American Heart Journal
Volume 141, Issue 2, Supplement , Pages S1-S11 , February 2001

The smooth muscle cell membrane during atherogenesis: A potential target for amlodipine in atheroprotection

References 

  1. In:  Bahn PG editors. 100 great archeological discoveries. New York: : Barnes and Noble; 1999;p. 84
  2. National Center for Health Statistics . Vital statistics of the United States, 1990-1995. In: Mortality. Part A. vol 2:Washington (DC): : Government Printing Office; 1995;
  3. In: Tenth report of the director. Vol. 2: Heart and vascular diseases. Bethesda (MD): : National Heart, Lung and Blood Institute; 1982;p. 35
  4. Morbidity and mortality: 1996 chartbook on cardiovascular, lung and blood diseases. Bethesda (MD): : National Heart, Lung and Blood Institute; 1996;
  5. Breslow J. Cardiovascular disease myths and facts. Cleveland Clin J Med. 1998;65:286–287
  6. Kannel WB, Castelli WP, Gordon T. Cholesterol in the prediction atherosclerotic disease. New perspectives based on The Framingham Study. Ann Intern Med. 1979;90:825–836
  7. Kannel WB. High density lipoproteins: epidemiologic profile and risks of coronary artery disease. Am J Cardiol. 1983;52:9B–13B
  8. Kannel WB, Neaton JD, Wentworth D. Overall coronary heart disease mortality rate in relation to major risk factors in 325,348 men screened for the MRFIT. Am Heart J. 1986;112:825–836
  9. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science. 1986;232:34–37
  10. Smith S. Lessons from cholesterol-lowering trials. Am J Med. 1998;104:28S–32S
  11. Gorelick P, Sacco RL, Smith DB, et al.  Prevention of a first stroke: a review of guidelines and a multidisciplinary consensus statement from the National Stroke Association. JAMA. 1999;281:1112–1120
  12. Braunwald E. Cardiovascular medicine at the turn of the millennium: triumphs, concerns and opportunities. N Engl J Med. 1997;337:1360–1369
  13. Ross R, Glomset JA. The pathogenesis of atherosclerosis. N Engl J Med. 1976;295:369–377
  14. Ross R. Atherosclerosis: a problem of the biology of arterial wall cells and their interactions with blood components. Arteriosclerosis. 1981;1:293–311
  15. Ross R. The pathogenesis of atherosclerosis: an update. N Engl J Med. 1986;314:488–500
  16. Ross R. Pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801–809
  17. Ross R. Atherosclerosis: a defense mechanism gone awry. Am J Pathol. 1993;413:985–1002
  18. Ross R. Cell biology of atherosclerosis. Ann Rev Physiol. 1995;57:791–804
  19. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999;340:115–126
  20. Morel DW, DiCorleto PE, Chisolm GM. Endothelial and smooth muscle cells alter low density lipoprotein in vitro by free radical oxidation. Arteriosclerosis. 1984;4:357–364
  21. Libby P, Clinton S. The role of macrophages in atherogenesis. Curr Opin Lipidol. 1993;4:355–363
  22. Libby P, Hansson GK. Cytokines as modulators of cell proliferation in fibrotic diseases. Am Rev Resp Dis. 1989;140:1114–1117
  23. Wolfbauer G, Glick JM, Minor LK, et al.  Development of the smooth muscle foam cell: uptake of macrophage lipid inclusions. Proc Nat Acad Sci USA. 1986;83:7760–7764
  24. Campbell GR, Campbell JH. Smooth muscle phenotypic changes in arterial wall homeostasis: implications for the pathogenesis of atherosclerosis. Exp Mol Pathol. 1985;42:139–162
  25. Campbell GR, Campbell JH. Phenotypic modulation of smooth muscle cells in culture. In:  Campbell JH,  Campbell GR editor. Vascular smooth muscle in culture. Boca Raton (FL): : CRC Press; 1987;p. 39–55
  26. Hoff HF, Wagner WD. Plasma LDL accumulation in aortas of hypercholesterolemic swine correlates with modifications in aortic glycosaminoglycan composition. Atherosclerosis. 1986;61:231–236
  27. Camejo G, Acquatella H, Lalaguna F. Proteoglycans and lipoproteins in atherosclerosis. Curr Opin Lipidol. 1993;4:385–391
  28. Camejo G, Acquatella H, Lalaguna F. The interaction of low density lipoproteins with arterial proteoglycans. Atherosclerosis. 1980;36:55–65
  29. Mayne R. Collagenous proteins of blood vessels. Arteriosclerosis. 1986;6:585–593
  30. Munroe J, Cotran R. The pathogenesis of atherosclerosis: atherogenesis and inflammation. Lab Invest. 1988;58:249–261
  31. Steinberg D, Parthasarathy S, Carew TE, et al.  Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med. 1989;320:915–924
  32. Lehr HA, Seemuller J, Hubner C, et al.  Oxidized LDL-induced leukocyte/endothelium interaction in vivo involves the receptor for platelet-activating factor. Arterioscler Thromb. 1993;13:1013–1018
  33. Mehta A, Yang B, Khan S, et al.  Oxidized low density lipoproteins facilitate leukocyte adhesion to aortic intima without affecting endothelium-dependent relaxation: Role of P-selectin. Arterioscler Thromb. 1995;15:2076–2083
  34. Brown MS, Goldstein JL. Lipoprotein metabolism in the macrophage. Ann Rev Biochem. 1983;52:223–261
  35. Libby P, Ordover JM, Auger KR, et al.  Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells. Am J Pathol. 1986;124:179–185
  36. Sasahara M, Raines EW, Chait A, et al.  Inhibition of hypercholesterolemia-induced atherosclerosis in the nonhuman primate by probucol. I. Is the extent of atherosclerosis related to resistance of LDL to oxidation?. J Clin Invest. 1994;94:155–164
  37. Carew TE, Schwenke DC, Steinberg D. Antiatherogenic effect of probucol unrelated to its hypocholesterolemic effect: evidence that antioxidants in vivo can selectively inhibit LDL protein degradation in macrophage-rich fatty streaks slowing the progression of atherosclerosis in the WHHL rabbit. Proc Natl Acad Sci USA. 1987;84:7725–7729
  38. Mao SJ, Yates MT, Parker RA, et al.  Attenuation of atherosclerosis in a modified strain of hypercholesterolemic Watanabe rabbits with use of a probucol analogue that does not lower serum cholesterol. Arterioscler Thromb. 1991;11:1266–1275
  39. Shaish A, Daugherty A, O’Sullivan F, et al.  Beta-carotene inhibits atherosclerosis in hypercholesterolemic rabbits. J Clin Invest. 1995;96:2075–2082
  40. Elinder LS, Walldius G. Antioxidants and atherosclerosis progression: unresolved questions. Curr Opin Lipidol. 1994;5:265–268
  41. Walldius G, Erikson U, Olsson AG, et al.  The effect of probucol on femoral atherosclerosis: the Probucol Quantitative Regression Swedish Trial (PQRST). Am J Cardiol. 1994;74:875–883
  42. Hennekens C, Buring JE, Manson JE, et al.  Lack of effect of long-term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. N Engl J Med. 1996;334:1145–1149
  43. Omenn G, Goodman JE, Thornquist MD, et al.  Effects of a combination of β-carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med. 1996;334:1150–1155
  44. The Alpha-Tocopherol Beta Carotene Cancer Prevention Study Group . The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med. 1994;330:1029–1035
  45. Lenfant C. NIH ALERT on beta carotene study findings (CARET). Embargoed Release. Jan 18, 1995;
  46. Yusuf S, Dagenais G, Pogue J, et al.  Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med. 2000;342:154–160
  47. Yusuf S, Sleight P, Pogue J, et al.  Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med. 2000;342:145–153
  48. Brand K, Page S, Rogler G, et al.  Activated transcription factor nuclear factor-kappa B is present in the atherosclerotic lesion. J Clin Invest. 1996;97:1715–1722
  49. Bourcier T, Sukhova G, Libby P. The nuclear factor kappa-B signaling pathway participates in dysregulation of vascular smooth muscle cells in vitro and in human atherosclerosis. J Biol Chem. 1997;272:15817–15824
  50. Maruyama I, Shigeta K, Mihayara H, et al.  Thrombin activates NF-kappa B through thrombin receptor and results in proliferation of vascular smooth muscle cells: role of thrombin in atherosclerosis and restenosis. Ann NY Acad Sci. 1997;811:429–436
  51. Lin J, Zhu H, Liao HL, et al.  Induction of vascular cell adhesion molecule-1 by low-density lipoprotein. Atherosclerosis. 1996;127:185–194
  52. Baeuerle P, Henkel T. Function and activation of NK-κB in the immune system. Ann Rev Immunol. 1994;12:141–179
  53. Brand K, Page S, Walli AK, et al.  Role of nuclear factor-kappa B in atherogenesis. Exp Physiol. 1997;82:297–304
  54. Navab M, Fogelman AM, Berliner JA, et al.  Pathogenesis of atherosclerosis. Am J Cardiol. 1995;76:18C–23C
  55. Hoff H, Heideman CL, Gotto AM, et al.  Apolipoprotein B retention in the grossly normal and atherosclerotic human aorta. Circ Res. 1977;41:684–690
  56. Smith EB, Ashall C. Low density lipoprotein concentration in interstitial fluid from human atherosclerotic lesions. Relation to theories of endothelial damage and lipoprotein binding. Biochim Biophys Acta. 1983;754:249–257
  57. Schwenke DC, Carew TE. Initiation of atherosclerotic lesions in cholesterol-fed rabbits. II. Selective retention of LDL vs selective increases in LDL permeability in susceptible sites of arteries. Arteriosclerosis. 1989;9:908–918
  58. Schwenke DC, Carew TE. Initiation of atherosclerotic lesions in cholesterol-fed rabbits. I. Focal increases in arterial LDL concentration precede development of fatty streak lesions. Arteriosclerosis. 1989;9:895–907
  59. Linden T, Bondjers G, Camejo G, et al.  Affinity of LDL to a human arterial proteoglycan among male survivors of myocardial infarction. Eur J Clin Invest. 1989;19:38–44
  60. Jimi S, Sakata N, Matunaga A, et al.  Low density lipoproteins bind more to type I and II collagens by negative charge-dependent mechanisms than to type IV and V collagens. Atherosclerosis. 1994;107:109–116
  61. Williams KJ, Tabas I. The response to retention hypothesis of early atherogenesis. Arterioscler Thromb. 1995;15:551–561
  62. Simionescu N, Vasile E, Lupu F, et al.  Prelesional events in atherogenesis. Accumulation of extracellular cholesterol-rich liposomes in the arterial intima and cardiac valves of the hyperlipidemic rabbit. Am J Pathol. 1986;123:109–125
  63. Guyton JR, Klemp KF. The lipid-rich core region of human atherosclerotic fibrous plaques: prevalence of small lipid droplets and vesicles by electron microscopy. Am J Pathol. 1989;134:705–717
  64. Mora R, Lupus R, Simionescu N. Prelesional events in atherosclerosis: colocalization of apolipoprotein B, unesterified cholesterol and extracellular phospholipid liposomes in the hyperlipidemic rabbit aorta. Atherosclerosis. 1987;67:143–154
  65. Arbogast LY, et al.  Cellular cholesteryl ester accumulation induced by free cholesterol-rich lipid dispersions. Proc Natl Acad Sci USA. 1976;73:3680–3684
  66. Bialecki RA, Tulenko TN. Excess membrane cholesterol alters calcium channel activity in smooth muscle of rabbit carotid arteries. Am J Physiol. 1989;257:H170–H178
  67. Gleason MM, Medow MS, Tulenko TN. Excess membrane cholesterol alters calcium movements, cytosolic calcium levels, and membrane fluidity in arterial smooth muscle cells. Circ Res. 1991;69:216–227
  68. Agopal PV. Enhanced synthesis and accumulation of proteoglycans in cholesterol-enriched arterial smooth muscle cells. Biochem J. 1993;294:603–611
  69. Chen M, Mason RP, Tulenko TN. Atherosclerosis alters composition, structure and function of arterial smooth muscle plasma membranes. Biochim Biophys Acta. 1995;1272:101–112
  70. Lange Y, Swaisgood MH, Ramos BV, et al.  Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J Biol Chem. 1989;264:3786–3793
  71. Tulenko TN, Chen M, Mason PE, et al.  Physical effects of cholesterol on arterial smooth muscle membranes: evidence of immiscible cholesterol domains and alterations in bilayer width during atherogenesis. J Lipid Res. 1998;39:947–956
  72. Kurzchalia T, Parton R. Membrane microdomains and caveolae. Curr Opin Cell Biol. 1999;11:424–431
  73. Tulenko T, Laury-Kleintop L, Mason R. Cholesterol, calcium and atherogenesis. Int J Cardiol. 1997;62:55–66
  74. Stepp DS, Tulenko TN. Alterations in basal and serotonin-stimulated Ca2+ movements and vasoconstriction in atherosclerotic aorta. Arterioscler Thromb. 1994;14:1854–1859
  75. Weisbrod R, Griswold MC, Du Y, et al.  Reduced responsiveness of hypercholesterolemic rabbit aortic smooth muscle cells to nitric oxide. Arterioscler Thromb Vasc Biol. 1997;17:394–402
  76. Broderick R, Bialecki R, Tulenko T. Cholesterol-induced changes in arterial sensitivity to adrenergic stimulation. Am J Physiol. 1989;257:H170–H178
  77. Gesquiere L, Loreau N, Minnich A, et al.  Oxidative stress leads to cholesterol accumulation in vascular smooth muscle cells. Free Radic Biol Med. 1999;27:134–145
  78. Chen M, Mason RP, Tulenko TN. Restoration of membrane structure, composition and function in atherosclerosis arterial smooth muscle cells by human HDL. Biophys J. 1994;66:A388
  79. Tulenko T, et al.  The actions of the charged dihydropyridine amlodipine (Norvasc) in a cell culture model of dietary atherosclerosis. J Cardiovasc Pharmacol. 1995;26:S11–S17
  80. Mason RP, Moisey DM, Shajenko L. Cholesterol alters the binding of Ca2+ channel blockers to the membrane lipid bilayer. Mol Pharmacol. 1992;41:315–321
  81. McMurray HF, Chahwala SB. Amlodipine exerts a potent antimigrational effect on aortic smooth muscle cells in culture. J Am Coll Cardiol. 1991;17:194A
  82. Roth M, et al.  Ca2+ channel blockers modulate metabolism of collagens within the extracellular matrix. Proc Natl Acad Sci. 1996;83:5478–5482
  83. Nayler WG. Experimental models to study the prevention of atherosclerosis by calcium antagonists. J Cardiovasc Pharmacol. 1995;26:S18–S24
  84. Kramsch DM. Limits of lipid-lowering therapy: the benefits of amlodipine as an anti-atherogenic agent. J Hum Hypertens. 1995;9:S3–S9
  85. Pitt B, Byington RP, Furberg CD, et al.  for The PREVENT Investigators. Effect of amlodipine on the progression of atherosclerosis and the occurrence of clinical events. Circulation. 2000;102:1503–1510
  86. Chambless LE, Heiss G, Folsom AR, et al.  Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) Study, 1987-1993. Am J Epidemiol. 1997;146:483–494
  87. O’Leary DH, Polak JF, Kronmal RA, et al. , for the Cardiovascular Health Study Collaborative Research Group   Carotid artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N Engl J Med. 1999;340:14–22
  88. Hodis HN, Mack WJ, LaBree L, et al.  The role of carotid intima-media thickness in predicting clinical coronary events. Ann Intern Med. 1998;128:262–269
  89. Byington R, Riley W, Booth D, Herrington D, et al.  Effect of amlodipine on progression of carotid atherosclerosis in patients with documented heart disease. Am J Hypertens. 1999;12:42A

 Supported in part by National Institutes of Health grants HL-66273 and HL-51538 (T.N.T.) and grants from the American Heart Association (L.L.K.), The Pfizer Pharmaceutical Group, the John S. Sharpe Research Foundation, and the Baylis Family Endowment.

☆☆ Reprint requests: Thomas N. Tulenko, PhD, Director, Division of Vascular Biology, Lankenau Medical Research Center, 100 Lancaster Ave, Wynnewood, PA 19095. E-mail: tulenkot@MLHS.org

PII: S0002-8703(01)70037-3

American Heart Journal
Volume 141, Issue 2, Supplement , Pages S1-S11 , February 2001