Mercury Exposure and Endothelial Dysfunction: An Interplay between Nitric Oxide and Oxidative Stress

International Journal of Toxicology

Volumn 34, Issue 4, 2015, Pages 300-307

  Omanwar, Swati ^a   Fahim, M ^b  

^a INDIRA GANDHI NATIONAL OPEN UNIVERSITY   (India)

^b HAMDARD UNIVERSITY   (India)

Author keywords

cardiovascular disease; endothelium; mercury; NO; oxidative stress

Indexed keywords

MERCURY; NITRIC OXIDE;

ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; ENDOTHELIAL DYSFUNCTION; HOMEOSTASIS; HUMAN; ISCHEMIC HEART DISEASE; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENDOTHELIUM CELL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MERCURY; NITRIC OXIDE; OXIDATIVE STRESS;

EID: 84938677019     PISSN: 10915818     EISSN: 1092874X     Source Type: Journal    
DOI: 10.1177/1091581815589766     Document Type: Article

References (90)

1. Salonen JT, Seppänen K, Nyyssönen K,. Intake of mercury from fish, lipid peroxidation, and the risk of myocardial infarction and coronary, cardiovascular, and any death in eastern Finnish men. Circulation. 1995; 91 (3): 645-655.
2. Virtanen JK, Voutilainen S, Rissanen TH,. Mercury, fish oils, and risk of acute coronary events and cardiovascular disease, coronary heart disease, and all-cause mortality in men in eastern Finland. Arterioscler Thromb Vasc Biol. 2005; 25 (1): 228-233.
3. Houston MC,. The role of mercury and cadmium heavy metals in vascular disease, hypertension, coronary heart disease, and myocardial infarction. Altern Ther Health Med. 2007; 13 (2): S128-S133.
4. Clarkson TW, Magos L, Myers GJ,. The toxicology of mercury-current exposures and clinical manifestations. N Engl J Med. 2003; 349 (18): 1731-1737.
5. Sarkar NN, Bhan A,. Mercury in the environment: effect on health and reproduction. Rev Environ Health. 2005; 20 (1): 39-56.
6. Miller DM, Woods JS,. Urinary porphyrins as biological indicators of oxidative stress in the kidney. Interaction of mercury and cephaloridine. Biochem Pharmacol. 1993; 46 (12): 2235-2241.
7. Huang YL, Cheng SL, Lin TH,. Lipid peroxidation in rats administrated with mercuric chloride. Biol Trace Elem Res. 1996; 52 (2): 193-206.
8. Mahboob M, Shireen KF, Atkinson A, Khan AT,. Lipid peroxidation and antioxidant enzyme activity in different organs of mice exposed to low level of mercury. J Environ Sci Health B. 2001; 36 (5): 687-697.
9. Reus IS, Bando I, Andrés D, Cascales M,. Relationship between expression of HSP70 and metallothionein and oxidative stress during mercury chloride induced acute liver injury in rats. J Biochem Mol Toxicol. 2003; 17 (3): 161-168.
10. Chen C, Qu L, Li B,. Increased oxidative DNA damage, as assessed by urinary 8-hydroxy-2′-deoxyguanosine concentrations, and serum redox status in persons exposed to mercury. Clin Chem. 2005; 51 (4): 759-767.
11. Omanwar S, Ravi K, Fahim M,. 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. 2011; 30 (11): 1777-1784.
12. Golpon HA, Püchner A, Barth P, Welte T, Wichert PV, Feddersen CO,. Nitric oxide-dependent vasorelaxation and endothelial cell damage caused by mercury chloride. Toxicology. 2003; 192 (2-3): 179-188.
13. da Cunha V, Souza HP, Rossoni LV, França AS, Vassallo DV,. Effects of mercury on the isolated perfused rat tail vascular bed are endothelium-dependent. Arch Environ Contam Toxicol. 2000; 39 (1): 124-130.
14. Wiggers GA, Peçanha FM, Briones AM,. Low mercury concentrations cause oxidative stress and endothelial dysfunction in conductance and resistance arteries. Am J Physiol Heart Circ Physiol. 2008; 295 (3): 33-43.
15. Jalili HA, Abbasi AH,. Poisoning by ethyl mercury toluene sulphonanilide. Br J Ind Med. 1961; 18: 303-308.
16. Eto K,. Minamata disease. Neuropathology. 2000; 20 (suppl): S14-S19.
17. Garcia Gomez M, Boffetta P, Caballero K, Español S, Gómez Quintana J,. Cardiovascular mortality in mercury miners. Med Clin (Barc). 2007; 128 (20): 766-771.
18. Choi AL, Weihe P, Budtz-Jorgensen E,. Methylmercury exposure and adverse cardiovascular effects in Faroese whaling men. Environ Health Perspect. 2009; 117 (3): 367-372.
19. Trakhtenberg IM,. Chronic effects of mercury on organisms: the micromercurialism phenomenon on mercury handlers. 1974; Chap. VI: 109-34,. DHEW Publ. No. (NIH).
20. Snodgrass W, Sullivan JB, Rumack BH,. Mercury poisoning from home gold ore processing: use of penicillamine and dimercaprol. JAMA. 1981; 246 (17): 1929-1931.
21. Barregard L, Sallsten G, Jarvholm B,. Mortality and cancer incidence in chloralkali workers exposed to inorganic mercury. Br J Ind Med. 1990; 47 (2): 99-104.
22. Boffetta P, Sallsten G, Garcia-Gomez M,. Mortality from cardiovascular disease and exposure to inorganic mercury. Occup Environ Med. 2001; 58 (7): 461-466.
23. Siblerud RL,. The relationship between mercury from dental amalgam and the cardiovascular system. Sci Total Environ. 1990; 99 (1-2): 23-36.
24. Fagala GE, Wigg CL,. Psychiatric manifestations of mercury poisoning. J Am Acad Child Adolesc Psychiatry. 1992; 31 (2): 306-311.
25. Goodrich JM, Wang Y, Gillespie B, Werner R, Franzblau A, Basu N,. Glutathione enzyme and selenoprotein polymorphisms associate with mercury biomarker levels in Michigan dental professionals. Toxicol Appl Pharmacol. 2011; 257 (2): 301-308.
26. Valera B, Dewailly E, Poirier P,. Association between methylmercury and cardiovascular risk factors in a native population of Quebec (Canada): a retrospective evaluation. Environ Res. 2013; 120: 102-108.
27. Kim DS, Lee EH, Yu SD, Cha JH, Ahn SC,. Heavy metal as risk factor of cardiovascular disease-an analysis of blood lead and urinary mercury. J Prev Med Pub Health. 2005; 38 (4): 401-407.
28. Guallar E, Sanz-Gallardo MI, Veer PV,. Mercury, fish oils, and the risk of myocardial infarction. N Engl J Med. 2002; 347 (22): 1747-1754.
29. Chan HM, Egeland GM,. Fish consumption, mercury exposure, and heart disease. Nutr Rev. 2004; 62 (2): 68-72.
30. Landmark K, Aursnes I,. Mercury, fish, fish oil and the risk of cardiovascular disease. Tidsskr Nor. Laegeforen. 2004; 124 (2): 198-200.
31. Hong D, Cho SH, Park SJ, Kim SY, Park SB,. Hair mercury level in smokers and its influence on blood pressure and lipid metabolism. Environ Toxicol Pharmacol. 2013; 36 (1): 103-107.
32. Valera B, Dewailly E, Poirier P, Counil E, Suhas E,. Influence of mercury exposure on blood pressure, resting heart rate and heart rate variability in French Polynesians: a cross-sectional study. Environ Health. 2011; 10: 99.
33. Eom SY, Choi SH, Ahn SJ,. Reference levels of blood mercury and association with metabolic syndrome in Korean adults. Int Arch Occup Environ Health. 2014; 87 (5): 501-513.
34. Virtanen JK, Nyantika AN, Kauhanen J, Voutilainen S, Tuomainen TP,. Serum long-chain n-3 polyunsaturated fatty acids, methylmercury and blood pressure in an older population. Hypertens Res. 2012; 35 (10): 1000-1004.
35. Kalish BT, Rifas-Shiman SL, Wright RO,. Associations of prenatal maternal blood mercury concentrations with early and mid-childhood blood pressure: a prospective study. Environ Res. 2014; 133: 327-333.
36. Périard D, Beqiraj B, Hayoz D,. Associations of baroreflex sensitivity, heart rate variability, and initial orthostatic hypotension with prenatal and recent postnatal methylmercury exposure in the Seychelles Child Development Study at age 19 years. Int J Environ Res Public Health. 2015; 12 (3): 3395-3405.
37. Wakita Y,. Hypertension induced by methyl mercury in rats. Toxicol Appl Pharmacol. 2011; 89 (1): 144-147.
38. Carmignani M, Finelli VN, Boscolo P,. Mechanisms in cardiovascular regulation following chronic exposure of male rats to inorganic mercury. Toxicol Appl Pharmacol. 1983; 69 (3): 442-450.
39. Carmignani M, Boscolo P, Preziosi P,. Renal ultrastructural alterations and cardiovascular functional changes in rats exposed to mercuric chloride. Arch Toxicol Suppl. 1989; 13: 353-356.
40. Rossoni LV, Amaral SM, Vassallo PF,. Effects of mercury on the arterial blood pressure of anesthetized rats. Braz J Med Biol Res. 1999; 32 (8): 989-997.
41. da Cunha V, Souza HP, Rossoni LV, França AS, Vassallo DV,. Effects of mercury on the isolated perfused rat tail vascular bed are endothelium-dependent. Arch Environ Contam Toxicol. 2000; 39 (1): 124-130.
42. Jindal M, Garg GR, Mediratta PK, Fahim M,. Protective role of melatonin in myocardial oxidative damage induced by mercury in murine model. Hum Exp Toxicol. 2011; 30 (10): 1489-1500.
43. Moreira EL, de Oliveira J, Dutra MF,. Does methylmercury-induced hypercholesterolemia play a causal role in its neurotoxicity and cardiovascular disease? Toxicol Sci. 2012; 130 (2): 373-382.
44. Skoczy.,ska A, Poreba R, Steinmentz-Beck A,. The dependence between urinary mercury concentration and carotid arterial intima-media thickness in workers occupationally exposed to mercury vapour. Int J Occup Med Environ Health. 2009; 22 (2): 135-142.
45. Park ST, Lim KT, Chung YT, Kim SU,. Methylmercury-induced neurotoxicity in cerebral neuron culture is blocked by antioxidants and NMDA receptor antagonists. Neurotoxicology. 1996; 17 (1): 37-45.
46. Ganther HE, Goudie C, Sunde ML, Kopecky MJ, Wagner P,. Selenium: relation to decreased toxicity of methylmercury added to diets containing tuna. Science. 1972; 175 (4026): 1122-1124.
47. Valera B, Dewailly E, Poirier P,. ss. Hypertension. 2009; 54 (5): 981-986.
48. Yorifuji T, Tsuda T, Kashima S, Takao S, Harada M,. Long-term exposure to methylmercury and its effects on hypertension in Minamata. Environ Res. 2010; 110 (1): 40-46.
49. Vupputuri S, Longnecker MP, Daniels JL, Guo X, Sandler DP,. Blood mercury level and blood pressure among US women: results from the National Health and Nutrition Examination Survey 1999-2000. Environ Res. 2005; 97 (2): 195-200.
50. Moszczyski P,. Mercury and the risk of coronary heart disease. Przegl Lek. 2006; 63 (suppl 7): 84-87.
51. Virtanen JK, Rissanen TH, Voutilainen S, Tuomainen TP,. Mercury as a risk factor for cardiovascular diseases. J Nutr Biochem. 2007; 18 (2): 75-85.
52. Wennberg M, Strömberg U, Bergdahl IA,. Myocardial infarction in relation to mercury and fatty acids from fish: a riskbenefit analysis based on pooled Finnish and Swedish data in men. Am J Clin Nutr. 2012; 96 (4): 706-713.
53. Virtanen JK, Laukkanen JA, Mursu J, Voutilainen S, Tuomainen TP,. Serum long-chain n-3 polyunsaturated fatty acids, mercury, and risk of sudden cardiac death in men: a prospective population-based study. PLoS One. 2012; 7 (7): e41046.
54. McGuire JJ, Ding H, Triggle CR,. Endothelium-derived relaxing factors: a focus on endothelium-derived hyperpolarizing factor(s). Can J Physiol Pharmacol. 2001; 79 (6): 443-470.
55. Moncada S, Rees DD, Schulz R, Palmer RM,. Development and mechanism of a specific supersensitivity to nitrovasodilators after inhibition of vascular nitric oxide synthesis in vivo. Proc Natl Acad Sci U S A. 1991; 88 (6): 2166-2170.
56. Forstermann U, Closs EI, Pollock JS,. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension. 1994; 23 (6 pt 2): 1121-1131.
57. 2+-calmodulin and caveolin. J Biol Chem. 1997; 272 (25): 15583-1556.
58. Feron O, Saldana F, Michel JB, Michel T,. The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem. 1998; 273 (6): 3125-3128.
59. Ayajiki K, Kindermann M, Hecker M, Fleming I, Busse R,. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ Res. 1996; 78 (5): 750-758.
60. Rapoport RM, Murad F,. Agonist-induced endothelium-dependent relaxation in rat thoracic aorta may be mediated through cGMP. Circ Res. 1983; 52 (3): 352-357.
61. Lincoln TM, Komalavilas P, Cornwell TL,. Pleiotropic regulation of vascular smooth muscle tone by cyclic GMP-dependent protein kinase. Hypertension. 1994; 23 (6 pt 2): 1141-1147.
62. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA,. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature. 1994; 368 (6474): 850-853.
63. Ignarro LJ, Napoli C, Loscalzo J,. Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide: an overview. Circ Res. 2002; 90 (1): 21-28.
64. Böhm F, Pernow J,. The importance of endothelin-1 for vascular dysfunction in cardiovascular disease. Cardiovasc Res. 2007; 76 (1): 8-18.
65. Exton JH,. Regulation of Phospholipase D. Biochim Biophys Acta. 1999; 1439 (2): 121-133.
66. Natarajan V, Garcia JG,. Agonist-induced activation of phospholipase D in bovine pulmonary artery endothelial cells: regulation by protein kinase C and calcium. J Lab Clin Med. 1993; 121 (2): 337-347.
67. Brindley DN, Waggoner DW,. Phosphatidate phosphohydrolase and signal transduction. Chem Phys Lipids. 1996; 80 (1-2): 45-57.
68. McGill SN, Ahmed NA, Christou NV,. Endothelial cells: role in infection and inflammation. World J Surg. 1998; 22 (2): 171-178.
69. Rubanyi GM, Vanhoutte PM,. Superoxide anions and hyperoxia inactivate EDRR. Am J Physiol. 1986; 250 (5 pt 2): H822-H827.
70. Radi R, Beckman JS, Bush KM, Freeman BA,. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys. 1991; 288 (2): 481-487.
71. Soloviev AI, Tishkin SM, Parshikov AV, Ivanova IV, Goncharov EV, Gurney AM,. Mechanisms of endothelial dysfunction after ionized radiation: selective impairment of the nitric oxide component of endothelium-dependent vasodilation. Br J Pharmacol. 2003; 138 (5): 837-844.
72. Torres AD, Rai AN, Hardiek ML,. Mercury intoxication and arterial hypertension: report of two patients and review of the literature. Pediatrics. 2000; 105 (3): E34.
73. Omanwar S, Saidullah B, Ravi K, Fahim M,. Vasorelaxant effects of mercury on rat thoracic aorta: the nitric oxide signaling mechanism. Hum Exp Toxicol. 2013; 33 (9): 904-910.
74. Shimizu S, Ishii M, Yamamoto T, Kawanishi T, Momose K, Kuroiwa Y,. Bradykinin induces generation of reactive oxygen species in bovine aortic endothelial cells. Res Commun Chem Pathol Pharmacol. 1994; 84 (3): 301-14.
75. Katusic ZS, Vanhoutte PM,. Superoxide anion is an endothelium-derived contracting factor. Am J Physiol. 1989; 257 (1 pt 2): H33-H37.
76. 2+ release from vascular smooth muscle sarcoplasmic reticulum. Am J Physiol. 1992; 262 (1 pt 2): H114-H116.
77. Jin N, Packer CS, Rhoades RA,. Reactive oxygen-mediated contraction in pulmonary arterial smooth muscle: cellular mechanisms. Can J Physiol Pharmacol. 1991; 69 (3): 383-388.
78. Stohs SJ, Bagchi D,. Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 1995; 18 (2): 321-336.
79. Ercal N, Gurer-Orhan H, Aykin-Burns N,. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem. 2001; 1 (6): 529-523.
80. Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini AF,. The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol. 2003; 66 (8): 1499-1503.
81. Wolf MB, Baynes JW,. Cadmium and mercury cause an oxidative stress-induced endothelial dysfunction. Biometals. 2007; 20 (1): 73-81.
82. Park EJ, Park K,. Induction of reactive oxygen species and apoptosis in BEAS-2B cells by mercuric chloride. Toxicol In Vitro. 2007; 21 (5): 789-94.
83. Peltz A, Sherwani SI, Kotha SR,. Calcium and calmodulin regulate mercury-induced phospholipase D activation in vascular endothelial cells. Int J Toxicol. 2009; 28 (3): 190-206.
84. Mazerik JN, Mikkilineni H, Kuppusamy VA,. Mercury activates phospholipase a(2) and induces formation of arachidonic Acid metabolites in vascular endothelial cells. Toxicol Mech Methods. 2007; 17 (9): 541-557.
85. Lemos NB, Angeli Jhuli K,. Low mercury concentration produces vasoconstriction, decreases nitric oxide bioavailability and increases oxidative stress in rat conductance artery. PLoS One. 2012; 7 (11): e49005.
86. Rizzetti DA, Torres JG, Escobar AG,. Apocynin prevents vascular effects caused by chronic exposure to low concentrations of mercury. PLoS One. 2013; 8 (2): e55806.
87. Harisa GI, Mariee AD, Abo-Salem OM, Attiaa SM,. Erythrocyte nitric oxide synthase as a surrogate marker for mercury-induced vascular damage: the modulatory effects of naringin. Environ Toxicol. 2014; 29 (11): 1314-1322.
88. Furchgott RF, Zawadzki JV,. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980 27; 288 (5789): 373-6.
89. Harisa GI, Alanazi FK, El-Bassat RA, Malik A, Abdallah GM,. Protective effect of pravastatin against mercury induced vascular cells damage: erythrocytes as surrogate markers. Environ Toxicol Pharmacol. 2012; 34 (2): 428-435.
90. Omanwar S, Saidullah B, Ravi K, Fahim M,. Modulation of vasodilator response via the nitric oxide pathway after acute methyl mercury chloride exposure in rats. Biomed Res Int. 2013; 2013: 530603.