunoglobulin production by human peripheral blood mononuclear cells: astaxanthin, a carotenoid without vitamin A activity, enhances in vitro immunoglobulin production in response to a T-dependent stimulant and antigen. Nutr. Cancer 1995, 23:171-183.
16. Jyonouchi H., Zhang L., Gross M., Tomita Y. Immunomodulating actions of carotenoids: enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutr. Cancer 1994, 21:47-58.
17. Cancelas J., Prieto P.G., Villanueva-Peñacarrillo M.L., Valverde I., Malaisse W.J. Effects of an olive oil-enriched diet on glucagon-like peptide 1 release and intestinal content, plasma insulin concentration, glucose tolerance and pancreatic insulin content in an animal model of type 2 diabetes. Horm. Metab. Res. 2006, 38:98-105.
18. Otton R., da Silva D.O., Campoio T.R., Silveira L.R., de Souza M.O., Hatanaka E., Curi R. Non-esterified fatty acids and human lymphocyte death: a mechanism that involves calcium release and oxidative stress. J. Endocrinol. 2007, 195:133-143.
19. McGowan M.W., Artiss J.D., Strandbergh D.R., Zak B. A peroxidase-coupled method for the colorimetric determination of serum triglycerides. Clin. Chem. 1983, 29:538-542.
20. Trinder P. Determination of blood glucose using 4-amino phenazone as oxygen acceptor. J. Clin. Pathol. 1969, 22:246.
21. Murphy M.E., Kehrer J.P. Oxidation state of tissue thiol groups and content of protein carbonyl groups in chickens with inherited muscular dystrophy. Biochem. J. 1989, 260:359-364.
22. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994, 233:346-357.
23. Fraga C.G., Leibovitz B.E., Tappel A.L. Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic. Biol. Med. 1988, 4:155-161.
24. Ding A.H., Nathan C.F., Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 1988, 141:2407-2412.
25. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
26. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
27. Mannervik B. Glutathione peroxidase. Methods Enzymol. 1985, 113:490-495.
28. Ewing J.F., Janero D.R. Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal. Biochem. 1995, 232:243-248.
29. Duc H.T., Nakagawa S., Rucay P., Righenzi S., Voisin G.A. Differential modulation of the in vitro lymphocyte activation pathways by soluble and solubilized placental substances. Am. J. Reprod. Immunol. 1990, 24:73-79.
30. Laurindo F.R., Fernandes D.C., Santos C.X. Assessment of superoxide production and NADPH oxidase activity by HPLC analysis of dihydroethidium oxidation products. Methods Enzymol. 2008, 441:237-260.
31. Pick E., Mizel D. Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. J. Immunol. Methods 1981, 46:211-226.
32. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
33. Petri D., Lundebye A.K. Tissue distribution of astaxanthin in rats following exposure to graded levels in the feed. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 145:202-209.
34. Mercke-Odeberg J., Lignell A., Pettersson A., Hoglund P. Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur. J. Pharm. Sci. 2003, 19:299-304.
35. Brunham L.R., Kruit J.K., Hayden M.R., Verchere C.B. Cholesterol in beta-cell dysfunction: the emerging connection between HDL cholesterol and type 2 diabetes. Curr. Diab. Rep. 2010, 10:55-60.
36. Naguib Y.M. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 2000, 48:1150-1154.
37. Aoi W., Naito Y., Takanami Y., Ishii T., Kawai Y., Akagiri S., Kato Y., Osawa T., Yoshikawa T. Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem. Biophys. Res. Commun. 2008, 366:892-897.
38. Sies H. Glutathione and its role in cellular functions. Free Radic. Biol. Med. 1999, 27:916-921.
39. 2+ homeostasis in type 2 diabetes mellitus. Int. J. Exp. Diabetes Res. 2001, 1:275-287.
40. Krinsky N.I., Yeum K.J. Carotenoid-radical interactions. Biochem. Biophys. Res. Commun. 2003, 305:754-760.
41. Kobayashi N., Schmid-Schönbein G.W. Intrinsic disturbance of cellular redox balance enhances blood lymphocyte apoptosis in the spontaneously hypertensive rat. Free Radic. Biol. Med. 2006, 41:484-492.
42. Mano C.M., Barros M.P., Faria P.A., Prieto T., Dyszy F.H., Nascimento O.R., Nantes I.L., Bechara E.J.H. Superoxide radical protects liposome-contained cytochrome c against oxidative damage promoted by peroxynitrite and free radicals. Free Radic. Biol. Med. 2009, 47:841-849.
43. Heckford S.E., Gelmann E.P., Agnor C.L., Jacobson S., Zinn S., Matis L.A Distinct signals are required for proliferation and lymphokine gene expression in murine T cell clones. J. Immunol. 1986, 137:3652-3663.
44. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 2002, 3:1129-1134.
45. Kono K., Salazar-Onfray F., Petersson M., Hansson J., Masucci G., Wasserman K., Nakazawa T., Anderson P., Kiessling R. Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing zeta molecules and inhibits tumor-specific T cell-and natural killer cell-mediated cytotoxicity. Eur. J. Immunol. 1996, 26:1308-1313.
46. Chaudhri G., Hunt N.H., Clark I.A., Ceredig R. Antioxidants inhibit proliferation and cell surface expression of receptors for interleukin-2 and transferrin in T lymphocytes stimulated with phorbol myristate acetate and ionomycin. Cell Immunol. 1998, 115:204-213.
47. Miller L.J., Marx J., Apoptosis Science 1998, 281:1301.