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

Volumn 97, Issue 11, 1998, Pages 1079-1086

  Hiltunen, Timo P ^a,b   Luoma, Jukka S ^c   Nikkari, Tapio ^a   Ylä Herttuala, Seppo ^c  

^a UNIVERSITY OF TAMPERE MEDICAL SCHOOL   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Atherosclerosis; Lipoproteins; Proteins; Receptors

Indexed keywords

LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA INTIMA; ARTICLE; ATHEROSCLEROSIS; CHOLESTEROL INTAKE; CONTROLLED STUDY; ENDOTHELIUM CELL; FOAM CELL; HYPERLIPIDEMIA; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LIPID TRANSPORT; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0032562276     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.97.11.1079     Document Type: Article

References (57)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
2. Ylä-Herttuala S. Expression of lipoprotein receptors and related molecules in atherosclerotic lesions. Curr Opin Lipidol. 1996;7:292-297.
3. Brown MS, Goldstein JL. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu Rev Biochem. 1983;52:223-261.
4. 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 U S A. 1992;89: 9252-9256.
5. Krieger M, Herz J. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu Rev Biochem. 1994;63:601-637.
6. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med. 1989;320:915-924.
7. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science. 1986;232:34-47.
8. 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.
9. Kodama T, Freeman M, Rohrer L, Zabrecky J, Matsudaira P, Krieger M. Type I macrophage scavenger receptor contains α-helical and collagen-like coiled coils. Nature. 1990;343:531-535.
10. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Sigal E, Särkioja T, Witztum JL, Steinberg D. Gene expression in macrophage-rich human atherosclerotic lesions: 15-lipoxygenase and acetyl low density lipoprotein receptor messenger RNA colocalize with oxidation specific lipid-protein adducts. J Clin Invest. 1991;87:1146-1152.
11. Suzuki J, Takahashi S, Oida K, Shimada A, Kohno M, Tamai T, Miyabo S, Yamamoto T, Nakai T. 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.
12. Wyne KL, Pathak RK, Seabra MC, Hobbs HH. Expression of the VLDL receptor in endothelial cells. Arterioscler Thromb Vasc Biol. 1996;16: 407-415.
13. Multhaupt HAB, Gåfvels ME, Kariko K, Jin H, Arenas-Elliott C, Goldman BI, Strauss JF III, Angelin B, Warhol MJ, McCrae KR. 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.
14. 2-macroglobulin receptor/low density lipoprotein receptor-related protein and scavenger receptor in human atherosclerotic lesions. J Clin Invest. 1994;93:2014-2021.
15. Fraser I, Hughes D, Gordon S. Divalent cation-independent macrophage adhesion inhibited by monoclonal antibody to murine scavenger receptor. Nature. 1993;364:343-346.
16. Van Lenten BJ, Fogelman AM, Haberland ME, Edwards PA. The role of lipoproteins and receptor-mediated endocytosis in the transport of bacterial lipopolysaccharide. Proc Natl Acad Sci U S A. 1986;83:2704-2708.
17. Parhami F, Fang ZT, Fogelman AM, Andalibi A, Territo MC, Berliner JA. Minimally modified low density lipoprotein-induced inflammatory responses in endothelial cells are mediated by cyclic adenosine monophosphate. J Clin Invest. 1993;92:471-478.
18. Shackelford RE, Misra UK, Florine-Casteel K, Thai SF, Pizzo SV, Adams DO. Oxidized low density lipoprotein suppresses activation of NFκB in macrophages via a pertussis toxin-sensitive signaling mechanism. J Biol Chem. 1995;270:3475-3478.
19. Hiltunen T, Luoma J, Nikkari T, Ylä-Herttuala S. Induction of 15-lipoxygenase mRNA and protein in early atherosclerotic lesions. Circulation. 1995;92:3297-3303.
20. Kingston RE. CsCl purification of RNA from tissue. In: Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Smith J, Struhl K, eds. Current Protocols in Molecular Biology. New York, NY: Greene Publishing Assocs and John Wiley & Sons; 1991:4.2.3-4.2.4.
21. Hiltunen T, Raja-Honkala M, Nikkari T, Ylä-Herttuala S. A PCR artifact under low-stringency conditions due to amplification by only one primer. Biotechniques. 1994;17:240-242.
22. Yamamoto T, Bishop RW, Brown MS, Goldstein JL, Russell DW. Deletion in cysteine-rich region of LDL receptor impedes transport to cell surface in WHHL rabbit. Science. 1986;232:1230-1237.
23. Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, Stanley K. Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J. 1988;7:4119-4127.
24. Bickel PE, Freeman MW. Rabbit aortic smooth muscle cells express inducible macrophage scavenger receptor messenger RNA that is absent from endothelial cells. J Clin Invest. 1992;90:1450-1457.
25. Harris DE, Warshaw DM, Periasamy M. Nucleotide sequences of the rabbit α-smooth-muscle and β-non-muscle actin mRNAs. Gene. 1992; 112:265-266.
26. Raeymaekers L. Quantitative PCR: theoretical considerations with practical implications. Anal Biochem. 1993;214:582-585.
27. McCulloch RK, Choong C, Hurley D. An evaluation of competitor type and size for use in the determination of mRNA by competitive PCR. PCR Methods Appl. 1995;4:219-226.
28. Saito A, Pietromonaco S, Loo AK, Farquhar MG. Complete cloning and sequencing of rat gp330/'megalin', a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci U S A. 1994;91: 9725-9729.
29. Korenberg JR, Argraves K, Chen X, Tran H, Strickland DK, Argraves WS. Chromosomal localization of human genes for the LDL receptor family member glycoprotein 330 (LRP2) and its associated protein RAP (LRPAP1). Genomics. 1994;22:88-93.
30. Kim DH, Iijima H, Goto K, Sakai J, Ishii H, Kim HJ, Suzuki H, Kondo H, Saeki S, Yamamoto T. Human apolipoprotein E receptor 2: a novel lipoprotein receptor of the low density lipoprotein receptor family predominantly expressed in brain. J Biol Chem. 1996;271:8373-8380.
31. Novak S, Hiesberger T, Schneider WJ, Nimpf J. A new low density lipoprotein receptor homologue with 8 ligand binding repeats in brain of chicken and mouse. J Biol Chem. 1996;271:11732-11736.
32. Yamazaki H, Bujo H, Kusunoki J, Seimiya K, Kanaki T, Morisaki N, Schneider WJ, Saito Y. Elements of neural adhesion molecules and a yeast vacuolar protein sorting receptor are present in a novel mammalian low density lipoprotein receptor family member. J Biol Chem. 1996;271: 24761-24768.
33. Elomaa O, Kangas M, Sahlberg C, Tuukkanen J, Sormunen R, Liakka A, Thesleff I, Kraal G, Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 1995;80:603-609.
34. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994;269: 21003-21009.
35. Calvo D, Vega MA. Identification, primary structure, and distribution of CLA-1, a novel member of the CD36/LIMPII gene family. J Biol Chem. 1993;268:18929-18935.
36. Oquendo P, Hundt E, Lawler J, Seed B. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell. 1989;58: 95-101.
37. Ylä-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, Steinberg D. Colocalization of 15-lipoxygenase mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci U S A. 1990; 87:6959-6963.
38. Rosenfeld ME, Palinski W, Ylä-Herttuala S, Butler S, Witztum JL. Distribution of oxidation specific lipid-protein adducts and apolipoprotein B in atherosclerotic lesions of varying severity from WHHL rabbits. Arteriosclerosis. 1990;10:336-349.
39. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, Tanaka T, Miwa S, Katsura Y, Kita T, Masaki T. An endothelial receptor for oxidized low-density lipoprotein. Nature. 1997;386:73-77.
40. Wang AM, Doyle MV, Mark DF. Quantitation of mRNA by the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989;86:9717-9721.
41. Powell EE, Kroon PA. Low density lipoprotein receptor and 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression in human mononuclear leukocytes is regulated coordinately and parallels gene expression in human liver. J Clin Invest. 1994;93:2168-2174.
42. Niendorf A, Gebhardt A. Quantitative Analyse der mRNA-Expression von LDL-Rezeptor und HMG-CoA Reduktase im bovinen Gewebe mittels kompetitiver RT-PCR. Pathologe. 1994;15:201-206.
43. 2-macroglobulin receptor in monocytes and fibroblasts: monoclonal antibodies define the receptor as a monocyte differentiation antigen. Exp Cell Res. 1990;190:195-203.
44. Naito M, Suzuki H, Mori T, Matsumoto A, Kodama T, Takahashi K. Coexpression of type I and type II human macrophage scavenger receptors in macrophages of various organs and foam cells in atherosclerotic lesions. Am J Pathol. 1992;141:591-599.
45. Li H, Freeman MW, Libby P. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. J Clin Invest. 1995;95:122-133.
46. Geng YJ, Kodama T, Hansson GK. Differential expression of scavenger receptor isoforms during monocyte-macrophage differentiation and foam cell formation. Arterioscler Thromb. 1994;14:798-806.
47. Suzuki H, Kurihara Y, Takeya M, Kamada N, Kataoka M, Jishage K, Ueda O, Sakaguchi H, Higashi T, Suzuki T, Takashima Y, Kawabe Y, Cynshi O, Wada Y, Honda M, Kurihara H, Aburatani H, Doi T, Matsumoto A, Azuma S, Noda T, Toyoda Y, Itakura H, Yazaki Y, Horiuchi S, Takahashi K, Kruijt JK, van Berkel TJC, Steinbrecher UP, Ishibashi S, Maeda N, Gordon S, Kodama T. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 1997;386:292-296.
48. Ylä-Herttuala S, Jaakkola O, Ehnholm C, Tikkanen MJ, Solakivi T, Särkioja T, Nikkari T. Characterization of two lipoproteins containing apolipoproteiris B and E from lesion-free human aortic intima. J Lipid Res. 1988;29:563-572.
49. Rapp JH, Lespine A, Hamilton RL, Colyvas N, Chaumeton AH, Tweedie-Hardman J, Kotite L, Kunitake ST, Havel RJ, Kane JP. Triglyceride-rich lipoproteins isolated by selected-affinity antiapolipoprotein B immunosorption from human atherosclerotic plaque. Arterioscler Thromb. 1994;14:1767-1774.
50. Ylä-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S, Carew TE, Butler S, Witztum JL, Steinberg D. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest. 1989;84:1086-1095.
51. Beisiegel U, Weber W, Ihrke G, Herz J, Stanley KK. The LDL receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature. 1989;341:162-164.
52. Beisiegel U, Weber W, Bengtsson-Olivecrona G. Lipoprotein lipase enhances the binding of chylomicrons to low density lipoprotein receptor-related protein. Proc Natl Acad Sci U S A. 1991;88:8342-8346.
53. Takahashi S, Suzuki J, Kohno M, Oida K, Tamai T, Miyabo S, Yamamoto T, Nakai T. 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.
54. Salomon RN, Underwood R, Doyle MV, Wang A, Libby P. Increased apolipoprotein E and c-fms gene expression without elevated interleukin 1 or 6 mRN A levels indicates selective activation of macrophage functions in advanced human atheroma. Proc Natl Acad Sci U S A. 1992;89:2814-2818.
55. Rosenfeld ME, Butler S, Ord VA, Lipton BA, Dyer CA, Curtiss LK, Palinski W, Witztum JL. Abundant expression of apoprotein E by macrophages in human and rabbit atherosclerotic lesions. Arterioscler Thromb. 1993;13:1382-1389.
56. Ylä-Herttuala S, Lipton BA, Rosenfeld ME, Goldberg IJ, Steinberg D, Witztum JL. Macrophages and smooth muscle cells express lipoprotein lipase in human and rabbit atherosclerotic lesions. Proc Natl Acad Sci U S A. 1991;88:10143-10147.
57. Heegaard CW, Wiborg Simonsen AC, Oka K, Kjøller L, Christensen A, Madsen B, Ellgaard L, Chan L, Andreasen PA. Very low density lipoprotein receptor binds and mediates endocytosis of urokinase-type plasminogen activator-type-1 plasmmogen activator inhibitor complex. J Biol Chem. 1995;270:20855-20861.