Atherosclerosis
Volume 183, Issue 2 , Pages 230-237 , December 2005

Role of the macrophage very-low-density lipoprotein receptor in atherosclerotic lesion development

  • Miranda Van Eck

      Affiliations

    • Division of Biopharmaceutics, Leiden/Amsterdam Center for Drug Research, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands
    • Corresponding Author InformationCorresponding author. Tel.: +31 71 5276238; fax: +31 71 5276032.
    web address
  • ,
  • Jenina Oost
  • ,
  • Jeltje R. Goudriaan

      Affiliations

    • TNO Prevention and Health, Gaubius Laboratory, The Netherlands
  • ,
  • Menno Hoekstra

      Affiliations

    • Division of Biopharmaceutics, Leiden/Amsterdam Center for Drug Research, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands
  • ,
  • Reeni B. Hildebrand

      Affiliations

    • Division of Biopharmaceutics, Leiden/Amsterdam Center for Drug Research, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands
  • ,
  • I. Sophie T. Bos

      Affiliations

    • Division of Biopharmaceutics, Leiden/Amsterdam Center for Drug Research, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands
  • ,
  • Ko Willems van Dijk

      Affiliations

    • Departments of General Internal Medicine and Human Genetics, Leiden University Medical Center, The Netherlands
  • ,
  • Theo J.C. Van Berkel

      Affiliations

    • Division of Biopharmaceutics, Leiden/Amsterdam Center for Drug Research, Gorlaeus Laboratories, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands

Received 17 September 2004 ,Revised 9 March 2005 ,Accepted 15 March 2005.

References 

  1. Takahashi S, Kawarabayasi Y, Nakai T, Sakai J, Yamamoto T. Rabbit very low-density lipoprotein receptor: a low-density lipoprotein-receptor-like protein with distinct ligand specificity. Proc Natl Acad Sci USA. 1992;89:9252–9256
  2. Gåfvels ME, Caird M, Britt D, Jackson CL, Patterson D, Strauss JF. Cloning of a cDNA encoding a putative human very low density lipoprotein/apolipoprotein E receptor and assignment of the gene to chromosome 9pter-p23. Somat Cell Mol Genet. 1993;19:557–569
  3. Oka K, Ishimura-Oka K, Chu MJ, et al. Mouse very-low-density-lipoprotein receptor (VLDLR) cDNA cloning, tissue- specific expression and evolutionary relationship with the low-density-lipoprotein receptor. Eur J Biochem. 1994;224:975–982
  4. Gåfvels ME, Paavola LG, Boyd CO, et al. Cloning of a complementary deoxyribonucleic acid encoding the murine homolog of the very low density lipoprotein/apolipoprotein-E receptor: Expression pattern and assignment of the gene to mouse chromosome 19. Endocrinology. 1994;135:387–394
  5. Sakai J, Hoshino A, Takahashi S, et al. Structure, chromosome location, and expression of the human very low density lipoprotein receptor gene. J Biol Chem. 1994;269:2173–2182
  6. Takahashi S, Suzuki J, Kohno M, et al. Enhancement of the binding of triglyceride-rich lipoproteins to the very low density lipoprotein receptor by apolipoprotein E and lipoprotein lipase. J Biol Chem. 1995;270:15747–15754
  7. Niemeier A, Grafvels M, Heeren J, Myer N, Angelin B, Beisiegel U. VLDL receptor mediates the uptake of human chylomicron remnants in vitro. J Lipid Res. 1996;37:1733–1742
  8. Argraves KM, Battey FD, MacCalman CD, et al. The very low density lipoprotein receptor mediates the cellular catabolism of lipoprotein lipase and urokinase-plasminogen activator inhibitor type I complexes. J Biol Chem. 1995;270:26550–26557
  9. Battey FD, Gåfvels ME, FitzGerald DJ, et al. The 39kDa receptor-associated protein regulates ligand binding by the very low-density lipoprotein receptor. J Biol Chem. 1994;269:23268–23273
  10. Rettenberger PM, Oka K, Ellgaard L, et al. Ligand binding properties of the very low density lipoprotein receptor Absence of the third complement-type repeat encoded by exon 4 is associated with reduced binding of Mr 40,000 receptor-associated protein. J Biol Chem. 1999;274:8973–8980
  11. Kasza A, Petersen HH, Heegaard CW, et al. Specificity of serine proteinase/serpin complex binding to very- low-density lipoprotein receptor and alpha2-macroglobulin receptor/low-density- lipoprotein-receptor-related protein. Eur J Biochem. 1997;248:270–281
  12. D’Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T. Reelin is a ligand for lipoprotein receptors. Neuron. 1999;24:471–479
  13. Webb JC, Patel DD, Jones MD, Knight BL, Soutar AK. Characterization and tissue-specific expression of the human ‘very low density lipoprotein (VLDL) receptor’ mRNA. Hum Mol Genet. 1994;3:531–537
  14. Tiebel O, Oka K, Robinson K, et al. Mouse very low-density lipoprotein receptor (VLDLR): gene structure, tissue-specific expression and dietary and developmental regulation. Atherosclerosis. 1999;145:239–251
  15. Kwok S, Singh-Bist A, Natu V, Kraemer FB. Dietary regulation of the very low density lipoprotein receptor in mouse heart and fat. Horm Metab Res. 1997;29:524–529
  16. Frykman PK, Brown MS, Yamamoto T, Goldstein JL, Herz J. Normal plasma lipoproteins and fertility in gene-targeted mice homozygous for a disruption in the gene encoding very low density lipoprotein receptor. Proc Natl Acad Sci USA. 1995;92:8453–8457
  17. Goudriaan JR, Tacken PJ, Dahlmans VE, et al. Protection from obesity in mice lacking the VLDL receptor. Arterioscler Thromb Vasc Biol. 2001;21:1488–1493
  18. Yagyu H, Lutz EP, Kako Y, et al. Very low density lipoprotein (VLDL) receptor-deficient mice have reduced lipoprotein lipase activity. Possible causes of hypertriglyceridemia and reduced body mass with VLDL receptor deficiency. J Biol Chem. 2002;277:10037–10043
  19. Tacken PJ, Teusink B, Jong MC, et al. LDL receptor deficiency unmasks altered VLDL triglyceride metabolism in VLDL receptor transgenic and knockout mice. J Lipid Res. 2000;41:2055–2062
  20. Multhaupt HA, Gafvels ME, Kariko K, et al. Expression of very low-density lipoprotein receptor in the vascular wall. Analysis of human tissues by in situ hybridization and immunohistochemistry. Am J Pathol. 1996;148:1985–1997
  21. Nakazato K, Ishibashi T, Shindo J, Shiomi M, Maruyama Y. Expression of very low density lipoprotein receptor mRNA in rabbit atherosclerotic lesions. Am J Pathol. 1996;149:1831–1838
  22. Argraves KM, Kozarsky KF, Fallon JT, Harpel PC, Strickland DK. The atherogenic lipoprotein Lp(a) is internalised and degraded in a process mediated by the VLDL receptor. J Clin Invest. 1997;100:2170–2181
  23. Hiltunen TP, Luoma JS, Nikkari T, Yla-Herttuala S. Expression of LDL receptor, VLDL receptor, LDL receptor-related protein, and scavenger receptor in rabbit atherosclerotic lesions: marked induction of scavenger receptor and VLDL receptor expression during lesion development. Circulation. 1998;97:1079–1086
  24. Wijnberg MJ, Quax PH, Nieuwenbroek NM, Verheijen JH. The migration of human smooth muscle cells in vitro is mediated by plasminogen activation and can be inhibited by alpha2-macroglobulin receptor associated protein. Thromb Haemost. 1997;78:880–886
  25. Wada Y, Homma Y, Nakazato K, Ishibashi T, Maruyama Y. Effect of overexpression of very low density lipoprotein receptor on cell growth. Heart Vessels. 2000;15:74–80
  26. Tacken PJ, Delsing DJM , Gijbels MJJ , et al. VLDL receptor deficiency enhances intimal thickening after vascular injury but does not affect atherosclerotic lesion area. Atherosclerosis. 2002;162:103–110
  27. Suzuki J, Takahashi S, Oida K, et al. Lipid accumulation and foam cell formation in Chinese hamster ovary cells overexpressing very low density lipoprotein receptor. Biochem Biophys Res Commun. 1995;206:835–842
  28. Kosaka S, Takahashi S, Masamura K, et al. Evidence of macrophage foam cell formation by very low-density lipoprotein receptor: interferon-gamma inhibition of very low-density lipoprotein receptor expression and foam cell formation in macrophages. Circulation. 2001;103(1):142–147
  29. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–159
  30. Kast HR, Nguyen CM, Sinal CJ, et al. Farnesoid X-activated receptor induces apolipoprotein C-II transcription: a molecular mechanism linking plasma triglyceride levels to bile acids. Mol Endocrinol. 2001;15:1720–1728
  31. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–126
  32. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem. 1997;272:20963–20966
  33. Koo C, Wernette-Hammond ME, Garcia Z, et al. Uptake of cholesterol-rich remnant lipoproteins by human monocyte-derived macrophages is mediated by low-density lipoprotein receptors. J Clin Invest. 1988;81:1332–1340
  34. Perrey S, Ishibashi S, Kitamine T, et al. The LDL receptor is the major pathway for β-VLDL uptake by mouse peritoneal macrophages. Atherosclerosis. 2001;154:51–60
  35. Kruth HS. Macrophage foam cells and atherosclerosis. Front Biosci. 2001;6:D429–D455
  36. Herijgers N, Van Eck M, Korporaal SJ, Hoogerbrugge PM. Van Berkel ThJC: relative importance of the LDL receptor and scavenger receptor class B in the beta-VLDL-induced uptake and accumulation of cholesteryl esters by peritoneal macrophages. J Lipid Res. 2000;41:1163–1171
  37. Herijgers N, Van Eck M, Groot PHE , Hoogerbrugge PM. Van Berkel ThJC Low density lipoprotein receptor of macrophages facilitates atherosclerotic lesion formation in C57Bl/6 mice. Arterioscler Thromb Vasc Biol. 2000;20:1961–1967
  38. Linton MF, Babaev VR, Gleaves LA, Fazio S. A direct role for the macrophage low density lipoprotein receptor in atherosclerotic lesion formation. J Biol Chem. 1999;274:19204–19210
  39. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science. 1986;232:34–47
  40. Ishibashi S, Goldstein JL, Brown MS, Herz J, Burns DK. Massive xanthomatosis and atherosclerosis in cholesterol-fed low-density lipoprotein receptor-negative mice. J Clin Invest. 1994;93:1885–1893
  41. Brown MS, Faust JR, Goldstein JL. Role of the low density lipoprotein receptor in regulating the content of free and esterified cholesterol in human fibroblasts. J Clin Invest. 1975;55:783–793
  42. Ginsberg HN. New perspectives on atherogenesis: role of abnormal triglyceride-rich lipoprotein metabolism. Circulation. 2002;106:2137–2142

PII: S0021-9150(05)00210-8

doi: 10.1016/j.atherosclerosis.2005.03.045

Atherosclerosis
Volume 183, Issue 2 , Pages 230-237 , December 2005