Nutrition, Metabolism & Cardiovascular Diseases
Volume 22, Issue 1 , Pages 1-7 , January 2012

Retention of atherogenic lipoproteins in the artery wall and its role in atherogenesis

Received 6 September 2011 ,Accepted 27 September 2011.

References 

  1. Steinberg D. The cholesterol controversy is over. Why did it take so long?. Circulation. 1989;80(4):1070–1078
  2. Powell LM, Wallis SC, Pease RJ, Edwards YH, Knott TJ, Scott J. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell. 1987;50(6):831–840
  3. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995;15(5):551–561
  4. Camejo G, Lopez A, Vegas H, Paoli H. The participation of aortic proteins in the formation of complexes between low density lipoproteins and intima-media extracts. Atherosclerosis. 1975;21(1):77–91
  5. Camejo G, Lalaguna F, Lopez F, Starosta R. Characterization and properties of a lipoprotein-complexing proteoglycan from human aorta. Atherosclerosis. 1980;35(3):307–320
  6. Vijayagopal P, Srinivasan SR, Radhakrishnamurthy B, Berenson GS. Interaction of serum lipoproteins and a proteoglycan from bovine aorta. J Biol Chem. 1981;256(15):8234–8241
  7. Nordestgaard BG, Wootton R, Lewis B. Selective retention of VLDL, IDL, and LDL in the arterial intima of genetically hyperlipidemic rabbits in vivo. Molecular size as a determinant of fractional loss from the intima-inner media. Arterioscler Thromb Vasc Biol. 1995;15(4):534–542
  8. Simionescu N, Simionescu M. Cellular interactions of lipoproteins with the vascular endothelium: endocytosis and transcytosis. Targeted Diagn Ther. 1991;5:45–95
  9. Proctor SD, Mamo JC. Intimal retention of cholesterol derived from apolipoprotein B100- and apolipoprotein B48-containing lipoproteins in carotid arteries of Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb Vasc Biol. 2003;23(9):1595–1600
  10. Schwenke DC, St Clair RW. Influx, efflux, and accumulation of LDL in normal arterial areas and atherosclerotic lesions of white Carneau pigeons with naturally occurring and cholesterol-aggravated aortic atherosclerosis. Arterioscler Thromb. 1993;13(9):1368–1381
  11. Proctor SD, Mamo JC. Retention of fluorescent-labelled chylomicron remnants within the intima of the arterial wall–evidence that plaque cholesterol may be derived from post-prandial lipoproteins. Eur J Clin Invest. 1998;28(6):497–503
  12. Camejo G. The interaction of lipids and lipoproteins with the intercellular matrix of arterial tissue: its possible role in atherogenesis. Adv Lipid Res. 1982;19:1–53
  13. Schonherr E, Jarvelainen HT, Sandell LJ, Wight TN. Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J Biol Chem. 1991;266(26):17640–17647
  14. Schonherr E, Jarvelainen HT, Kinsella MG, Sandell LJ, Wight TN. Platelet-derived growth factor and transforming growth factor-beta 1 differentially affect the synthesis of biglycan and decorin by monkey arterial smooth muscle cells. Arterioscler Thromb. 1993;13(7):1026–1036
  15. Jarvelainen HT, Kinsella MG, Wight TN, Sandell LJ. Differential expression of small chondroitin/dermatan sulfate proteoglycans, PG-I/biglycan and PG-II/decorin, by vascular smooth muscle and endothelial cells in culture. J Biol Chem. 1991;266(34):23274–23281
  16. O’Brien KD, Olin KL, Alpers CE, Chiu W, Ferguson M, Hudkins K, et al. Comparison of apolipoprotein and proteoglycan deposits in human coronary atherosclerotic plaques: colocalization of biglycan with apolipoproteins. Circulation. 1998;98(6):519–527
  17. Nakashima Y, Fujii H, Sumiyoshi S, Wight TN, Sueishi K. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol. 2007;27(5):1159–1165
  18. Tran-Lundmark K, Tran PK, Paulsson-Berne G, Friden V, Soininen R, Tryggvason K, et al. Heparan sulfate in perlecan promotes mouse atherosclerosis: roles in lipid permeability, lipid retention, and smooth muscle cell proliferation. Circ Res. 2008;103(1):43–52
  19. Iverius PH. The interaction between human plasma lipoproteins and connective tissue glycosaminoglycans. J Biol Chem. 1972;247(8):2607–2613
  20. Camejo G, Olofsson SO, Lopez F, Carlsson P, Bondjers G. Identification of Apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arteriosclerosis. 1988;8(4):368–377
  21. Hirose N, Blankenship DT, Krivanek MA, Jackson RL, Cardin AD. Isolation and characterization of four heparin-binding cyanogen bromide peptides of human plasma apolipoprotein B. Biochemistry. 1987;26(17):5505–5512
  22. Weisgraber KH, Rall SC. Human apolipoprotein B-100 heparin-binding sites. J Biol Chem. 1987;262(23):11097–11103
  23. Boren J, Olin K, Lee I, Chait A, Wight TN, Innerarity TL. Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J Clin Invest. 1998;101(12):2658–2664
  24. Chan L. Apolipoprotein B, the major protein component of triglyceride-rich and low density lipoproteins. J Biol Chem. 1992;267(36):25621–25624
  25. Skalen K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature. 2002;417(6890):750–754
  26. Rosenfeld ME, Polinsky P, Virmani R, Kauser K, Rubanyi G, Schwartz SM. Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler Thromb Vasc Biol. 2000;20(12):2587–2592
  27. Veniant MM, Pierotti V, Newland D, Cham CM, Sanan DA, Walzem RL, et al. Susceptibility to atherosclerosis in mice expressing exclusively apolipoprotein B48 or apolipoprotein B100. J Clin Invest. 1997;100(1):180–188
  28. Flood C, Gustafsson M, Richardson PE, Harvey SC, Segrest JP, Boren J. Identification of the proteoglycan binding site in apolipoprotein B48. J Biol Chem. 2002;277(35):32228–32233
  29. Flood C, Gustafsson M, Pitas RE, Arnaboldi L, Walzem RL, Boren J. Molecular mechanism for changes in proteoglycan binding on compositional changes of the core and the surface of low-density lipoprotein-containing human apolipoprotein B100. Arterioscler Thromb Vasc Biol. 2004;24(3):564–570
  30. Camejo G, Olsson U, Hurt-Camejo E, Baharamian N, Bondjers G. The extracellular matrix on atherogenesis and diabetes-associated vascular disease. Atheroscler Suppl. 2002;3(1):3–9
  31. Sartipy P, Camejo G, Svensson L, Hurt-Camejo E. Phospholipase A(2) modification of low density lipoproteins forms small high density particles with increased affinity for proteoglycans and glycosaminoglycans. J Biol Chem. 1999;274(36):25913–25920
  32. Kugiyama K, Ota Y, Takazoe K, Moriyama Y, Kawano H, Miyao Y, et al. Circulating levels of secretory type II phospholipase A(2) predict coronary events in patients with coronary artery disease. Circulation. 1999;100(12):1280–1284
  33. Griffin BA, Freeman DJ, Tait GW, Thomson J, Caslake MJ, Packard CJ, et al. Role of plasma triglyceride in the regulation of plasma low density lipoprotein (LDL) subfractions: relative contribution of small, dense LDL to coronary heart disease risk. Atherosclerosis. 1994;106(2):241–253
  34. Austin MA, King MC, Vranizan KM, Krauss RM. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease risk. Circulation. 1990;82(2):495–506
  35. Twickler T, Dallinga-Thie GM, Chapman MJ, Cohn JS. Remnant lipoproteins and atherosclerosis. Curr Atheroscler Rep. 2005;7(2):140–147
  36. Chung BH, Tallis G, Yalamoori V, Anantharamaiah GM, Segrest JP. Liposome-like particles isolated from human atherosclerotic plaques are structurally and compositionally similar to surface remnants of triglyceride-rich lipoproteins. Arterioscler Thromb. 1994;14(4):622–635
  37. Nakajima T, Origuchi N, Matsunaga T, Kawai S, Hokari S, Nakamura H, et al. Localization of oxidized HDL in atheromatous plaques and oxidized HDL binding sites on human aortic endothelial cells. Ann Clin Biochem. 2000;37(2):179–186
  38. Thorne RF, Mhaidat NM, Ralston KJ, Burns GF. CD36 is a receptor for oxidized high density lipoprotein: implications for the development of atherosclerosis. FEBS Lett. 2007;581(6):1227–1232
  39. Olin-Lewis K, Krauss RM, La Belle M, Blanche PJ, Barrett PH, Wight TN, et al. ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan. J Lipid Res. 2002;43(11):1969–1977
  40. Davidsson P, Hulthe J, Fagerberg B, Olsson BM, Hallberg C, Dahllof B, et al. A proteomic study of the apolipoproteins in LDL subclasses in patients with the metabolic syndrome and type 2 diabetes. J Lipid Res. 2005;46(9):1999–2006
  41. Hiukka A, Stahlman M, Pettersson C, Levin M, Adiels M, Teneberg S, et al. ApoCIII-enriched LDL in type 2 diabetes displays altered lipid composition, increased susceptibility for sphingomyelinase, and increased binding to biglycan. Diabetes. 2009;58(9):2018–2026
  42. Sacks FM, Alaupovic P, Moye LA, Cole TG, Sussex B, Stampfer MJ, et al. VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation. 2000;102(16):1886–1892
  43. Lee SJ, Campos H, Moye LA, Sacks FM. LDL containing apolipoprotein CIII is an independent risk factor for coronary events in diabetic patients. Arterioscler Thromb Vasc Biol. 2003;23(5):853–858
  44. Mauger JF, Couture P, Bergeron N, Lamarche B. Apolipoprotein C-III isoforms: kinetics and relative implication in lipid metabolism. J Lipid Res. 2006;47(6):1212–1218
  45. Kawakami A, Aikawa M, Alcaide P, Luscinskas FW, Libby P, Sacks FM. Apolipoprotein CIII induces expression of vascular cell adhesion molecule-1 in vascular endothelial cells and increases adhesion of monocytic cells. Circulation. 2006;114(7):681–687
  46. Nakashima Y, Chen YX, Kinukawa N, Sueishi K. Distributions of diffuse intimal thickening in human arteries: preferential expression in atherosclerosis-prone arteries from an early age. Virchows Arch. 2002;441(3):279–288
  47. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W, Richardson M, et al. A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb. 1992;12(1):120–134
  48. Kaprio J, Norio R, Pesonen E, Sarna S. Intimal thickening of the coronary arteries in infants in relation to family history of coronary artery disease. Circulation. 1993;87(6):1960–1968
  49. Kalan JM, Roberts WC. Morphologic findings in saphenous veins used as coronary arterial bypass conduits for longer than 1 year: necropsy analysis of 53 patients, 123 saphenous veins, and 1865 five-millimeter segments of veins. Am Heart J. 1990;119(5):1164–1184
  50. Camejo G, Hurt E, Wiklund O, Rosengren B, Lopez F, Bondjers G. Modifications of low-density lipoprotein induced by arterial proteoglycans and chondroitin-6-sulfate. Biochim Biophys Acta. 1991;1096(3):253–261
  51. Mateu L, Avila EM, Camejo G, Leon V, Liscano N. The structural stability of low-density lipoprotein. A kinetic X-ray scattering study of its interaction with arterial proteoglycans. Biochim Biophys Acta. 1984;795(3):525–534
  52. Hurt E, Bondjers G, Camejo G. Interaction of LDL with human arterial proteoglycans stimulates its uptake by human monocyte-derived macrophages. J Lipid Res. 1990;31(3):443–454
  53. Hurt-Camejo E, Camejo G, Rosengren B, Lopez F, Ahlstrom C, Fager G, et al. Effect of arterial proteoglycans and glycosaminoglycans on low density lipoprotein oxidation and its uptake by human macrophages and arterial smooth muscle cells. Arterioscler Thromb. 1992;12(5):569–583
  54. Camejo G, Hurt-Camejo E, Rosengren B, Wiklund O, Lopez F, Bondjers G. Modification of copper-catalyzed oxidation of low density lipoprotein by proteoglycans and glycosaminoglycans. J Lipid Res. 1991;32(12):1983–1991
  55. Upritchard JE, Sutherland WH. Oxidation of heparin-treated low density lipoprotein by peroxidases. Atherosclerosis. 1999;146(2):211–219
  56. Camejo G, Fager G, Rosengren B, Hurt-Camejo E, Bondjers G. Binding of low density lipoproteins by proteoglycans synthesized by proliferating and quiescent human arterial smooth muscle cells. J Biol Chem. 1993;268(19):14131–14137
  57. Chang MY, Potter-Perigo S, Tsoi C, Chait A, Wight TN. Oxidized low density lipoproteins regulate synthesis of monkey aortic smooth muscle cell proteoglycans that have enhanced native low density lipoprotein binding properties. J Biol Chem. 2000;275(7):4766–4773
  58. Gustafsson M, Levin M, Skalen K, Perman J, Friden V, Jirholt P, et al. Retention of low-density lipoprotein in atherosclerotic lesions of the mouse: evidence for a role of lipoprotein lipase. Circ Res. 2007;101(8):777–783
  59. Babaev VR, Fazio S, Gleaves LA, Carter KJ, Semenkovich CF, Linton MF. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in vivo. J Clin Invest. 1999;103(12):1697–1705
  60. Wilson K, Fry GL, Chappell DA, Sigmund CD, Medh JD. Macrophage-specific expression of human lipoprotein lipase accelerates atherosclerosis in transgenic apolipoprotein e knockout mice but not in C57BL/6 mice. Arterioscler Thromb Vasc Biol. 2001;21(11):1809–1815
  61. Tabas I, Li Y, Brocia RW, Xu SW, Swenson TL, Williams KJ. Lipoprotein lipase and sphingomyelinase synergistically enhance the association of atherogenic lipoproteins with smooth muscle cells and extracellular matrix. A possible mechanism for low density lipoprotein and lipoprotein(a) retention and macrophage foam cell formation. J Biol Chem. 1993;268(27):20419–20432
  62. Devlin CM, Leventhal AR, Kuriakose G, Schuchman EH, Williams KJ, Tabas I. Acid sphingomyelinase promotes lipoprotein retention within early atheromata and accelerates lesion progression. Arteriosclerosis, Thrombosis, Vascular Biology. 2008;28(10):1723–1730
  63. Oorni K, Hakala JK, Annila A, Ala-Korpela M, Kovanen PT. Sphingomyelinase induces aggregation and fusion, but phospholipase A2 only aggregation, of low density lipoprotein (LDL) particles. Two distinct mechanisms leading to increased binding strength of LDL to human aortic proteoglycans. J Biological Chemistry. 1998;273(44):29127–29134
  64. Marathe S, Choi Y, Leventhal AR, Tabas I. Sphingomyelinase converts lipoproteins from apolipoprotein E knockout mice into potent inducers of macrophage foam cell formation. Arteriosclerosis, Thrombosis, Vascular Biology. 2000;20(12):2607–2613
  65. Daoud AS, Jarmolych J, Augustyn JM, Fritz KE. Sequential morphologic studies of regression of advanced atherosclerosis. Arch Pathol Lab Med. 1981;105(5):233–239
  66. Armstrong ML, Warner ED, Connor WE. Regression of coronary atheromatosis in rhesus monkeys. Circ Res. 1970;27(1):59–67
  67. Armstrong ML. Evidence of regression of atherosclerosis in primates and man. Postgrad Med J. 1976;52(609):456–461
  68. Reis ED, Li J, Fayad ZA, Rong JX, Hansoty D, Aguinaldo JG, et al. Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein E-deficient mouse in a novel transplantation model. J Vasc Surg. 2001;34(3):541–547
  69. Wissler RW, Vesselinovitch D. Studies of regression of advanced atherosclerosis in experimental animals and man. Ann N Y Acad Sci. 1976;275:363–378
  70. Nissen SE, Tuzcu EM, Schoenhagen P, Brown BG, Ganz P, Vogel RA, et al. Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial. Jama. 2004;291(9):1071–1080
  71. Nissen SE, Nicholls SJ, Sipahi I, Libby P, Raichlen JS, Ballantyne CM, et al. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. Jama. 2006;295(13):1556–1565
  72. Manning JM, Gebre AK, Edwards IJ, Wagner WD, Rudel LL, Parks JS. Dietary polyunsaturated fat decreases interaction between low density lipoproteins and arterial proteoglycans. Lipids. 1994;29(9):635–641
  73. Carmena R, Ascaso JF, Camejo G, Varela G, Hurt-Camejo E, Ordovas JM, et al. Effect of olive and sunflower oils on low density lipoprotein level, composition, size, oxidation and interaction with arterial proteoglycans. Atherosclerosis. 1996;125(2):243–255
  74. Wiklund O, Bondjers G, Wright I, Camejo G. Insoluble complex formation between LDL and arterial proteoglycans in relation to serum lipid levels and effects of lipid lowering drugs. Atherosclerosis. 1996;119(1):57–67
  75. Getachew R, Ballinger ML, Burch ML, Reid JJ, Khachigian LM, Wight TN, et al. PDGF beta-receptor kinase activity and ERK1/2 mediate glycosaminoglycan elongation on biglycan and increases binding to LDL. Endocrinology. 2010;151(9):4356–4367
  76. Burch ML, Yang SN, Ballinger ML, Getachew R, Osman N, Little PJ. TGF-beta stimulates biglycan synthesis via p38 and ERK phosphorylation of the linker region of Smad2. Cell Mol Life Sci. 2010;67(12):2077–2090

PII: S0939-4753(11)00227-4

doi: 10.1016/j.numecd.2011.09.007

Nutrition, Metabolism & Cardiovascular Diseases
Volume 22, Issue 1 , Pages 1-7 , January 2012