Red cells, hemoglobin, heme, iron, and atherogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 30, Issue 7, 2010, Pages 1347-1353

  Nagy, Emoke ^a   Eaton, John W ^b   Jeney, Viktória ^c,d   Soares, Miguel P ^d   Varga, Zsuzsa ^c   Galajda, Zoltán ^c   Szentmiklósi, József ^c   Méhes, Gábor ^c   Csonka, Tamás ^c   Smith, Ann ^e   Vercellotti, Gregory M ^f   Balla, György ^a,c   Balla, József ^a,c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c UNIVERSITY OF DEBRECEN   (Hungary)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

atherosclerosis; heme; heme oxygenase 1; hemoglobin; oxidized lipids; reactive oxygen species

Indexed keywords

HEME; HEME OXYGENASE 1; HEMOGLOBIN; IRON; REACTIVE OXYGEN METABOLITE;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; CELL INFILTRATION; CONTROLLED STUDY; ERYTHROCYTE; HEMOLYSIS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIPID OXIDATION; OXIDATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING;

AORTA; ATHEROSCLEROSIS; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIAL CELLS; ERYTHROCYTES; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HAPTOGLOBINS; HEMATOMA; HEME; HEME OXYGENASE-1; HEMOGLOBINS; HEMOLYSIS; HEMOPEXIN; HUMANS; IRON; LIPID PEROXIDATION; LIPOPROTEINS, LDL; METHEMOGLOBIN; OXIDATION-REDUCTION; OXIDATIVE STRESS; TYROSINE;

EID: 77953961138     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.206433     Document Type: Article

References (36)

1. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ. Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Circulation. 1995;92:1355-1374.
2. Paterson JC. Vascularization and hemorrhage of the intima of arterioscle-rotic coronary arteries. Arch Pathol. 1936;22:313-324.
3. Barger AC, Beeuwkes R III, Lainey LL, Silverman KJ. Hypothesis: vasa vasorum and neovascularization of human coronary arteries\a possible role in the pathophysiology of atherosclerosis. N Engl J Med. 1984;310: 175-177.
4. Fogelman AM, Shechter I, Seager J, Hokom M, Child FS, Edwards PA. Malondialdehyde alteration of low density lipoproteins leads to cho-lesteryl ester accumulation in human monocyte-macrophages. Proc Natl Acad Sci USA. 1980;77:2214-2218.
5. Sevanian A, McLeod LL. Cholesterol autoxidation in phospholipid bilayers. Lipids. 1987;22:627-631.
6. Li W, Ostblom M, Xu LH, Hellsten A, Leanderson P, Liedberg B, Brunk UT, Eaton JW, Yuan XM. Cytocidal effects of atheromatous plaque components: the death zone revisited. FASEB J. 2006;20:2281-2290.
7. Therond P, Abella A, Laurent D, Couturier M, Chalas J, Legrand A, Lindenbaum A. In vitro study of the cytotoxicity of isolated oxidized lipid low density lipoprotein fractions in human endothelial cells: relationship with the glutathione status and cell morphology. Free Radic Biol Med. 2000;28:585-596.
8. Balla G, Jacob HS, Eaton JW. Belcher JD, Vercellotti GM. Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial cell injury. Arterioscler Thromb. 1991;11:1700-1711.
9. Balla J, Vercellotti GM, Jeney V, Yachie A, Varga Z, Jacob HS, Eaton JW, Balla G. Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and dies) in an iron-rich environment. Antioxid Redox Signal. 2007;9:2119-2137.
10. Miller YI, Shaklai N. Oxidative crosslinking of LDL protein induced by hemin: involvement of tyrosines. Biochem Mol Biol Int. 1994;34: 1121-1129.
11. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen ME, Shibahara S, Kappas A. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci USA. 1995;92:6798-6802.
12. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton JW, Vercellotti GM. Ferritin: a cytoprotective antioxidant strategem of endo-thelium. J Biol Chem. 1992;267:18148-18153.
13. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endo-thelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA. 1993; 90:9285-9289.
14. Soares MP, Bach FH. Heme oxygenase-1: from biology to therapeutic potential. Trends Mol Med. 2009;15:50-58.
15. Wang LJ, Lee TS, Lee FY, Pai RC, Chau LY. Expression of heme oxygenase-1 in atherosclerotic lesions. Am J Pathol. 1998;152:711-720.
16. Juckett MB, Balla J, Balla G, Jessurun J, Jacob HS, Vercelotti GM. Ferritin protects endothelial cells from oxidized low density lipoprotein in vitro. Am J Pathol. 1995;147:782-789.
17. Ishikawa K, Sugawara D, Goto J, Watanabe Y, Kawamura K, Shiomi M, Itabe H, Maruyama Y. Heme oxygenase-1 inhibits atherogenesis in Watanabe Heritable Hyperlipidemic rabbits. Circulation. 2001;104: 1831-1836.
18. Juan SH, Lee TS, Tseng KW, Liou JY, Shyue SK, Wu KK, Chau LY. Adenovirus-mediated heme oxygenase-1 gene transfer inhibits the development of atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2001;104:1519-1525.
19. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1deficiency. J Clin Invest. 1999;103: 129-135.
20. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Biophys. 1959;37:911-917.
21. 2-induced dityrosine and tyrosine oxidation products in hemoglobin and red blood cells. J Biol Chem. 2001;276:24129-24136.
22. Carpenter KL, Taylor SE, Ballantine JA, Fussel B, Halliwell B, Mitchinson MJ. Lipids and oxidised lipids in human atheroma and normal aorta. Biochim Biophys Acta. 1993;1167:121-130.
23. van den Berg JJ, Op den Kamp JA, Lubin BH, Roelofsen B, Kuypers FA. Kinetics and site specificity of hydroperoxide-induced oxidative damage in red blood cells. Free Radic Biol Med. 1992;12:487-498.
24. Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW, Balla G. Pro-oxidant and cytotoxic effect of circulating heme. Blood. 2002;100: 879-887.
25. Nagy E, Jeney V, Yachie A, Szabó RP, Wagner O, Vercellotti GM, Eaton JW, Balla G, Balla J. Oxidation of hemoglobin by lipid hydroperoxide associated with low-density lipoprotein (LDL) and increased cytotoxic effect by LDL oxidation in heme oxygenase-1 (HO-1) deficiency. Cell Mol Biol (Noisy-le-grand). 2005;51:377-385.
26. Gutteridge JM, Smith A. Antioxidant protection by haemopexin of haem-stimulated lipid peroxidation. Biochem J. 1988;256:861-865.
27. Gutteridge JM. The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim Biophys Acta. 1987; 917:319-1223
28. Bunn HF, Jandl JH. Exchange of heme among hemoglobins and between hemoglobin and albumin. J Biol Chem. 1968;243:465-475.
29. Hill-Kapturczak N, Voakes C, Garcia J, Visner G, Nick HS, Agarwal A. A cis-acting region regulates oxidized lipid-mediated induction of the human heme oxygenase-1 gene in endothelial cells. Arterioscler Thromb Vasc Biol. 2003;23:1416-1422.
30. Weiss SJ. Neutrophil-mediated methemoglobin formation in the eryth-rocyte: the role of superoxide and hydrogen peroxide. J Biol Chem. 1982;257:2947-2953.
31. Giulivi C, Davies KJ. Hydrogen peroxide-mediated ferrylhemoglobin generation in vitro and in red blood cells. Methods Enzymol. 1994;231: 490-496.
32. Svistunenko DA,. Patel RP, Voloshchenko SV, and Wilson MT. The globin-based free radical of ferryl hemoglobin is detected in normal human blood. J Biol Chem. 1997;272:7114-7121.
33. Vollaard NB, Reeder BJ, Shearman JP, Menu P, Wilson MT, Cooper CE. A new sensitive assay reveals that hemoglobin is oxidatively modified in vivo. Free Radic Biol Med. 2005;39:1216-1228.
34. Reeder BJ, Grey M, Silaghi-Dumitrescu RL, Svistunenko DA, Bülow L, Cooper CE, Wilson MT. Tyrosine residues as redox cofactors in human hemoglobin: implications for engineering nontoxic blood substitutes. J Biol Chem. 2008;283:30780-30787.
35. Maples KR, Kennedy CH, Jordan SJ, Mason RP. In vivo thiyl free radical formation from hemoglobin following administration of hydroperoxides. Arch Biochem Biophys. 1990;277:402-409.
36. Silva G, Jeney V, Chora A, Larsen R, Balla J, Soares MP. Oxidized hemoglobin is an endogenous proinflammatory agonist that targets vascular endothelial cells. J Biol Chem. 2009;284:29582-29595.