Macrophage iron, hepcidin, and atherosclerotic plaque stability

Experimental Biology and Medicine

Volumn 232, Issue 8, 2007, Pages 1014-1020

  Sullivan, Jerome L ^a,b,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b University of Central Florida ^*  (United States)

^c UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Hemochromatosis; Hepcidin; Iron; Macrophage

Indexed keywords

HEPCIDIN; IRON;

ATHEROSCLEROTIC PLAQUE; DISEASE COURSE; DOWN REGULATION; HEMOCHROMATOSIS; HORMONE ACTION; HUMAN; IRON DEFICIENCY ANEMIA; IRON DEPLETION; IRON KINETICS; IRON TRANSPORT; LIPID PEROXIDATION; MACROPHAGE; NONHUMAN; SHORT SURVEY;

ANEMIA, IRON-DEFICIENCY; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ARTERIES; ATHEROSCLEROSIS; DOWN-REGULATION; ERYTHROPOIESIS; FOAM CELLS; HEMOCHROMATOSIS; HUMANS; INTESTINAL ABSORPTION; IRON; LIPID PEROXIDATION; PEPTIDE HORMONES;

ANIMALIA;

EID: 34548429748     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0703-MR-54     Document Type: Short Survey

References (73)

1. Sullivan JL. Iron and the sex difference in heart disease risk. Lancet 1: 1293-1294, 1981.
2. Sullivan JL. The iron paradigm of ischemic heart disease. Am Heart J 117:1177-1188, 1989.
3. Sullivan JL. Stored iron and ischemic heart disease. Empirical support for a new paradigm (editorial; comment). Circulation 86:1036-1037, 1992.
4. Sullivan JL. Are menstruating women protected from heart disease because of, or in spite of, estrogen? Relevance to the iron hypothesis. Am Heart J 145:190-194, 2003.
5. Sullivan JL. Stored iron and vascular reactivity. Arterioscler Thromb Vasc Biol 25:1532-1535, 2005.
6. Sullivan JL. Misconceptions in the debate on the iron hypothesis. J Nutr Biochem 12:33-37, 2001.
7. Yuan XM, Li W. The iron hypothesis of atherosclerosis and its clinical impact. Ann Med 35:578-591, 2003.
8. Brewer GJ. Iron and copper toxicity in diseases of aging, particularly atherosclerosis and Alzheimer's disease. Exp Biol Med 232:323-335, 2007.
9. Li L, Frei B. Iron chelation inhibits NF-κB-mediated adhesion molecule expression by inhibiting p22phox protein expression and NADPH oxidase activity. Arterioscler Thromb Vasc Biol 26:2638-2643, 2006.
10. Duffy SJ, Biegelsen ES, Holbrook M, Russell JD, Gokce N, Keaney JF, Jr, Vita JA. Iron chelation improves endothelial function in patients with coronary artery disease. Circulation 103:2799-2804, 2001.
11. Meyers DG. The iron hypothesis: does iron play a role in atherosclerosis? Transfusion 40:1023-1029, 2000.
12. Salonen JT, Tuomainen TP, Salonen R, Lakka TA, Nyyssonen K. Donation of blood is associated with reduced risk of myocardial infarction. The Kuopio Ischaemic Heart Disease Risk Factor Study. Am J Epidemiol 148:445-451, 1998.
13. Minqin R, Rajendran R, Pan N, Kwong-Huat TB, Ong WY, Watt F, Halliwell B. The iron chelator desferrioxamine inhibits atherosclerotic lesion development and decreases lesion iron concentrations in the cholesterol-fed rabbit. Free Radic Biol Med 38:1206-1211, 2005.
14. Lee HT, Chiu LL, Lee TS, Tsai HL, Chau LY. Dietary iron restriction increases plaque stability in apolipoprotein-e-deficient mice. J Biomed Sci 10:510-517, 2003.
15. Lee DH, Zacharski LR, Jacobs J. Comparison of the serum ferritin and percentage of transferrin saturation as exposure markers of iron-driven oxidative stress-related disease outcomes. Am Heart J 151:1247.e1-1247.e7, 2006.
16. Facchini FS, Saylor KL. Effect of iron depletion on cardiovascular risk factors: studies in carbohydrate-intolerant patients. Ann N Y Acad Sci 967:342-351, 2002.
17. Stadler N, Lindner RA, Davies MJ. Direct detection and quantification of transition metal ions in human atherosclerotic plaques: evidence for the presence of elevated levels of iron and copper. Arterioscler Thromb Vasc Biol 24:949-954, 2004.
18. Zheng H, Cable R, Spencer B, Votto N, Katz SD. Iron stores and vascular function in voluntary blood donors. Arterioscler Thromb Vasc Biol 25:1577-1583, 2005.
19. Zacharski LR, Chow BK, Howes PS, Shamayeva G, Baron JA, Dalman RL, Malenka DJ, Ozaki CK, Lavori PW. Reduction of iron stores and cardiovascular outcomes in patients with peripheral arterial disease: a randomized controlled trial. JAMA 297:603-610, 2007.
20. You SA, Wang Q. Ferritin in atherosclerosis. Clin Chim Acta 357:1-16, 2005.
21. Ferrara DE, Taylor WR. Iron chelation and vascular function: in search of the mechanisms. Arterioscler Thromb Vasc Biol 25:2235-2237, 2005.
22. Sullivan JL. Is homocysteine an iron-dependent cardiovascular risk factor? Kidney Int 69:642-644, 2006.
23. Sullivan J. Is stored iron safe? J Lab Clin Med 144:280-284, 2004.
24. Nemeth E, Ganz T. Regulation of iron metabolism by hepcidin. Annu Rev Nutr 26:323-342, 2006.
25. Ganz T. Hepcidin - a regulator of intestinal iron absorption and iron recycling by macrophages. Best Pract Res Clin Haematol 18:171-182, 2005.
26. Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, Ganz T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 113: 1271-1276, 2004.
27. Nguyen NB, Callaghan KD, Ghio AJ, Haile DJ, Yang F. Hepcidin expression and iron transport in alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 291:L417-L425, 2006.
28. Dunn LL, Rahmanto YS, Richardson DR. Iron uptake and metabolism in the new millennium. Trends Cell Biol 17:93-100, 2007.
29. Laine F, Deugnier Y. Increased expression of hepcidin in obese patients: impact on phenotypic expression of hemochromatosis and pathophysiology of dysmetabolic iron overload syndrome. Gastroenterology 131:2028, 2006.
30. Theurl I, Mattle V, Seifert M, Mariani M, Marth C, Weiss G. Dysregulated monocyte iron homeostasis and erythropoietin formation in patients with anemia of chronic disease. Blood 107:4142-4148, 2006.
31. Sullivan JL, Zacharski LR. Hereditary haemochromatosis and the hypothesis that iron depletion protects against ischemic heart disease. Eur J Clin Invest 31:375-377, 2001.
32. Ganz T, Nemeth E. Iron imports. IV. Hepcidin and regulation of body iron metabolism. Am J Physiol Gastrointest Liver Physiol 290:G199-G203, 2006.
33. Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S. The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110:1037-1044, 2002.
34. Kemna E, Tjalsma H, Laarakkers C, Nemeth E, Willems H, Swinkels D. Novel urine hepcidin assay by mass spectrometry. Blood 106:3268-3270, 2005.
35. Smith C, Mitchinson MJ, Aruoma OI, Halliwell B. Stimulation of lipid peroxidation and hydroxyl-radical generation by the contents of human atherosclerotic lesions. Biochem J 286:901-905, 1992.
36. Thong PS, Selley M, Watt F. Elemental changes in atherosclerotic lesions using nuclear microscopy. Cell Mol Biol (Noisy-Le-Grand) 42: 103-110, 1996.
37. Yuan XM, Anders WL, Olsson AG, Brunk UT. Iron in human atheroma and LDL oxidation by macrophages following erythrophagocytosis. Atherosclerosis 124:61-73, 1996.
38. Pang JH, Jiang MJ, Chen YL, Wang FW, Wang DL, Chu SH, Chau L. Increased ferritin gene expression in atherosclerotic lesions. J Clin Invest 97:2204-2212, 1996.
39. Matthews AJ, Vercellotti GM, Menchaca HJ, Bloch PH, Michalek VN, Marker PH, Murar J, Buchwald H. Iron and atherosclerosis: inhibition by the iron chelator deferiprone (L1). J Surg Res 73:35-40, 1997.
40. Ponraj D, Makjanic J, Thong PS, Tan BK, Watt F. The onset of atherosclerotic lesion formation in hypercholesterolemic rabbits is delayed by iron depletion. FEBS Lett 459:218-222, 1999.
41. Minqin R, Watt F, Huat BT, Halliwell B. Correlation of iron and zinc levels with lesion depth in newly formed atherosclerotic lesions. Free Radic Biol Med 34:746-752, 2003.
42. Ren M, Rajendran R, Ning P, Tan Kwong Huat B, Choon Nam O, Watt F, Jenner A, Halliwell B. Zinc supplementation decreases the development of atherosclerosis in rabbits. Free Radic Biol Med 41: 222-225, 2006.
43. Watt F, Rajendran R, Ren MQ, Tan BKH, Halliwell B. A nuclear microscopy study of trace elements Ca, Fe, Zn and Cu in atherosclerosis. Nucl Instrum Methods Phys Res B 249:646-652, 2006.
44. Lee FY, Lee TS, Pan CC, Huang AL, Chau LY. Colocalization of iron and ceroid in human atherosclerotic lesions. Atherosclerosis 138:281-288, 1998.
45. Lee TS, Shiao MS, Pan CC, Chau LY. Iron-deficient diet reduces atherosclerotic lesions in apoE-deficient mice. Circulation 99:1222-1229, 1999.
46. Lee TS, Lee FY, Pang JH, Chau LY. Erythrophagocytosis and iron deposition in atherosclerotic lesions. Chin J Physiol 42:17-23, 1999.
47. Stanley N, Stadler N, Woods AA, Bannon PG, Davies MJ. Concentrations of iron correlate with the extent of protein, but not lipid, oxidation in advanced human atherosclerotic lesions. Free Radic Biol Med 40:1636-1643, 2006.
48. Lapenna D, Pierdomenico SD, Ciofani G, Ucchino S, Neri M, Giamberardino MA, Cuccurullo F. Association of body iron stores with low molecular weight iron and oxidant damage of human atherosclerotic plaques. Free Radic Biol Med 42:492-498, 2007.
49. Yuan XM. Apoptotic macrophage-derived foam cells of human atheromas are rich in iron and ferritin, suggesting iron-catalysed reactions to be involved in apoptosis. Free Radic Res 30:221-231, 1999.
50. Yuan XM, Li W, Baird SK, Carlsson M, Melefors O. Secretion of ferritin by iron-laden macrophages and influence of lipoproteins. Free Radic Res 38:1133-1142, 2004.
51. Li W, Xu LH, Yuan XM. Macrophage hemoglobin scavenger receptor and ferritin accumulation in human atherosclerotic lesions. Ann N Y Acad Sci 1030:196-201, 2004.
52. Li W, Hellsten A, Nyhalah JD, Yuan XM. Enhanced expression of natural resistance-associated macrophage protein 1 in atherosclerotic lesions may be associated with oxidized lipid-induced apoptosis. Ann N Y Acad Sci 1030:202-207, 2004.
53. Li W, Hellsten A, Xu LH, Zhuang DM, Jansson K, Brunk UT, Yuan XM. Foam cell death induced by 7-hydroxycholesterol is mediated by labile iron-driven oxidative injury: mechanisms underlying induction of ferritin in human atheroma. Free Radic Biol Med 39:864-875, 2005.
54. 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 20:2281-2290, 2006.
55. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349:2316-2325, 2003.
56. Kraml PJ, Klein RL, Huang Y, Nareika A, Lopes-Virella MF. Iron loading increases cholesterol accumulation and macrophage scavenger receptor I expression in THP-1 mononuclear phagocytes. Metabolism 54:453-459, 2005.
57. Asleh R, Marsh S, Shilkrut M, Binah O, Guetta J, Lejbkowicz F, Enav B, Shehadeh N, Kanter Y, Lache O, Cohen O, Levy NS, Levy AP. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 92:1193-1200, 2003.
58. Levy AP, Levy JE, Kalet-Litman S, Miller-Lotan R, Levy NS, Asaf R, Guetta J, Yang C, Purushothaman KR, Fuster V, Moreno PR. Haptoglobin genotype is a determinant of iron, lipid peroxidation, and macrophage accumulation in the atherosclerotic plaque. Arterioscler Thromb Vasc Biol 27:134-140, 2007.
59. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 94:10919-10924, 1997.
60. Chen YH, Lin SJ, Lin MW, Tsai HL, Kuo SS, Chen JW, Charng MJ, Wu TC, Chen LC, Ding YA, Pan WH, Jou YS, Chau LY. Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet 111:1-8, 2002.
61. Dick P, Schillinger M, Minar E, Mlekusch W, Amighi J, Sabeti S, Schlager O, Raith M, Endler G, Mannhalter C, Wagner O, Exner M. Haem oxygenase-1 genotype and cardiovascular adverse events in patients with peripheral artery disease. Eur J Clin Invest 35:731-737, 2005.
62. Baranano DE, Wolosker H, Bae BI, Barrow RK, Snyder SH, Ferris CD. A mammalian iron ATPase induced by iron. J Biol Chem 275:15166-15173, 2000.
63. Pittock ST, Norby SM, Grande JP, Croatt AJ, Bren GD, Badley AD, Caplice NM, Griffin MD, Nath KA. MCP-1 is up-regulated in unstressed and stressed HO-1 knockout mice: pathophysiologic correlates. Kidney Int 68:611-622, 2005.
64. Chen JC, Huang KC, Lin WW. HMG-CoA reductase inhibitors upregulate heme oxygenase-1 expression in murine RAW264.7 macrophages via ERK, p38 MAPK and protein kinase G pathways. Cell Signal 18:32-39, 2006.
65. Nanami M, Ookawara T, Otaki Y, Ito K, Moriguchi R, Miyagawa K, Hasuike Y, Izumi M, Eguchi H, Suzuki K, Nakanishi T. Tumor necrosis factor-a-induced iron sequestration and oxidative stress in human endothelial cells. Arterioscler Thromb Vasc Biol 25:2495-2501, 2005.
66. Sullivan JL. Heterozygous hemochromatosis as a risk factor for premature myocardial infarction. Med Hypotheses 31:1-5, 1990.
67. Miller M, Hutchins GM. Hemochromatosis, multiorgan hemosiderosis, and coronary artery disease. JAMA 272:231-233, 1994.
68. Niederau C. Iron overload and atherosclerosis. Hepatology 32:672-674, 2000.
69. Franco RF, Zago MA, Trip MD, ten Cate H, van den EA, Prins MH, Kastelein JJ, Reitsma PH. Prevalence of hereditary haemochromatosis in premature atherosclerotic vascular disease. Br J Haematol 102:1172-1175, 1998.
70. DePalma RG, Hayes VW, Cafferata HT, Mohammadpour HA, Chow BK, Zacharski LR, Hall MR. Cytokine signatures in atherosclerotic claudicants. J Surg Res 111:215-221, 2003.
71. Ridker PM, Rifai N, Stampfer MJ, Hennekens CH. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 101:1767-1772, 2000.
72. Zacharski LR, Chow BK, Howes PS, Lavori PW, Shamayeva G. Implementation of an iron reduction protocol in patients with peripheral vascular disease: VA cooperative study no. 410: the Iron (Fe) and Atherosclerosis Study (FeAST). Am Heart J 148:386-392, 2004.
73. Amar J, Fauvel J, Drouet L, Ruidavets JB, Perret B, Chamontin B, Boccalon H, Ferrieres J. Interleukin 6 is associated with subclinical atherosclerosis: a link with soluble intercellular adhesion molecule 1. J Hypertens 24:1083-1088, 2006.