Deficiency of glutathione peroxidase-1 sensitizes hyperhomocysteinemic mice to endothelial dysfunction

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 22, Issue 12, 2002, Pages 1996-2002

  Dayal, Sanjana ^a   Brown, Kara L ^a   Weydert, Christine J ^a   Oberley, Larry W ^a   Arning, Erland ^b   Bottiglieri, Teodoro ^b   Faraci, Frank M ^a   Lentz, Steven R ^a,c  

^a UNIVERSITY OF IOWA   (United States)

^b BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Endothelium; Homocysteine; Nitric oxide; Peroxide

Indexed keywords

ACETYLCHOLINE; ETHIDIUM; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; HOMOCYSTEINE; HYDROETHIDINE; METHIONINE; NITROPRUSSIDE SODIUM; PAPAVERINE; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ENZYME ACTIVITY; ENZYME DEFICIENCY; HYPERHOMOCYSTEINEMIA; HYPOTHESIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RISK FACTOR; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASOMOTOR REFLEX;

ANIMALS; AORTA, THORACIC; CAROTID ARTERIES; CATALASE; DIET; ENDOTHELIUM, VASCULAR; ETHIDIUM; GLUTATHIONE PEROXIDASE; HOMOCYSTEINE; HYPERHOMOCYSTEINEMIA; LIVER; METHIONINE; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; SUPEROXIDE DISMUTASE; SUPEROXIDES; VASOMOTOR SYSTEM;

EID: 0036924890     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000041629.92741.DC     Document Type: Article

References (48)

1. Eikelboom JW, Lonn E, Genest JJ, Hankey G, Yusuf S. Homocyst(e)ine and cardiovascular disease: A critical review of the epidemiologic evidence. Ann Intern Med. 1999;131:363-375.
2. den Heijer M. Rosendaal FR, Blom H, Gerrits WBJ, Bos GMJ. Hyperhomocysteinemia and venous thrombosis: a meta-analysis. Thromb Haemost. 1998;80:874-877.
3. Lentz SR. Homocysteine and cardiovascular physiology. In: Carmel R, Jacobsen DW, eds. Homocysteine in Health and Disease. Cambridge, UK: Cambridge University Press; 2001:441-450.
4. Loscalzo J. The oxidant stress of hyperhomocyst(e)inemia. J Clin Invest. 1996;98:5-7.
5. Parthasarathy S. Oxidation of low density lipoprotein by thiol compounds leads to its recognition by the acetyl LDL receptor. Biochim Biophys Acta. 1987;917:337-340.
6. Heinecke JW, Rosen H, Suzuki LA, Chair A. The role of sulfurcontaining amino acids in superoxide production and modification of low density lipoprotein by arterial smooth muscle cells. J Biol Chem. 1987;262:10098-10103.
7. Jones BG, Rose FA, Tudball N. Lipid peroxidation and homocysteine induced toxicity. Atherosclerosis. 1994;105:165-170.
8. Upchurch GR, Welch GN, Fabian AJ. Freedman JE, Johnson JL, Keaney JF. Loscalzo J. Homocyst(e)ine decreases bioavailable nitric oxide by a mechanism involving glutathione peroxidase. J Biol Chem. 1997;272:17012-17017.
9. Zhang X, Li H, Jin H, Ebin Z, Brodsky S, Goligorsky MS. Effects of homocysteine on endothelial nitric oxide production. Am J Physiol. 2000;279:F671-F678.
10. Starkebaum G, Harlan JM. Endothelial cell injury due to coppercatalyzed hydrogen peroxide generation from homocysteine. J Clin Invest. 1986;77:1370-1376.
11. Outinen PA, Sood SK, Pfeifer SI, Pamidi S, Podor TJ, Li J, Weitz JI, Austin RC. Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells. Blood. 1999;94:959-967.
12. Jacobsen DW. Hyperhomocysteinemia and oxidative stress: Time for a reality check? Arterioscler Thromb Vasc Biol. 2000;20:1182-1184.
13. Blom HJ, Engelen DP, Boers GH, Stadhouders AM, Sengers RC, de Abreu R, TePoele-Pothoff MT, Trijbels JM. Lipid peroxidation in homocysteinaemia, J Inherit Metabol Dis. 1992;15:419-422.
14. Nightingale AK, James PP, Morris-Thurgood J. Harrold F, Tong R, Jackson SK. Cockcroft JR, Frenneaux MP. Evidence against oxidative stress as mechanism of endothelial dysfunction in methionine loading model. Am J Physiol. 2001;280:HI334-HI339.
15. Dudman NPB, Wilcken DEL, Stocker R. Circulating lipid hydroperoxide levels in human hyperhomocysteinemia: Relevance to development of arteriosclerosis. Arterioscler Thromb. 1993;13:512-516.
16. Domagala TB, Libura M, Szczeklik A. Hyperhomocysteinemia following oral methionine load is associated with increased lipid peroxidation. Thromb Res. 1997;87:411-416.
17. Chambers JC, McGregor A, Jean-Marie J, Obeid OA, Kooner JS. Demonstration of rapid onset vascular endothelial dysfunction after hyperhomocysteinemia: An effect reversible with vitamin C therapy. Circulation. 1999;99:1156-1160.
18. Kanani PM, Sinkey CA, Browning RL. Allaman M. Knapp HR, Haynes WG. Role of oxidant stress in endothelial dysfunction produced by experimental hyperhomocyst(e)inemia in humans. Circulation. 1999;100:1161-1168.
19. Raghuveer G, Sinkey CA, Chenard C, Stumbo P, Haynes WG. Effect of vitamin E on resistance vessel endothelial dysfunction induced by methionine. Am J Cardiol. 2001;88:285-290.
20. Eberhardt RT, Forgione MA, Cap A, Leopold JA, Rudd MA, Tolliet M, Heyrick S, Stark R, Klings ES, Moldovan NI, Yaghoubi M, Goldschmidt-Clermont PJ, Farber HW, Cohen R, Loscalzo J. Endothelial dysfunction in a murine model of mild hyperhomocyst(e)inemia J Clin Invest. 2000;106:483-491.
21. Lentz SR, Erger RA, Dayal S, Maeda N, Malinow MR, Heistad DD, Faraci FM. Folate dependence of hyperhomocysteinemia and endothelial dysfunction in cystathionine β-synthase-deficient mice. Am J Physiol. 2000;278:H970-H975.
22. Dayal S, Bottiglieri T, Arning E, Maeda N, Malinow MR, Sigmund CD, Heistad DD, Faraci FM, Lentz SR. Endothelial dysfunction and elevation of S-adenosylhomocysteine in cystathionine β-synthase-deficient mice. Circ Res. 2001;88:1203-1209.
23. Weiss N, Heydrick S, Zhang YY, Bierl C, Cap A, Loscalzo J. Cellular redox state and endothelial dysfunction in mildly hyperhomocysteinemic cystathionine beta-synthase-deficient mice. Arterioscler Thromb Vasc Biol. 2002;22:34-41.
24. Weiss N, Zhang YY, Heydrick S, Bierl C, Loscalzo J. Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction. Proc Natl Acad Sci U S A. 2001;98:12503-12508.
25. Ho YS, Magnenat JL, Bronson RT, Cao J, Gargano M. Sugawara M, Funk CD. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem. 1997;272:16644-16651.
26. Forgione MA, Weiss N. Heydrick S, Cap A, Klings ES, Bierl C, Eberhardt RT, Farber HW, Loscalzo J. Cellular glutathione peroxidase deficiency and endothelial dysfunction. Am J Physiol. 2002;282: H1255-HI261.
27. Mudd SH, Finkelstein JD, Refsum H, Ueland PM, Malinow MR, Lentz SR, Jacobsen DW, Brattström L, Wilcken B, Wilcken DEL, Blom HJ, Stabler SP, Allen RH, Selhub J, Rosenberg IH. Homocysteine and its disulfide derivatives: A suggested consensus terminology. Arterioscler Thromb Vasc Biol. 2000;20:1704-1706.
28. Martin SC, Hilton AC. Bartlett WA, Jones AF. Plasma total homocysteine measurement by ion-paired reversed-phase HPLC with electrochemical detection. Biomed Chromatogr. 1999;13:81-82.
29. Paglia PE, Valentine WN. Studies on the quantitation and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70:158-169.
30. Zhong W, Oberley LW, Oberley TD, Yan T. Domann FE, St. Clair DK. Inhibition of cell growth and sensitization to oxidative damage by overexpression of manganese superoxide dismutase in rat glioma cells. Cell Growth Differ. 1996;7:1175-1186.
31. Beers RF, Jr, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952:195:133-140.
32. 2 resistant Chinese hamster fibroblasts, Arch Biochem Biophys. 1990;279:249-260.
33. Spitz DR, Oberley LW. An assay for superoxide dismutase in mammalian tissue homogenates. Anal Biochem. 1989;179:8-18.
34. Faraci FM, Sigmund CD, Shesely EG, Maeda N, Heistad DD. Responses of carotid artery in mice deficient in expression of the gene for endothelial NO synthase. Am J Physiol. 1998;274:H564-H570.
35. Lake-Bruse KD, Faraci FM, Shesely EG, Meada N, Heistad DD. Gene transfer of endothelial nitric oxide synthase (eNOS) in eNOS-deficient mice. Am J Physiol. 1999;46:H770-H776.
36. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD. Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res. 1998;82:1298-1305.
37. Hathaway CA, Heistad DD, Piegors DJ, Miller FJ Jr. Regression of atherosclerosis in monkeys reduces vascular superoxide levels. Circ Res. 2002;90:277-283.
38. Arthur JR. The glutathione peroxidases. Cell Mol Life Sci. 2000;57:1825-1835.
39. Yoshida T, Maulik N, Engelman RM, Ho YS, Magnenat JL, Rousou JA, Flack JE, Deaton D, Das DK. Glutathione peroxidase knockout mice are susceptible to myocardial ischemia reperfusion injury. Circulation. 1997;96(suppl 11):II-216-II-220.
40. Beck MA, Esworthy RS. Ho YS, Chu FF. Glutathione peroxidase protects mice from viral-induced myocarditis. FASEB J. 1998;12:1143-1149.
41. Reddy VN, Lin LR, Ho YS, Magnenat JL, Ibaraki N, Giblin FJ, Dang L. Peroxide-induced damage in lenses of transgenic mice with deficient and elevated levels of glutathione peroxidase. Ophthalmologica. 1997;211:192-200.
42. Jaeschke H, Ho YS, Fisher MA, Lawson JA, Farhood A. Glutathione peroxidase-deficient mice are more susceptible to neutrophil-mediated hepatic parenchymal cell injury during endotoxemia: Importance of an intracellular oxidant stress. Hepatology, 1999:29:443-450.
43. Sengupta S, Wehbe C, Majors AK. Ketterer ME, DiBello PM. Jacobsen DW. Relative roles of albumin and ceruloplasmin in the formation of homocysteine, homocysteine-cysteine mixed disulfide and cystine in circulation. J Biol Chem. 2001;276:46896-46904.
44. Bagi Z, Ungvari Z, Koller A. Xanthine oxidase-derived reactive oxygen species convert flow-induced arteriolar dilation to constriction in hyperhomocysteinemia: Possible role of peroxynitrite. Arterioscler Thromb Vasc Biol. 2002;22:28-33.
45. Doshi SN, Mcdowell IFW, Moat SJ, Payne N, Durrant HJ, Lewis MJ, Goodfellow J. Folic acid improves endothelial function in coronary artery disease via mechanisms largely independent of homocysteine lowering. Circulation. 2002;105:22-26.
46. Huang RF, Hsu YC, Lin HL, Yang FL, Folate depletion and elevated plasma homocysteine promote oxidative stress in rat livers. J Nutr. 2001;131:33-38.
47. Cai H, Harrison DG, Drummond GR, Cai H, Davis ME. Ramasamy S, Harrison DG. Endothelial dysfunction in cardiovascular diseases: The role of oxidant stress: Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ Res. 2000;87:840-844.
48. Sies H, Sharov VS, Klotz LO, Briviba K. Glutathione peroxidase protects against peroxynitrite-mediated oxidations: A new function for selenoproteins as peroxynitrite reductase. J Biol Chem. 1997;272:27812-27817.