Accelerated atherosclerosis and premature calcified cartilaginous metaplasia in the aorta of diabetic male Apo E knockout mice can be prevented by chronic treatment with 17β-estradiol

Atherosclerosis

Volumn 144, Issue 2, 1999, Pages 303-313

  Tse, Jenny ^a   Martin Mcnaulty, Baby ^a   Halks Miller, Meredith ^a   Kauser, Katalin ^a   DelVecchio, Virginia ^a   Vergona, Ronald ^a   Sullivan, Mark E ^a   Rubanyi, Gabor M ^a  

^a BAYER AG   (Germany)

Author keywords

17 Estradiol; Atherosclerosis; Calcification; Cartilaginous metaplasia; Diabetes; Hyperglycemia; Triglyceride

Indexed keywords

CHOLESTEROL; ESTRADIOL; GLUCOSE; STREPTOZOCIN; TRIACYLGLYCEROL;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; ARTERY CALCIFICATION; ARTICLE; ATHEROSCLEROTIC PLAQUE; CARTILAGINOUS TISSUE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; HYPERGLYCEMIA; KNOCKOUT MOUSE; MALE; METAPLASIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUBCUTANEOUS DRUG ADMINISTRATION; TRIACYLGLYCEROL BLOOD LEVEL; VASCULAR LESION;

ANIMALS; AORTA; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; CALCINOSIS; CARTILAGE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; ESTRADIOL; FEMALE; HUMANS; MALE; METAPLASIA; MICE; MICE, KNOCKOUT;

EID: 0033011076     PISSN: 00219150     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0021-9150(98)00325-6     Document Type: Article

References (57)

1. Hayashi T., Fukuto J.M., Ignarro L.J., Chaudhuri G. Gender differences in atherosclerosis: possible roles of nitric oxide. J Cardiovasc Pharmacol. 26:1995;792-802.
2. Isles C.G., Hole D.J., Hawthorne V.M., Lever A.F. Relation between coronary risk and coronary mortality in women of the Renfrew and Paisley survey: comparison with men. Lancet. 339:1992;702-706.
3. Stampfer M.J., Colditz G.A., Willett W.C., Manson J.E., Rosner B., Speizer F.E., Hennekens C.H. Postmenopausal estrogen therapy and cardiovascular disease: ten-year follow-up from the Nurses' Health Study. New Engl J Med. 325:1991;756-762.
4. Stampfer M.J. A review of the epidemiology of postmenopausal estrogens and the risk of coronary heart disease. Ramwell P., Rubanyi G.M., Schillinger E. Sex Steroids and the Cardiovascular System. 1992;145-160 Springer, Berlin.
5. Bush T.L., Fried L.P., Barrett-Connor E. Cholesterol, lipoproteins, and coronary heart disease in women. Clin Chem. 34:1988;B60-B70.
6. Cummings S.R. Evaluating the benefits and risks of postmenopausal hormone therapy. Am J Med. 91:1991;14S-18S.
7. Barrett-Connor E. Postmenopausal estrogen and heart disease. Atherosclerosis. 118:1995;S7-S10.
8. Bush T.L., Barrett-Connor E., Cowan L.D., Criqui M.H., Wallace R.B., Suchindran C.M., Tyroler H.A., Rifkind B.M. Cardiovascular mortality and noncontraceptive estrogen use in women: results from the Lipid Research Clinic's Program Follow-up Study. Circulation. 75:1987;1102-1109.
9. Bourassa P.A., Milos P.M., Gaynor B.J., Breslow J.L., Aiello R.J. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA. 93(19):1996;10022-10027.
10. Kauser K., Rubanyi G.M. Effect of 17β-estradiol on atherosclerotic lesion formation in Apo E-deficient mice. J Vasc Res. 33:1996;48.
11. Elhage R., Arnal J.-F., Pieraggi M.-T., Duverger N., Fievet C., Faye J.-C., Bayard F. 17β-Estradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 17:1997;2679-2684.
12. Beadenkopf W.G., Daoud A.S., Love B.M. Calcification in the coronary arteries and its relationship to arteriosclerosis and myocardial infarction. Am J Roentgenol. 92:1964;865-871.
13. McCarthy J.H., Palmer F.J. Incidence and significance of coronary artery calcification. Br Heart J. 36:1974;499-506.
14. Warburton R.K., Tampas J.P., Soule A.B., Taylor H.C. I.I.I. Coronary artery calcification: its relationship to coronary artery stenosis and myocardial infarction. Radiology. 91:1968;109-115.
15. Breen J.F., Sheedy P.F. I.I., Schwartz R.S., Stanson A.W., Kaufmann R.B., Moll P.P., Rumberger J.A. Coronary artery calcification detected with ultrafast CT as an indication of coronary artery disease. Radiology. 185:1992;435-439.
16. Witteman J.C.M., Kannel W.B., Wolf P.A., Grobbee D.E., Hofman A., D'Agostino R.B., Cobb J.C. Aortic calcified plaques and cardiovascular disease (the Framingham study). Am J Cardiol. 66:1990;1060-1064.
17. Simons D.B., Schwartz R.S., Edwards W.D., Sheedy P.F., Breen J.F., Rumberger J.A. Noninvasive definition of anatomic coronary artery disease by ultrafast computed tomographic scanning: a quantitative pathologic comparison study. J Am Coll Cardiol. 20:1992;1118-1126.
18. Bormann J.L., Stanford W., Stenberg R.G., Winniford M.D., Berbaum K.S., Talman C.L., Galvin J.R. Ultrafast computed tomographic detection of coronary artery calcification as an indicator of stenosis. Am J Card Imaging. 6:1992;191-196.
19. Qiao J.-H., Xie P.-Z., Fishbein M.C., Kreuzer J., Drake T.A., Demer L.L., Lusis A.J. Pathology of atheromatous lesions in inbred and genetically engineered mice: genetic determination of arterial calcification. Arterioscler Thromb. 14:1994;1480-1497.
20. Zhang S.H., Reddick R.L., Piedrahita J.A., Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 258:1992;468-471.
21. Plump A.S., Smith J.D., Hayek T., Aalto-Setala K., Walsh A., Verstuyft J.G., Rubin E.M., Breslow J.L. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 71:1992;343-353.
22. Nakashima Y., Plump A.S., Raines E.W., Breslow J.L., Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 14:1994;133-140.
23. Pyorala K., Laakso M., Uusitupa M. Diabetes and atherosclerosis: an epidemiologic view. Diabetes Metab Rev. 3:1987;463-524.
24. Bierman E.L. George Lyman Duff Memorial Lecture. Atherogenesis in diabetes. Arterioscler Thromb. 12:1992;647-656.
25. Krolewski A.S., Kosinski E.J., Warram J.H., Leland O.S., Busick E.J., Asmal A.C., Rand L.I., Christlieb A.R., Bradley R.F., Kahn C.R. Magnitude and determinants of coronary artery disease in juvenile-onset, insulin-dependent diabetes mellitus. Am J Cardiol. 59:1987;750-755.
26. Kunjathoor V.V., Wilson D.L., LeBoeuf R.C. Increased atherosclerosis in streptozotocin-induced diabetic mice. J Clin Invest. 97:1996;1767-1773.
27. Bradbury P., Gordon K.C. Connective tissues and stains. Bancroft J.D., Stevens A. Theory and Practice of Histological Techniques. 1990;133 Churchill Livingstone, New York.
28. Page K.M. Bone. Bancroft J.D., Stevens A. Theory and Practice of Histological Techniques. 1990;333-334 Churchill Livingstone, New York.
29. Mullarkey C.J., Edelstein D., Brownlee M. Free radical generation by early glycation products: a mechanism for accelerated atherogenesis in diabetes. Biochem Res Commun. 173:1990;932-939.
30. Baynes J.W. Role of oxidative stress in development of complications in diabetes. Diabetes. 40:1991;405-412.
31. Pfeiffer A., Schatz H. Diabetic microvascular complications and growth factors. Endocrinol Diabetes. 103:1995;7-14.
32. Jokinen M.P., Clarkson T.B., Prichard R.W. Recent advances in molecular pathology: animal models in atherosclerosis research. Exp Mol Pathol. 42:1985;1-28.
33. Hueper W.C. Cartilaginous foci in the hearts of white rats and of mice. Arch Pathol. 27:1939;466-468.
34. Hollander C.F. Cartilaginous focus at the base of the non-coronary semilunar valve of the aorta in rats of different ages. Exp Gerontol. 3:1968;303-307.
35. Seemayer T.Z., Thelmo W.L., Morin J. Cartilaginous transformation of the aortic valve. Am J Clin Pathol. 60:1973;616-620.
36. Groom D.A., Starke W.R. Cartilaginous metaplasia in calcific aortic valve disease. Am J Clin Pathol. 93:1990;809-812.
37. Demer L.L., Watson K.E., Bostrom K. Mechanism of calcification in atherosclerosis. Trends Cardiovasc Med. 4:1994;45-49.
38. Bostrom K., Watson K.E., Horn S., Wortham C., Herman I.M., Demer L.L. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 91:1993;1800-1809.
39. O'Brien E.R., Garvin M.R., Stewart D.K., Hinohara T., Simpson J.B., Schwartz S.M., Giachelli C.M. Osteopontin mRNA and protein are overexpressed in human coronary atherectomy specimens: clues to lesion calcification. Circulation. 88:1993;619.
40. Shanahan C.M., Cary N.R.B., Metcalfe J.C., Weissberg P.L. High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest. 93:1994;2393-2402.
41. Hirota S., Imakita M., Kohri K., Ito A., Morii E., Adachi S., Kim H.-M., Kitamura Y., Yutani C., Nomura S. Expression of osteopontin messenger RNA by macrophages in atherosclerotic plaques: a possible association with calcification. Am J Pathol. 143:1993;1003-1008.
42. O'Brien E.R., Garvin M.R., Stewart D.K., Hinohara T., Simpson J.B., Schwartz S.M., Giachelli C.M. Osteopontin is synthesized by macrophage, smooth muscle, and endothelial cells in primary and restenotic human coronary atherosclerotic plaques. Arterioscler Thromb. 14:1994;1648-1656.
43. Fitzpatrick L.A., Severson A., Edwards W.D., Ingram R.T. Diffuse calcification in human coronary arteries: association of osteopontin with atherosclerosis. J Clin Invest. 94:1994;1597-1604.
44. Watson K.E., Bostrom K., Ravindranath R., Lam T., Norton B., Demer L.L. TGF-β1 and 25-hydroxycholesterol stimulate osteoblast-like vascular cells to calcify. J Clin Invest. 93:1994;2106-2113.
45. Qiao J.-H., Fishbein M.C., Demer L.L., Lusis A.J. Genetic determination of cartilaginous metaplasia in mouse aorta. Arterioscler Thromb Vasc Biol. 15:1995;2265-2272.
46. Gisclard V., Miller V.M., Vanhoutte P.M. Effect of 17 beta-estradiol on endothelium-dependent responses in the rabbit. J Pharmacol Exp Ther. 244:1988;19-22.
47. Kauser K., Rubanyi G.M. Gender difference in bioassayable endothelium-derived nitric oxide from isolated rat aorta. Am J Physiol. 267:1994;H2311-H2317.
48. Jiang C.W., Sarrel P.M., Lindsay D.C., Poole-Wilson P.A., Collins P. Endothelium-independent relaxation of rabbit coronary artery by 17 beta-oestradiol in vitro. Br J Pharmacol. 104:1991;1033-1037.
49. Freay A.D., Curtis S.W., Korach K.S., Rubanyi G.M. Mechanism of vascular smooth muscle relaxation by estrogen in depolarized rat and mouse aorta: role of nuclear estrogen receptor and calcium-uptake. Circ Res. 81:1997;242-248.
50. Foegh M.L., Asotra S., Howell M.H., Ramwell P.W. Estradiol inhibition of arterial neointimal hyperplasia after balloon injury. J Vasc Surg. 19:1994;722-726.
51. Jilma B., Eichler H.G., Breiteneder H., Wolzt M., Aringer M., Graninger W., Rohrer C., Veitl M., Wagner O.F. Effects of 17 beta-estradiol on circulating adhesion molecules. J Clin Endocrinol Metab. 79:1994;1619-1624.
52. Keaney J.F. Jr, Shwaery G.T., Xu A., Nicolosi R.J., Loscalzo J., Foxall T.L., Vita J.A. 17 Beta-estradiol preserves endothelial vasodilator function and limits low-density lipoprotein oxidation in hypercholesterolemic swine. Circulation. 89:1994;2251-2259.
53. Frazier-Jessen M.R., Kovacs E.J. Estrogen modulation of JE/monocyte chemoattractant protein-1 mRNA expression in murine macrophages. J Immunol. 154:1995;1838-1845.
54. Ralston S.H., Russel R.G., Gowen M. Estrogen inhibits release of tumor necrosis factor from peripheral blood mononuclear cells in postmenopausal women. J Bone Miner Res. 5:1990;983-988.
55. Demer L.L. A skeleton in the atherosclerosis closet. Circulation. 92:1995;2029-2032.
56. Barrett-Connor E., Slone S., Greendale G., Kritz-Silverstein D., Espeland M., Johnson S.R., Waclawiw M., Fineberg S.E. The Postmenopausal Estrogen/Progestin Interventions Study: primary outcomes in adherent women. Maturitas. 27:1997;261-274.
57. Rubanyi G.M., Freay A.D., Kauser K., Sukovich D., Burton G., Lubahn D.B., Couse J.F., Curtis S.W., Korach K.S. Vascular estrogen receptors and endothelium-derived nitric oxide production in the mouse aorta: gender differences and effect of estrogen receptor gene disruption. J Clin Invest. 99:1997;2429-2437.