Aging influences development and progression of early aortic atherosclerotic lesions in cholesterol-fed rabbits

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 20, Issue 4, 2000, Pages 1123-1136

  Orlandi, Augusto ^a   Marcellini, Marcella ^a   Spagnoli, Luigi Giusto ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Aging; Atherosclerosis; Endothelial nitric oxide synthase; Glycosaminoglycans; Smooth muscle cells

Indexed keywords

GLYCOSAMINOGLYCAN; NITRIC OXIDE SYNTHASE;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ATHEROSCLEROSIS; ARTERY WALL; ARTICLE; ATHEROGENESIS; CELL PROLIFERATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER;

EID: 0034031788     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.20.4.1123     Document Type: Article

References (68)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for 1990s. Nature. 1993;362:801-809.
2. Haust MD. The morphogenesis and fate of potential and early atherosclerotic lesions in man. Hum Pathol. 1971;2:1-13.
3. Stary HC. Macrophages, macrophage foam cells, and eccentric intimal thickening in the coronary arteries of young children. Atherosclerosis. 1987;64:91-108.
4. Virmani R, Avolio AP, Mergner WJ, Robinowitz M, Herderic EE, Cornhill JF, Guo SY, Liu TH, Ou DY, O'Rourke M. Effect of aging on aortic morphology in populations with high and low prevalence of hypertension and atherosclerosis. Am J Pathol. 1991;139:1119-1129.
5. Gotto AM, Gorry GA, Thompson JR, Cole JS, Trost R, Yeshrun D, De Bakey ME. Relationship between plasma lipid concentration and coronary artery disease in 496 patients. Circulation. 1977;56:875-883.
6. Kolodgie FD, Katocs AS Jr, Largis EE, Wrenn SM, Cornhill JF, Herderick EE, Lee SJ, Virmani R. Hypercholesterolemia in the rabbit induced by feeding graded amounts of low-level cholesterol: methodological considerations regarding individual variability in response to dietary cholesterol and development of lesion type. Arterioscler Thromb Vasc Biol. 1996;16:1454-1464.
7. Wilson RB, Miller RA, Middleton CC, Kinden D. Atherosclerosis in rabbits fed a low cholesterol diet for five years. Arteriosclerosis. 1982; 2:228-241.
8. McGill HC Jr, Geer JC, Strong GP; Sandler M, Bourne J, eds. Atherosclerosis and Its Origin. New York, NY: Academic Press; 1963:39-65.
9. Bierman EL, Ross R. Aging and atherosclerosis. In: Paoletti R, Gotto AM, eds. Atherosclerosis Reviews. New York, NY: Raven Press; 1977; 2:79-111.
10. Spagnoli LG, Mauriello A, Orlandi A, Sangiorgi G, Bonanno E. Age-related changes affecting atherosclerotic risk: potential for pharmacological intervention. Drugs Aging. 1996;8:275-298.
11. Luscher TF, Tanner FC, Dohi Y. Age, hypertension and hypercholesterolemia alter endothelium-dependent vascular regulation. Pharmacol Toxicol. 1992;70(suppl):32-39.
12. Nakamura H, Izumiyama N, Nakamura K, Ohtsubo K. Age-associated ultrastructural changes in the aortic intima of rats with diet-induced hypercholesterolemia. Atherosclerosis. 1989;79:101-111.
13. Movat ZH, More MH, Haust MD. The diffuse intimai thickening of human aorta with aging. Am J Pathol. 1958;34:1023-1035.
14. Dobrin PB. Mechanical properties of arteries. Physiol Rev. 1978;58: 397-421.
15. Spagnoli LG, Orlandi A, Mauriello A, Santeusanio G, De Angelis C, Lucreziotti R, Ramacci MT. Aging and atherosclerosis in the rabbits, 1: distribution, prevalence and morphology of atherosclerotic lesions. Atherosclerosis. 1991;89:11-24.
16. Weingand KW, Clarkson TB, Adams MR, Bostrom AD. Effects ot age and/or puberty on coronary artery atherosclerosis in cynomolgus monkeys. Atherosclerosis. 1986;62:137-144.
17. Barnes SE, Weinberg PD. Contrasting patterns of spontaneous aortic disease in young and old rabbits. Arterioscler Thromb Vasc Biol. 1998; 18:300-308.
18. Gordon D, Reidy MA, Beneditt EP, Schwartz SM. Cell proliferation in human coronary arteries. Proc Natl Acad Sci U S A. 1990;87:4600-4604.
19. Spagnoli LG, Orlandi A, Santeusanio G. Foam cells of the rabbit atherosclerotic plaque arrested in metaphase by colchicine show a macrophage phenotype. Atherosclerosis. 1991;88:87-92.
20. Stary HC. Evolution and progression of atherosclerosis in the coronary arteries of children and adults. In: Bates SR, Gangloff EC, eds. Atherogenesis and Aging. New York, NY: Springer-Verlag; 1987:20-36.
21. Kockx MM, De Meyer GRY, Muhring J, Bult H, Bultinck J, Herman AG. Distribution of cell replication and apoptosis in atherosclerotic plaques of cholesterol-fed rabbits. Atherosclerosis. 1996;120:115-124.
22. Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G. Age influences the replicative activity and the differentiation features of cultured rat aortic smooth muscle cell populations and clones. Arterioscler Thromb. 1993;13:1449-1455.
23. Orlandi A, Ropraz P, Gabbiani G. Proliferative activity and α-smooth muscle actin expression in cultured rat aortic smooth muscle cells are differently modulated by transforming growth factor-β and heparin. Exp Cell Res. 1994;214:528-536.
24. Stemerman MB, Weinstein R, Rowe JW, Maciag T, Fuhro R, Gardner R. Vascular smooth muscle cell growth kinetics in vivo in aged rats. Proc Natl Acad Sci U S A. 1982;79:3863-3866.
25. Beynen AC, Katan MB, Van Zutphen LFM. Hypo-and hyperresponders: individual differences in the response of serum cholesterol concentration to changes in diet. Adv Lipid Res. 1987;22:115-171.
26. Spagnoli LG, Orlandi A, Bonaventura M, Mauriello A, De Angelis C, Ramacci MT. Propionyl-L-carnitine prevents the progression of atherosclerotic lesions in aged hyperlipemic rabbits. Atherosclerosis. 1995;114: 29-44.
27. Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem. 1974;20:470-475.
28. Doumas BT, Biggs HG. Standard Methods of Clinical Chemistry. Vol 7. New York, NY: Academic Press; 1972:175-212.
29. Weibel ER. Stereological methods. In: Practical Methods for Biological Morphometry. Vol I. London, UK/San Francisco, Calif: Academic Press; 1979:9-60.
30. Wight TN, Curwen KD, Litrenta MM, Alonso DR, Minick CR. Effect of endothelium on glycosaminoglycan accumulation in injured rabbit aorta. Am J Pathol. 1983;113:156-164.
31. Orlandi A, Mauriello M, Marino B, Spagnoli LG. Age-related modifications of aorta and coronaries in the rabbit: a morphological and morphometrical assessment. Arch Gerontol Geriatr. 1993;17:37-53.
32. Tsukada T, Rosenfeld M, Ross R, Gown A. Immunocytochemical analysis of cellular components in atherosclerotic lesions: use of monoclonal antibodies with the Watanabe and fat-fed rabbits. Arteriosclerosis. 1986; 6:601-613.
33. Skalli O, Ropraz R, Trecuiak A, Benzonana G, Gillesen G, Gabbiani G. A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol. 1986;103:2787-2796.
34. Kotani M, Yamamura Y, Tamatani T, Kimatura F, Miyasaka M. Generation and characterization of monoclonal antibodies against rabbit CD4, CD5 and CD11a antigens. J Exp Med. 1993;157:241-252.
35. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 1992;119:493-501.
36. Staley K, Blaschke AJ, Chun J. Apoptotic DNA fragmentation is detected by a semiquantitative ligation-mediated PCR of blunt DNA ends. Cell Death Differ. 1997;4:66-75.
37. Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W Jr, Rosenfeld ME, Schaffer A, Schwartz CJ, Wagner WD, Wissler RW. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association: special report. Arterioscler Thromb. 1994;14:840-856.
38. 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: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995;92:1355-1374.
39. Rosenfeld ME, Tsukada T, Gown AM, Ross R. Fatty streak initiation in Watanabe Heritable Hyperlipemic and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1987;7:9-23.
40. Back MR, Carew TE, Schmid-Schoenbein GW. Deposition pattern of monocytes and fatty streak development in hypercholesterolemic rabbit. Atherosclerosis. 1995;116:103-115.
41. Rosenfeld ME, Ross R. Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1990;10:680-687.
42. Richardson M, Hatton MWC, Moore S. Proteoglycan distribution in the intima and media of the aortas of young and aging rabbits: an ultrastructural study. Atherosclerosis. 1988;71:243-256.
43. Wight TN. Cell biology of arterial proteoglycans. Arteriosclerosis. 1989;9:1-20.
44. Falcone DJ, Hajjar DP, Minick R. Enhancement of cholesterol and cholesteryl ester accumulation in re-endothelialized aorta. Am J Pathol. 1980;99:81-104.
45. Wolfbauer G, Glick JM, Minor LK, Rothblat GH. Development of the smooth muscle foam cell: uptake of macrophage lipid inclusions. Proc Natl Acad Sci U S A. 1986;83:7760-7764.
46. Torzewski M, Torzewski J, Bowyer DE, Waltenberger J, Fitzsimmons C, Hombach V, Gabbert HE. Immunohistochemical colocalization of the terminal complex of human complement and smooth muscle cell alpha-actin in early atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 1997;17:2448-2452.
47. Manderson JA, Mosse PR, Safstrom JA, Young SB, Campbell GR. Balloon catheter injury to rabbit carotid artery, I: changes in smooth muscle phenotype. Arteriosclerosis. 1989;9:289-298.
48. Kocher O, Skalli O, Bloom WS, Gabbiani G. Cytoskeleton of rat aortic smooth muscle cells: normal conditions and experimental intimal thickening. Lab Invest. 1984;50:645-652.
49. Bochaton-Piallat ML, Ropraz P, Gabbiani F, Gabbiani G. Phenotypic heterogeneity of rat arterial smooth muscle cell clones: implications for the development of experimental intimal thickening. Arterioscler Thromb Vasc Biol. 1996;16:815-820.
50. Sartore S, Chiavegato A, Franch R, Faggin E, Pauletto P. Myosin gene expression and cell phenotypes in vascular smooth muscle during development, in experimental models, and in vascular disease. Arterioscler Thromb Vasc Biol. 1997;17:1210-1215.
51. Belmin J, Corman B, Merval R, Tedgui A. Age-related changes in endothelial permeability and distribution volume of albumin in rat aorta. Am J Physiol. 1993;264:H679-H685.
52. Cernadas MR, Sanchez de Miguel L, Garcia-Duran M, Gonzalez-Fernandez F, Millas I, Monton M, Rodrigo J, Rico L, Fernandez P, de Frutos T, Rodriguez-Feo JA, Guerra J, Caramelo C, Casado S, Lopez-Farre. Expression of constitutive and inducible nitric oxide synthases in the vascular wall of young and aging rats. Circ Res. 1998;83: 279-286.
53. Challah M, Nadaud S, Philippe M, Battle T, Soubrier F, Corman B, Michel JB. Circulating and cellular markers of endothelial dysfunction with aging in rats. Am J Physiol. 1997;273:H1941-H1948.
54. Cayatte AJ, Palacino JJ; Horten K, Cohen RA. Chronic inhibition of nitric oxide production accelerates neointima formation and impairs endothelial function in hypercholesterolemic rabbits. Arterioscler Thromb. 1994;14: 753-759.
55. Shimokawa H. Primary endothelial dysfunction: atherosclerosis. J Mol Cell Cardiol. 1999;31:23-37.
56. Forster BA, Weinberg PD. Changes with age in the influence of endogenous nitric oxide on transport properties of the rabbit aortic wall near branches. Arterioscler Thromb Vasc Biol. 1997;17:1361-1368.
57. Ooboshi H, Toyoda K, Faraci MG, Heistad DD. Improvement of relaxation in an atherosclerotic artery by gene transfer of endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol. 1998;18: 1752-1758.
58. Drew AF, Tipping PG. T helper cell infiltration and foam cell proliferation are early events in the development of atherosclerosis in cholesterol-fed rabbits. Arterioscler Thromb Vasc Biol. 1995;15: 1563-1568.
59. Amore B, Chiavegato A, Paulon T, Pauletto P, Sartore S. Atherosclerosis resistance in rats correlates with lack of expansion of an immature smooth muscle cell population. J Vasc Res. 1996;33:442-453.
60. Haunstetter A, Izumo S. Apoptosis: basic mechanisms and implications for cardiovascular disease. Circ Res. 1998;82:1111-1129.
61. Bennet MR, Evan GI, Newby AC. Deregulated expression of the c-myc oncogene abolishes inhibition of proliferation of rat vascular smooth muscle cells by serum reduction, interferon-γ, heparin and cyclic nucleotide analogues and induces apoptosis. Circ Res. 1994;74:525-536.
62. Bennet MR, Littlewood TD, Schwartz SM, Weissberg PL. Increased sensitivity of human vascular smooth muscle cells from atherosclerotic plaques to p53-mediated apoptosis. Circ Res. 1997;81:591-599.
63. Cocks MM. Apoptosis in the atherosclerotic plaque: quantitative and qualitative aspects. Arterioscler Thromb Vasc Biol. 1998;18:1519-1522.
64. Bennet MR, Boyle JJ. Apoptosis of vascular smooth muscle cells in atherosclerosis. Atherosclerosis. 1998;138:3-9.
65. Hansson GK, Seifert PS, Olsson G, Bondjers G. Immunohistochemical detection of macrophages and T-lymphocytes in atherosclerotic lesions of cholesterol-fed rabbits. Arterioscler Thromb. 1991;11:745-750.
66. Molenaar R, Visser WJ, Verkerk A, Koster JF, Jongkind JF. Peroxidative stress and in vitro ageing of endothelial cells increases the monocyte-endothelial cell adherence in a human in vitro system. Atherosclerosis. 1989;76:193-202.
67. Kishikawa H, Shimokawa T, Watanabe T. Localization of T lymphocytes and macrophages expressing IL-1, IL-2 receptor, IL-6 and TNF in human aortic intima: role of cell-mediated immunity in human atherogenesis. Virchows Arch. 1993;423:433-442.
68. Flynn PD, Byrne CD, Baglin TP, Weissberg PL, Bennet MR. Thrombin generation by apoptotic vascular smooth muscle cells. Blood. 1997;89: 4378-4384.