Erythrocyte nitric oxide synthase as a surrogate marker for mercury-induced vascular damage: The modulatory effects of naringin

Environmental Toxicology

Volumn 29, Issue 11, 2014, Pages 1314-1322

  Harisa, Gamaleldin I ^a,b   Mariee, Amr D ^b,c   Abo Salem, Osama M ^b,d   Attiaa, Sabry M ^a,b  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b Al Azhar University   (Egypt)

^c TAIBAH UNIVERSITY   (Saudi Arabia)

^d TAIF UNIVERSITY   (Saudi Arabia)

Author keywords

Erythrocyte; Mercury; Naringin; Nitric oxide; Oxidative stress

Indexed keywords

ARGININE; BIOCHEMISTRY; BLOOD; CHLORINE COMPOUNDS; FLAVONOIDS; MERCURY (METAL); NITRIC OXIDE; OXIDATIVE STRESS; PEPTIDES; POSITIVE IONS;

ANTI-OXIDANT ACTIVITIES; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ERYTHROCYTE; GLUCOSE-6-PHOSPHATE DEHYDROGENASE; GLUTATHIONE S-TRANSFERASES; NARINGIN; PROTEIN CARBONYL CONTENT; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

MERCURY COMPOUNDS;

ARGININE; AURANTIIN; CARBONYL DERIVATIVE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; MERCURY CHLORIDE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; ANTIOXIDANT; BIOLOGICAL MARKER; FLAVANONE DERIVATIVE; MERCURIC CHLORIDE; NITRIC OXIDE SYNTHASE; POLLUTANT;

ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD TOXICITY; BLOOD VESSEL INJURY; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROCYTE; EXPOSURE; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATIVE STRESS; DRUG EFFECTS; LIPID PEROXIDATION; METABOLISM; OXIDATION REDUCTION REACTION; POLLUTANT; PROTEIN CARBONYLATION; TOXICITY;

ANTIOXIDANTS; ARGININE; BIOLOGICAL MARKERS; ENVIRONMENTAL POLLUTANTS; ERYTHROCYTES; FLAVANONES; GLUCOSEPHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEMOLYSIS; HUMANS; LIPID PEROXIDATION; MERCURIC CHLORIDE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITES; OXIDATION-REDUCTION; PROTEIN CARBONYLATION; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84912042360     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.21862     Document Type: Article

References (57)

1. Ademuyiwa O, Ugbaja RN, Rotimi SO, Abam E, Okediran BS, Dosumu OA, Onunkwor BO.2007. Erythrocyte acetylcholinesterase activity as a surrogate indicator of lead-induced neurotoxicity in occupational lead exposure in Abeokuta, Nigeria. Environ Toxicol Pharmacol 24:183-208.
2. Ajay M, Gilanib AU, Mustafa MR.2003. Effects of flavonoids on vascular smooth muscle of the isolated rat thoracic aorta. Life Sci 74:603-612.
3. Anand P, Stamler JS.2012. Enzymatic mechanisms regulating protein S-nitrosylation: Implications in health and disease. J Mol Med (Berl) 90:233-244.
4. Barakat M, El-Kadi AO, Du Souich P.1997. In vivo, ex vivo, and in vitro effects of L-NAME and L-arginine on the metabolism of theophylline in the rabbit. Drug Metab Dispos 25:191-195.
5. Baskurt OK, Ulker P, Meiselman HJ.2011. Nitric oxide, erythrocytes and exercise. Clin Hemorrheol Micrcirc 49:175-178.
6. Berthe MC, Bernard M, Rasmusen C, Darquy S, Cynober L, Couderc R.2011. Arginine or citrulline associated with a statin stimulates nitric oxide production in bovine aortic endothelial cells. Eur J Pharmacol 670:566-570.
7. Bhattacharya S, Chakroborty P, Patra S, Basu Roy S, Kahn NN, Sinha AK.2001. Purification and properties of insulin-activated nitric oxide synthase from human erythrocyte membranes. Arch Physiol Biochem 109:441-449.
8. Chen LY, Mehta JL.1998. Evidence for the presence of L-arginine-nitric oxide pathway in human red blood cells: Relevance in the effects of red blood cells on platelet function. J Cardiovasc Pharmacol 32:57-61.
9. Chen K, Popel AS.2009. Nitric oxide production pathways in erythrocytes and plasma. Biolrheology 46:107-119.
10. Cheun LH.1966. Glucose-6-phosphate dehydrogenase activity in erythrocytes of experimental animals. J Clin Path 19:614-616.
11. Cutler MJ, Plummer BN, Wan X, Sun QA, Hess D, Liu H, Deschenes I, Rosenbaum DS, Stamler JS, Laurita KR.2012. Aberrant S-nitrosylation mediates calcium-triggered ventricular arrhythmia in the intact heart. Proc Natl Acad Sci USA 109:18186-18191.
12. Durak D, Kalender S, Uzun FG, Demir F, Kalender Y.2010. Mercury chloride-induced oxidative stress in human erythrocytes and the effect of vitamins C and E in vitro. Afr J Biotechnol 9:488-495.
13. Durham HD, Minotti S, Caporicci E.1997. Sensitivity of platelet microtubules to disassembly by methylmercury. J Toxicol Environ Health 48:57-69.
14. Ellman GL.1959. Tissue sulfhydryl groups. Arch Biochem Biophys 82:70-77.
15. Fu JY, Qian LB, Zhu LG, Liang HT, Tan YN, Lu HT, Lu JF, Wang HP, Xia Q.2011. Betulinic acid ameliorates endothelium-dependent relaxation in L-NAME-induced hypertensive rats by reducing oxidative stress. Eur J Pharm Sci 44:385-391.
16. Furieri LB, Galán M, Avendaño MS, García-Redondo AB, Aguado A, Martínez S, Cachofeiro V, Bartolome MV, Alonso MJ, Vassallo DV, Salaices M.2011. Endothelial dysfunction of rat coronary arteries after exposure to low concentrations of mercury is dependent on reactive oxygen species. Br J Pharmacol 162:1819-1831.
17. Gasparini L, Racchi M, Binetti C, Trabucchi M, Solerte SB, Alkon D, Etcheberrigaray R, Gibson G, Paoletti R, Govoni S.1998. Peripheral markers in testing pathophysiological hypothesis and diagnosing Alzheimer's disease. FASEB J 12:17-34.
18. Green L, Wagner D, Glogowski J, Skipper P, Wishnok J, Tannenbaum S.1982. Analysis of nitrate, nitrite and [15N] nitrate in biological fluids. Anal Biochem 126:131-138.
19. Gonzalez FM, Shiva S, Vincent PS, Ringwood LA, Hsu LY, Hon YY, Aletras AH, Cannon ROIII, Gladwin MT, Arai AE.2008. Nitrite anion provides potent cytoprotective and antiapoptotic effects as adjunctive therapy to reperfusion for acute myocardial infarction. Circulation 117:2986-2994.
20. Habig WH, Pabst MJ, Jakoby WB.1974. Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 49:130-139.
21. Harisa GI, Alanazi FK, El-Bassat RA, Malik A, Abdallah GM.2012. Protective effect of pravastatin against mercury induced vascular cells damage: Erythrocytes as surrogate markers. Environ Toxicol Pharmacol 34:428-435.
22. Hess DT, Stamler JS.2012. Regulation by S-nitrosylation of protein post-translational modification. J Biol Chem 287:4411-4418.
23. Iwalokun BA, Efedede BV, Alabisofunde JA, Odualo T, Maqbaqbeola OA, Akinwande AI.2006. Hepatoprotective and antioxidant activities of Vernonia amygdalina on acetaminophen induced hepatic damage in mice. J Med Food 9:524-530.
24. Jeon SM, Park YB, Choi MS.2004. Anti-hypercholesterolaemic property of naringin alters plasma and tissue lipids, cholesterol-regulating enzymes, fecal sterol and tissue morphology in rabbits. Clin Nutr 23:1025-1034.
25. Kang ES, Ford K, Grokulsky G, Chiang TM, Acchiardo SR.2000. Normal circulating adult human red blood cells contain inactive NOS proteins. J Lab Clin Med 135:444-451.
26. Kanno S, Shouji A, Asou K, Ishikawa M.2003. Effects of naringin on hydrogen peroxide-induced cytotoxicity and apoptosis in P388 cells. J Pharmacol Sci 92:166-170.
27. Kiruthiga P, Karutha Pandian S, Pandima Devi K.Silymarin prevents the toxicity induced by benzo(a)pyrene in human erythrocytes by preserving its membrane integrity: An in vitro study. Environ Toxicol (in press).
28. Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O, Scheeren T, Gödecke A, Schrader J, Schulz R, Heusch G, Schaub GA, Bryan NS, Feelisch M, Kelm M.2003. Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radical Biol Med 35:790-796.
29. Kleinbongard P, Schulz R, Rassaf T, Lauer T, Dejam A, Jax T, Kumara I, Gharini P, Kabanova S, Ozüyaman B, Schnürch HG, Gödecke A, Weber AA, Robenek M, Robenek H, Bloch W, Rösen P, Kelm M.2006. Red blood cells express a functional endothelial nitric oxide synthase. Blood 107:2943-2951.
30. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M, Kelm M.2001. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 98:12814-12819.
31. Levine R, Garland D, Oliver C, Amici A, Climent I, Lenz A, Ahn B, Shaltiel S, Stadtman E.1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464-478.
32. Lowry O, Rosebrough N, Farr A, Randall R.1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
33. McKee M, Scavone C, Nathanson JA.1994. Nitric oxide, cGMP, and hormone regulation of active sodium transport. Proc Natl Acad Sci USA 91:12056-12060.
34. Mihara M, Uchiyama M.1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271-278.
35. Minetti M, Agati L, Malorni W.2007. The microenvironment can shift erythrocytes from a friendly to a harmful behavior: Pathogenetic implications for vascular diseases. Cardiovasc Res 75:21-28.
36. Mira L, Fernandez MT, Santos M, Rocha R, Florencio MH, Jennings KR.2002. Interaction of flavonoids with iron and copper ions, a mechanism for their antioxidant activity. Free Radical Res 36:1199-1208.
37. Moss MB, Brunini TM, Soares De Moura R, Novaes Malagris LE, Roberts NB, Ellory JC, Mann GE, Mendes Ribeiro AC.2004. Diminished L-arginine bioavailability in hypertension. Clin Sci (Lond) 107:391-407.
38. Omanwar S, Ravi K, Fahim M.2011. Persistence of EDHF pathway and impairment of the nitric oxide pathway after chronic mercury chloride exposure in rats: Mechanisms of endothelial dysfunction. Hum Exp Toxicol 30:1777-1784.
39. Pari L, Amudha K.2011. Hepatoprotective role of naringin on nickel-induced toxicity in male Wistar rats. Eur J Pharmacol 650:364-370.
40. Pinto RE, Bartley W.1969. The effect of age and sex on glutathione reductase and glutathione peroxidase activities on aerobic glutathione oxidation in rat liver homogenate. Biochem J 112:109-115.
41. Raat NJ, Shiva S, Gladwin MT.2009. Effects of nitrite on modulating ROS generation following ischemia and reperfusion. Adv Drug Delivery Rev 61:339-350.
42. Renugadevi J, Prabu SM.2009. Naringenin protects against cadmium-induced oxidative renal dysfunction in rats. Toxicology 256:128-134.
43. Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG.1973. Selenium: Biochemical role as a component of glutathione peroxidase. Science 179:588-590.
44. Salonen JT, Seppanen K, Nyyssonen K.1995. Intake of mercury from fish, lipid peroxidation, and the risk of myocardial infarction and coronary, cardiovascular, and any death in eastern Finnish men. Circulation 91:645-655.
45. Saravanakumar M, Raja B.2011. Veratric acid, a phenolic acid attenuates blood pressure and oxidative stress in L-NAME induced hypertensive rats. Eur J Pharmacol 671:87-94.
46. Schmitt CA, Dirsch VM.2009. Modulation of endothelial nitric oxide by plant-derived products. Nitric Oxide 21:77-91.
47. Stohs SJ, Bagchi D.1995. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol Med 18:321-336.
48. Stuehr DJ.1999. Mammalian nitric oxide synthases. Biochim Biophys Acta 1411:217-230.
49. Tentori L, Salvati AM.1981. Hemoglobinometry in human blood. Methods Enzymol 76:707-715.
50. Tousoulis D, Kampoli AM, Tentolouris C, Papageorgiou N, Stefanadis C.2012. The role of nitric oxide on endothelial function. Curr Vasc Pharmacol 10:4-18.
51. Tripathi P, Chandra M, Misra MK.2009. Oral administration of L-arginine in patients with angina or following myocardial infarction may be protective by increasing plasma superoxide dismutase and total thiols with reduction in serum cholesterol and xanthine oxidase. Oxid Med Cell Longev 2:231-237.
52. Tsai HJ, Shang HF, Yeh CL, Yeh SL.2002. Effects of arginine supplementation on antioxidant enzyme activity and macrophage response in burned mice. Burns 28:258-263.
53. Ulker P, Sati L, Celik-Ozenci C, Meiselman HJ, Baskurt OK.2009. Mechanical stimulation of nitric oxide synthesizing mechanisms in erythrocytes. Biorheology 46:121-132.
54. Vallence P, Chan N.2001. Endothelial function and nitric oxide: Clinical relevance. Heart 85:342-350.
55. Van Acker FA, Schouten O, Haenen GR, van der Vijgh WJ, Bast A.2000. Flavonoids can replace alpha-tocopherol as an antioxidant. FEBS Lett 473:145-148.
56. Virtanen JK, Rissanen TH, Voutilainen S, Tuomainen TP.2007. Mercury as a risk factor for cardiovascular diseases. J Nutr Biochem 18:75-85.
57. White CR, Parks DA, Patel RP, Shelton J, Tarpey MM, Freeman BA, Darley-Usmar VM.2004. L-Arginine inhibits xanthine oxidase-dependent endothelial dysfunction in hypercholesterolemia. FEBS Lett 561:94-98.