Haem, haem oxygenase and ferritin in vascular endothelial cell injury

Nephrology Dialysis Transplantation

Volumn 18, Issue SUPPL. 5, 2003, Pages

  Balla, József ^a   Vercellotti, Gregory M ^b   Nath, Karl ^c   Yachie, Akihiro ^d   Nagy, Emoke ^a   Eaton, John W ^e   Balla, György ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c MAYO CLINIC   (United States)

^d KANAZAWA UNIVERSITY   (Japan)

^e UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Endothelium; Ferritin; Haem oxygenase; Oxidative damage; Stress adaptation

Indexed keywords

BILIVERDIN; CARBON MONOXIDE; FERRITIN; HEME; HEME OXYGENASE; HEME OXYGENASE 1; HEMOGLOBIN; IRON; LOW DENSITY LIPOPROTEIN; OXIDIZING AGENT; PORPHYRIN; REACTIVE OXYGEN METABOLITE;

ATHEROSCLEROSIS; CELL DAMAGE; CELL KILLING; CELL PROTECTION; CYTOTOXICITY; ENDOTHELIUM CELL; ENZYME DEFICIENCY; ENZYME DEGRADATION; EXPOSURE; HOMEOSTASIS; HUMAN; INTRAVASCULAR HEMOLYSIS; KIDNEY FAILURE; NEUTROPHIL; OXIDATION; OXIDATION REDUCTION REACTION; PATHOGENESIS; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; THROMBOTIC THROMBOCYTOPENIC PURPURA; TRANSPORT KINETICS; UPREGULATION; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULITIS;

CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FERRITINS; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; KIDNEY DISEASES; OXIDATION-REDUCTION; OXIDATIVE STRESS; SENSITIVITY AND SPECIFICITY; VASCULAR DISEASES;

EID: 0042312347     PISSN: 09310509     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (47)

1. Halliwell B, Gutteridge JMC. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 1984; 219: 1-14
2. Repine JE, Fox RB, Berger EM. Hydrogen peroxide kills Staphylococcus aureus by reacting with staphylococcal iron to form hydroxyl radical. J Biol Chem 1981; 256: 7094-7096
3. Gannon DE, Varani J, Phan SH et al. Source of iron in neutrophil-mediated killing of endothelial cells. Lab Invest 1987; 57: 37-44
4. Balla G, Vercellotti GM, Muller-Eberhard U, Eaton J, Jacob HS. Exposure of endothelial cells to free heme potentiates damage mediated by granulocyte and toxic oxygen species. Lab Invest 1991; 64: 648-655
5. Balla J, Balla G, Jeney V, Kakuk G, Jacob HS, Vercellotti GM. Ferriporphyrins and endothelium: a 2-edged sword-promotion of oxidation and induction of cytoprotectants. Blood 2000; 95: 3442-3450
6. 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
7. Miller YI, Shaklai N. Oxidative crosslinking of LDL protein induced by hemin: involvement of tyrosines. Biochem Mol Biol Int 1994; 34: 1121-1129
8. Camejo G, Halberg C, Manschik-Ludin A et al. Hemin binding and oxidation of lipoproteins in serum: mechanisms and effect on the interaction of LDL with human macrophages. J Lipid Res 1998; 39: 755-766
9. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc Natl Acad Sci USA 1993; 90: 9285-9289
10. Bunn HF, Jandl JH. Exchange of heme among hemoglobins and between hemoglobin and albumin. J Biol Chem 1968; 243: 465-475
11. Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW, Balla G. Pro-oxidant and cytotoxic effects of circulating heme. Blood 2002; 100: 879-887
12. Paganga G, Rice-Evans C, Rule R, Leake D. The interaction between ruptured erythrocytes and low-density lipoproteins. FEBS Lett 1992; 303: 154-158
13. Miller YI, Altamentova SM, Shaklai N. Oxidation of low-density lipoprotein by hemoglobin stems from a heme-initiated globin radical: antioxidant role of haptoglobin. Biochemistry 1997; 36: 12189-12198
14. Hogg N, Rice-Evans C, Darley-Usmar V, Wilson MT, Paganga G, Bourne L. The role of lipid hydroperoxides in the myoglobin-dependent oxidation of LDL. Arch Biochem Biophys 1994; 314: 39-44
15. Wieland E, Parthasarathy S, Steinberg D. Peroxidase-dependent metal-independent oxidation of low density lipoprotein in vitro: a model for in vivo oxidation? Proc Natl Acad Sci USA 1993; 90: 5929-5933
16. Savenkova ML, Mueller DM, Heinecke JW. Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein. J Biol Chem 1994; 269: 20394-20400
17. Giulivi C, Cadenas E. Heme protein radicals: formation, fate, and biological consequences. Free Radic Biol Med 1998; 24: 269-279
18. 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
19. Ziouzenkova O, Asatryan L, Akmal M et al. Oxidative cross-linking of ApoB100 and hemoglobin results in low density lipoprotein modification in blood. Relevance to atherogenesis caused by hemodialysis. J Biol Chem 1999; 274: 18916-18924
20. Balla G, Jacob HS, Balla J et al. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992; 267: 18148-18153
21. Balla J, Nath K, Balla G, Juckett MB, Jacob HS, Vercellotti GM. Endothelial cell heme oxygenase and ferritin induction in rat lung by hemoglobin in vivo. Am J Physiol 1995; 268: 321-327
22. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 1968; 61: 748-755
23. Maines MD, Kappas A. Cobalt induction of hepatic heme oxygenase; with evidence that cytochrome P-450 is not essential for this enzyme activity. Proc Natl Acad Sci USA 1974; 71: 4293-4297
24. Keyse SM, Tyrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblast by UVA radiation, hydrogen peroxide, and sodium arsenate. Proc Natl Acad Sci USA 1989; 86: 99-103
25. Choi AMK, Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 1996; 15: 9-19
26. Shibahara S, Yoshida T, Kikuchi G. Induction of heme oxygenase by hemin in cultured pig alveolar macrophages. Arch Biochem Biophys 1978; 188: 243-250
27. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 1997; 247: 725-732
28. Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1996; 1275: 161-203
29. Juckett MB, Balla J, Balla G, Jessurun J, Jacob HS, Vercellotti GM. Ferritin protects endothelial cells from oxidized low density lipoprotein in vitro. Am J Pathol 1995; 147: 782-789
30. Abraham NG, Lavrovsky Y, Schwartzman ML et al. 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
31. Ewing JF, Haber SN, Maines MD. Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J Neurochem 1992; 58: 1140-1149
32. Dore S, Takahashi M, Ferris CD, Hester LD, Guastella D, Snyder SH. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 1999; 96: 2445-2450
33. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235: 1043-1046
34. Graser T, Vedernikov YP, Li DS. Study on the mechanism of carbon monoxide induced endothelium-independent relaxation in porcine coronary artery and vein. Biomed Biochim Acta 1990; 49: 293-296
35. Morita T, Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest 1995; 96: 2676-2682
36. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997; 37: 517-554
37. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 1987; 32: 497-504
38. Agarwal A, Balla J, Balla G, Croatt AJ, Vercellotti GM, Nath KA. Renal tubular epithelial cells mimic endothelial cells upon exposure to oxidized LDL. Am J Physiol 1996; 271: 814-823
39. Sadrzadeh SM, Eaton JW. Hemoglobin-mediated oxidant damage to the central nervous system requires endogenous ascorbate. J Clin Invest 1988; 82: 1510-1515
40. Nath KA, Balla G, Vercellotti GM et al. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 1992; 90: 267-270
41. Ishikawa K, Navab M, Leitinger N, Fogelman AM, Lusis AJ. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest 1997; 100: 1209-1216
42. Soares MP, Lin Y, Anrather J et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998; 4: 1073-1077
43. Yuan XM. Apoptotic macrophage-derived foam cells of human atheromas are rich in iron and ferritin, suggesting iron-catalysed reactions to be involved in apoptotis. Free Radic Res 1999; 30: 221-231
44. 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
45. Yachie A, Niida Y, Wada T et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest 1999; 103: 129-135
46. Kawashima A, Oda Y, Yachie A, Koizumi S, Nakanishi I. Heme oxygenase-1 deficiency: the first autopsy case. Hum Pathol 2002; 33: 125-130
47. Poss KD, Tonegawa S. Reduced stress defence in heme-oxygenase 1-deficient cells. Proc Natl Acad Sci USA 1997; 94: 10925-10930.