Aging and atherosclerosis in human and nonhuman primates

Journal of the American Aging Association

Volumn 20, Issue 1, 1997, Pages 15-28

  Cefalu, William T ^a   Wagner, Janice D ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Atherosclerosis; Glycation; Insulin; Lipids; Nonhuman primates; Obesity

Indexed keywords

ADVANCED GLYCATION END PRODUCT; INSULIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CEREBROVASCULAR DISEASE; HUMAN; HYPERINSULINEMIA; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; MONKEY; NONHUMAN; PRIMATE; RISK FACTOR;

EID: 0031545342     PISSN: 01619152     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11357-997-0002-4     Document Type: Article

References (108)

1. Thom, TJ, Epstein, FH, Feldman, JJ, Leaverton, PE, and Wolz, M. Total mortality and mortality from heart disease, cancer, and stroke from 1950 to 1987 in 27 countries Bethesda, MD: National Institutes of Health, 1992 (NIH Publ. No. 92-3088).
2. American Heart Association: Heart and stroke facts: 1994 statistical supplement. Dallas, TX: American Heart Association, 1994:1-22.
3. Guritz, JH, Osganian, V, Goldberg, RJ, Chen, ZY, Gore, JM, et al: Diagnostic testing in acute myocardial infarction does patient age influence utilization patterns? Am. J Epidemiol. 134:948-957, 1991
4. Cannon, LA, and Marshall, JM: Cardiac disease in the elderly population. Clin. Geriatr. Med. 9:499-525, 1993.
5. Wei, JY, and Gersh, BJ: Heart disease in the elderly. Curr. Probl. Cardiol. 12:1-65, 1987.
6. Duncan, AK, Vittone, J, Fleming, KC, and Smith, HC: Cardiovascular disease in elderly patients. Mayo Clin Proc. 71:184-196, 1996.
7. The Expert Panel: Summary of the second report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel II) JAMA. 269:3015-3023, 1993
8. Schaefer. EJ, Lichenstein, AH, Lamon-Fava, S. McNamara, JR, and Ordovas, JM: Lipoproteins, nutrition, aging, and atherosclerosis. Am. J. Clin. Nutr. (suppl):726S-740S, 1995.
9. McGill HC, Jr: Risk factors for atherosclerosis Adv. Exp Med. Biol 104:273-280. 1978.
10. Clarkson. TB, Weingand. KW, Kaplan. JR, and Adams. MR: Mechanisms of atherogenesis. Circulation 76(Suppl 1):20-28 1987.
11. Clarkson, TB, Anthony, MS, and Prichard. RW: The comparative pathology of nonhuman primate atherosclerosis Life Sci[A]. 79:61-78, 1984.
12. Weingand, KW: Recent advances in molecular pathology Atherosclerosis research in cynomolgus monkeys (Macaca fascicularis). Exp. Mol. Pathol. 50:1-15. 1989.
13. Cefalu, WT, Wagner, JD, Wang, ZQ, Bell-Farrow, AD, Collins J, et al: Study of caloric restriction in cynomolgus monkeys (Macaca fascicularis): A potential model for aging research. J Gerontol., 52A:B10-B19, 1997.
14. Cooper, LT, Cooke, JP, and Dzau, VJ: The vasculopathy of aging. J. Gerontol. Biol. Sci. 49:B191-B196, 1994.
15. Kannel, WB: Epidemiology of cardiovascular disease in the elderly: an assessment of risk factors. Cardiovasc. Clin. 22:9-22, 1992.
16. Stokes J, III: Cardiovascular risk factors. Cardiovasc. Clin. 20: 3-20, 1990.
17. JNC V: The Fifth Report of the Joint National Committee on Detection, Evaluation, and Treatment of High Blood Pressure (JNC V). Arch. Intern Med. 153:154-183, 1993.
18. McGill, HC, and Stern, MP: Sex and atherosclerosis. Atheroscler. Rev. 4:157-235, 1979.
19. Harris, T, Cook, EF, Kannel, WB, and Goldman, L: Proportional hazards analysis of risk factors for coronary heart disease in individuals aged 65 and older: the Framingham Heart Study. J Am. Geriatr. Soc. 36:1023-1028, 1988.
20. Stary, HC: Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis 9(Suppl 1): 1-19-1-32, 1989
21. St. Clair, RW: Atherosclerosis regression in animal models' Current concepts of cellular and biochemical mechanisms Prog. Cardiovasc. Dis. 26:109-132, 1983.
22. Ross, R: The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 362:801-809, 1993.
23. Schwartz, SM, deBlois, D, and O'Brien, ERM: The intima. Soil for atherosclerosis and restenosis. Circ. Res. 77.445-465. 1995.
24. Clarkson. TB: Progression and regression of non-human primate coronary artery atherosclerosis: Considerations of experimental design, in Regression of Atherosclerotic Lesions: Experimental Studies and Observations in Humans, edited by Malinow. MR. and Blaton. VH, New York. Plenum Press. 1984, pp. 43-60.
25. Glagov, S. Weisenberg. E , Zarins, CK. Stankunavicius, R. and Kolettis, GJ: Compensatory enlargement of human atherosclerotic coronary arteries. N. Engl. J. Med. 316:1371-1375, 1987.
26. Clarkson, TB, Prichard. RW. Morgan, TM, Petrick, GS, and Klein. KP: Remodeling of coronary arteries in human and nonhuman primates. JAMA 271:289-294, 1994.
27. Ooyama, T, and Sakamato. H: Elastase in the prevention of arterial ageing and the treatment of atherosclerosis. CIBA Found. Symposium 192:307-320, 1995.
28. Clarkson, TB, Lofland, HB, Bullock, BC, and Goodman, HO: Genetic control of plasma cholesterol Studies on squirrel monkeys. Arch. Pathol. 92.37-45, 1971.
29. Rudel, LL: Plasma lipoproteins in atherogenesis in nonhuman primates, in The Use of Nonhuman Primates in Cardiovascular Disease, edited by Kalter, SS, Austin, TX: University of Texas Press, 1980, pp. 37-57.
30. Wagner, WD, and Clarkson, TB: Comparative primate atherosclerosis. II. A biochemical study of lipids, calcium, and collagen in atherosclerotic arteries Exp Mol. Pathol. 23:96-121, 1975.
31. Parks, JS: Dietary effects on experimental atherosclerosis in nonhuman primates. Curr. Opin. Lipidol. 3.329-334, 1992.
32. McGill, HC, Jr., McMahan, M. Kruski, AW, and Mott, GE: Relationship of lipoprotein cholesterol concentrations to experimental atherosclerosis in baboons. Arteriosclerosis 1:3-12, 1981.
33. Strong, JP, Eggen, DA. and Jirge, SK Atherosclerotic lesions produced in baboons by feeding an atherogenic diet for four years Exp. Mol. Pathol. 24:320-332, 1976
34. Joag, SV, Li. Z, Foresman, L, Stephens, EB, Zhao LJ. et al Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4+ T cells and AIDS in pig-tailed macaques. J.Virol. 70:3189-3197, 1996.
35. Rudel, LL, Leathers, CW, Bond, MG, and Bullock, BC: Dietary ethanol-induced modification in hyperlipoproteinemia and atherosclerosis in non-human primates (Macaca nemestrina). Arteriosclerosis 1:144-155, 1981.
36. Williams. JK, Anthony, MS. and Clarkson TB: Coronary heart disease in monkeys with diet-induced coronary artery atherosclerosis Arch Pathol Lab. Med. 115.784-790. 1991
37. Chawla. KK, Murthy CDS. Chakravarti RN. and Chuttani. PN: Arteriosclerosis and thrombosis in wild rhesus monkeys. Am. Heart J. 73:85-91, 1967.
38. Honoré, EK. Williams. JK. Washburn. SA. and Herrington. DM: The effects of disease severity and sex on coronary endothelium-dependent vasomotor function in an atherosclerotic primate model. Coron. Artery Dis., 7:579-585. 1996.
39. Armstrong, ML. Atherosclerosis in rhesus and cynomolgus monkeys. Primates Med. 9:16-40, 1976.
40. Wissler, RW, Vesselinovitch. D: Studies of regression of advanced atherosclerosis in experimental animals and man. Ann. N.Y. Acad. Sci. 275:363-378. 1976.
41. Ylä-Herttuala, S Biochemistry of the arterial wall in developing atherosclerosis. Ann. N.Y. Acad. Sci 623:40-59, 1991.
42. Wagner, WD, St. Clair. RW, and Clarkson, TB: Angiochemical and tissue cholesterol changes in Macaca fascicularis fed an atherogenic diet for 3 years. Exp. Mol. Pathol. 28:140-153, 1978.
43. Weingand, KW, Clarkson, TB, Adams, MR. and Bostrom, AD: Effects of age and/or puberty on coronary artery atherosclerosis in cynomolgus monkeys. Atherosclerosis 62:137-144, 1986.
44. Clarkson, TB, Adams, MR, Williams, JK, and Wagner, JD: Clinical implications of animal models of gender difference in heart disease, in Cardiovascular Health and Disease in Women, edited by Douglas, PS, Philadelphia. W B. Saunders Company, 1993, pp 283-304.
45. Clarkson, TB: Personality, gender and coronary artery atherosclerosis of monkeys. Arteriosclerosis 7:1-8, 1987
46. Adams. MR, Kaplan, JR, Manuck, SB. Kontnik, DR. Parks, JS, et al: Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys. Lack of an effect of added progesterone. Arteriosclerosis 10:1051-1057. 1990.
47. Barrett-Connor. E. and Bush, TL: Estrogen and coronary heart disease in women. JAMA 265:1861-1867. 1991.
48. Wagner, JD, Clarkson, TB, St. Clair. RW, Schwenke, DC, Shively. CA, et al: Estrogen and progesterone replacement therapy reduces LDL accumulation in the coronary arteries of surgically postmenopausal cynomolgus monkeys J. Clin. Invest 88 1995-2002, 1991.
49. Williams. JK, Adams. MR. and Klopfenstein, HS: Estrogen modulates responses of atherosclerotic coronary arteries Circulation 81:1680-1687.1990.
50. Bowness, JM: Atherosclerosis and aging of the arterial wall. Can. Med. Assoc J 147:201, 1992.
51. Masoro. EJ: Physiological system markers of aging. Exp. Gerontol. 23.391-394, 1988.
52. Nakamura, H. Izumiyama. N, Nakamura, KI, and Ohtsubo, K' Age-associated ultrastructural changes in the aortic intima of rats with diet-induced hypercholesterolemia. Atherosclerosis 79:101-111, 1989.
53. Baker, GT, and Sprott, RL: Biomarkers of aging. Exp Gerontol 23:223-239. 1988
54. Cerami, A, Vlassara, H. and Brownlee, M: Protein glycosylation and the pathogenesis of atherosclerosis Metabolism 34(Suppl 1):37-44, 1985.
55. Vague J: The degree of masculine differentiation of obesities' A factor determining predisposition to diabetes, atherosclerosis, gout and uric calculous disease. Am. J. Clin. Nutr. 4:20-34, 1956.
56. Lapidus, L, Bengtsson, C, Larsson, B, Pennert, K, Rybo, E, et al: Distribution of adipose tissue and risk of cardiovascular disease and death. Br. Med. J. 289:1257-1261, 1984.
57. Larsson, B, Svärdsudd, K, Welin, L, Wilhelmsen, L, Björntorp, P, et al: Abdominal adipose tissue distribution, obesity, and risk of cardiovascular disease and death: 13 year follow up of participants in the study of men born in 1913. Br. Med. J. 288:1401-1404. 1984.
58. Stokes, J, III, Garrison, RJ, and Kannel, WB: The independent contributions of various indices of obesity to the 22-year incidence of coronary heart disease The Framingham Heart Study, in Metabolic Complications of Human Obesities, edited by Vague, J, Amsterdam, Elsevier Science Publishers, 1985, pp. 49-57.
59. Ducimetiere, P, Richard, J, and Cambien, F. The pattern of subcutaneous fat distribution in middle-aged men and the risk of coronary heart disease. Int. J Obesity 10:229-240, 1986.
60. Gillum, RF: The association of body fat distribution with hypertension, hypertensive heart disease, coronary heart disease, diabetes and cardiovascular risk factors in men and women aged 18-79 years. J. Chron. Dis 40:421-428, 1987.
61. Haffner. SM. Fong, D. Hazuda, HP. Pugh, JA. and Patterson, JK: Hyperinsulinemia, upper body adiposity and cardiovascular risk factors in non-diabetics. Metabolism 37:338-345, 1988.
62. Folsom. AR, Burke, GL, Ballew. C. Jacobs, DR. Haskell, WL, et al: Relation of body fatness and its distribution to cardiovascular risk factors in young blacks and whites. The role of insulin. Am. J. Epidemiol. 130:911-924, 1989
63. Ostlund, RE, Jr., Staten, M, Kohrt. WM. Schultz J. and Malley M: The ratio of waist-to-hip circumference, plasma insulin level, and glucose intolerance as independent predictors of the HDL-cholesterol level in older adults N. Engl. J. Med. 322:229-234, 1990.
64. Enzi, G, Gasparo, M, Biodetti, PR, Fiore, D, Semisa, M, et al: Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am, J. Clin. Nutr. 44:739-746, 1986.
65. Baumgartner, RN, Heymsfield, SB, Roche, AF, and Bernardino, M: Abdominal composition quantified by computed tomography. Am. J. Clin. Nutr. 48:936-945, 1988.
66. Peiris, AN, Sothmann, MS, Hoffmann, RG, Hennes, MI, Wilson, CR, et al: Adiposity, fat distribution, and cardiovascular risk. Ann. Intern. Med. 110:867-872, 1989.
67. Shimokata, H, Muller, DC, Fleg JL, Sorkin, J, Ziemba, AW, et al. Age as an independent determinant of glucose tolerance Diabetes 40:44-51, 1991.
68. Zavaroni, I, Dall'Aglio, E, Bruschi, F, Bonora, E, Alpi, O, et al: Effect of age and environmental factors on glucose tolerance and insulin secretion in a workerpopulation. J. Am. Geriatr. Soc. 34:271-275, 1986.
69. Rowe, JW, Minaker, KL, Pallotta, JA, Flier, JS: Characterization of insulin resistance of aging. J. Clin. Invest. 71:1581-1587, 1983.
70. DeFronzo. RA Glucose intolerance and aging: evidence for tissue insensitivity to insulin. Diabetes 28:1095-1101, 1979.
71. Stout, RW: Insulin and atheroma: 20-year perspective. Diabetes Care 13:631-654, 1990
72. Stout, RW: Hyperinsulinemia and atherosclerosis. Diabetes 45(Suppl 3).S45-S46, 1996.
73. DeFronzo, RA, and Ferrannini, E: Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14:173-194. 1991.
74. Ross, R: The pathology of atherosclerosis. An update. N Engl. J. Med. 314:488-500. 1986.
75. Coon. PJ. Rogus. EM. Drinkwater D Muller. DC, and Goldberg. AP. Role of body fat distribution in the decline in insulin sensitivity and glucose tolerance with age. J. Clin. Endocrinol Metab. 75.1125-1132, 1992
76. Kohrt, WM, Kirwan JP, Staten, MA. Bourey, RE. and King, DS. Insulin resistance in aging is related to abdominal obesity. Diabetes 42:273-281, 1993
77. Matsuzawa, Y, Shimomura, I, Nakamura, T, Keno, Y, Kotani. K. et al: Pathophysiology and pathogenesis of visceral fat obesity Obesity Res. 3(Supp 2):187S-194S, 1995.
78. Fujioka, S, Matsuzawa, Y, Tokunaga, K, Tarui, S: Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism 36:54-59, 1987.
79. Cefalu, WT, Wang, ZQ, Werbel, S, Bell-Farrow,A, Crouse, JR, III, et al: Contribution of visceral fat mass to the insulin resistance of aging. Metabolism 44:954-959, 1995.
80. Cerami, A: Hypothesis: Glucose as a mediator of aging. J. Am Geriatr. Soc. 33:626-634, 1985.
81. Baynes, JW, and Monnier, VM, eds. The Maillard reaction in aging, diabetes and nutrition, New York, Alan R. Liss, 1989.
82. Pongor. S. Ulrich, PC, Benath, FA, and Cerami, A: Aging of proteins: Isolation and identification of a fluorescent chromophore from the reaction of polypeptides with glucose. Proc. Natl. Acad. Sci. U.S.A. 81:2684-2688. 1984.
83. Reynolds, TM: Chemistry of nonenzymatic browning II. Adv Food Res. 14:167-283. 1965
84. Monnier, VM, Kohn, RR, and Cerami, A: Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad. Sci. USA. 81.583-587, 1984
85. Horiuchi, S, Higashi, T, Ikeda, K, Saishoji, T, Jinnouchi, Y, et al: Advanced glycation end products and their recognition by macrophage and macrophage-derived cells Diabetes 45(Suppl 3):S73-S76, 1996.
86. Schmidt. AM, Hori, O. Cao, R, Yan, SD, Brett, J, et al. A novel cellular receptor for advanced glycation end products. Diabetes45(Suppl 3).S77-S80, 1996.
87. Vlassara, H, and Bucala, R. Recent progress in advanced glycation and diabetic vascular disease: role of advanced glycation end products receptors Diabetes 45(Suppl 3):S65-S66, 1996
88. Cerami. A, Vlassara, H, and Brownlee, M: Protein glycosylation and the pathogenesis of atherosclerosis. Metabolism 34(Suppl 1).37-44, 1985.
89. Steinberg. D. Lipoproteins and atherosclerosis: A look back and a look ahead. Arteriosclerosis 3 283-301. 1983
90. Smith. EB: The relation between plasma and tissue lipids in human atherosclerosis Adv Lipid Res 12:1-49 1974.
91. Brownlee, M. Vlassara, H, and Cerami. A: Non-enzymatic glycosylation products on collagen covalentty trap low density lipoprotein. Diabetes 34:938-941. 1985.
92. Jen, KLC, Hansen, BC, and Metzger. BI: Adiposity, anthropometric measures and plasma insulin levels of rhesus monkeys. Int. J. Obesity 9-213-224, 1985.
93. Kemnitz, JW, Goy, RW, Flitsch, TJ, Lohmiller, JJ, and Robinson, JA: Obesity in male and female rhesus monkeys: Fat distribution, glucoregulation and serum androgen levels. J. Clin. Endocrinol. Metab. 69:287-293, 1989.
94. Shively, CA, Clarkson. TB, Miller, LC, and Weingand. KW: Body fat distribution as a risk factor for coronary artery atherosclerosis in female cynomolgus monkeys. Arteriosclerosis 7:226-231, 1987.
95. Shively, CA, and Clarkson, TB: Regional obesity and coronary artery atherosclerosis in females' a nonhuman primate model. Acta Med. Scand. 723(Suppl):71-78, 1988.
96. Wagner, JD, Martino, MA, Jayo, MJ, Anthony, MS, Clarkson, TB, et al: The effects of hormone replacement therapy on carbohydrate metabolism and cardiovascular risk factors in surgically postmenopausal cynomolgus monkeys. Metabolism Clin. Exp., 45:1254-1262, 1996.
97. Wagner. JD, Carlson, CS, O'Brten, TD, Anthony, MS, Bullock, BC, et al: Diabetes mellitus and islet amyloidosis in cynomolgus monkeys. Lab Anim. Sci 46:36-41, 1996.
98. Hansen, B.C., and Bodkin, N.L.. Heterogeneity of insulin responses: Phases leading to type 2 (non-insulin-dependent) diabetes mellitus in the rhesus monkey. Diabetologia 29:713-719, 1986.
99. Howard. CF, and Yasuda, M.: Diabetes mellitus in nonhuman primates. Recent research advances and current husbandry practices J. Med. Primatol 19:609-625, 1990.
100. Wagner, JD. Bagdade, JD. Litwak. KN, Zhang, L, Bell-Farrow, AD. et al: Increased glycation of plasma lipoproteins in diabetic cynomolgus monkeys. Lab Anim Sci. 46:31-35, 1996.
101. Harano, Y. Kojima, H. Kosugi, K. Suzuki, M, Harada, M, et al: Hyperlipidemia and atherosclerosis in experimental insulinopenic diabetic monkeys. Diabetes 16.163-173 1992
102. Lehner, NDM. Clarkson, TB. and Lofland, HB: The effect of insulin deficiency, hypothyroidism, and hypertension on atherosclerosis in the squirrel monkey. Exp. Mol. Pathol. 15:230-244, 1971.
103. Howard. CF. Vesselinovitch, D, and Wissler, RW: Correlations of aortic histology with gross aortic atherosclerosis and metabolic measurements in diabetic and nondiabetic Macaca nigra. Atherosclerosis 52:85-100, 1984
104. Nishimoto. S, Oohara, T, Sakai, M, Igaki, N. Masuta, S, et al: Collagen-glycation in the aorta: A developmental factor of aging and atherosclerosis Kobe J. Med. Sci. 34:179-187, 1988.
105. Ingram, DK, Cutler, RG, Weindruch, R, Renquist, DM, Knapka, JJ, et al: Dietary restriction and aging. The initiation of a primate study. J. Gerontol. 45:148-163, 1990.
106. Kemnitz, JE, Weindruch, R, Roecker, EB, Crawford, K, Kaufman, PL, et al: Dietary restriction of adult male Rhesus monkeys: Design, methodology, and preliminary findings from the first year of study. J. Gerontol. 48:B17-B26, 1993.
107. Weindruch, R, and Walford, RI: The retardation of aging and disease by dietary restriction. Charles C. Thomas, Springfield, Illinois, 1988.
108. Snyder, DL, editor. Dietary restriction and aging. Alan R. Liss, Inc., New York, 1989.