Macrophage low-density lipoprotein receptor-related protein deficiency enhances atherosclerosis in apoE/LDLR double knockout mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 26, Issue 12, 2006, Pages 2710-2715

  Hu, L ^a   Boesten, L S M ^a,b   May, P ^c   Herz, J ^d   Bovenschen, N ^e   Huisman, M V ^a   Berbee J F P ^a   Havekes, L M ^a,b   Van Vlijmen, B J M ^a   Tamsma, J T ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TNO   (Netherlands)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Atherosclerosis; Collagen; Genetically altered mice; LRP; Macrophage

Indexed keywords

APOLIPOPROTEIN E; CD3 ANTIGEN; CHOLESTEROL; COLLAGEN; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ROOT; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL COUNT; CHOLESTEROL BLOOD LEVEL; CONTROL GROUP; CONTROLLED STUDY; FEMALE; GENE DELETION; IN VIVO STUDY; KNOCKOUT MOUSE; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; OBSERVATION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; COLLAGEN; FEMALE; GENE EXPRESSION REGULATION; LDL-RECEPTOR RELATED PROTEIN 1; LIPOPROTEINS; MACROPHAGES; MICE; MICE, KNOCKOUT; RECEPTORS, LDL;

EID: 33751194412     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000249641.96896.e6     Document Type: Article

References (35)

1. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
2. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
3. Degryse B, Neels JG, Czekay RP, Aertgeerts K, Kamikubo Y, Loskutoff DJ. The Low Density Lipoprotein Receptor-related Protein Is a Motogenic Receptor for Plasminogen Activator Inhibitor-1. J Biol Chem. 2004;279:22595-22604.
4. Rohlmann A, Gotthardt M, Hammer RE, Herz J. Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest. 1998;101:689-695.
5. Van Vlijmen BJ, Rohlmann A, Page ST, Bensadoun A, Bos IS, van Berkel TJ, Havekes LM, Herz J. An extrahepatic receptor-associated protein-sensitive mechanism is involved in the metabolism of triglyceride-rich lipoproteins. J Biol Chem. 1999;274:35219-35226.
6. 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.
7. Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science. 2003;300:329-332.
8. Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, Stockinger W, Nimpf J, Herz J. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J Biol Chem. 2000;275:25616-25624.
9. Herz J, Strickland DK. LRP: a multifunctional scavenger and signaling receptor. J Clin Invest. 2001;108:779-784.
10. Lillis AP, Mikhailenko I, Strickland DK. Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability. J Thromb Haemost. 2005;3:1884-1893.
11. Moestrup SK, Gliemann J, Pallesen G. Distribution of the alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein in human tissues. Cell Tissue Res. 1992;269:375-382.
12. Espirito Santo SM, Pires NM, Boesten LS, Gerritsen G, Bovenschen N, Van Dijk KW, Jukema JW, Princen HM, Bensadoun A, Li WP, Herz J, Havekes LM, Van Vlijmen BJ. Hepatic low-density lipoprotein receptor-related protein deficiency in mice increases atherosclerosis independent of plasma cholesterol. Blood. 2004;103:3777-3782.
13. Luoma J, Hiltunen T, Sarkioja T, Moestrup SK, Gliemann J, Kodama T, Nikkari T, Yla-Herttuala S. Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein and scavenger receptor in human atherosclerotic lesions. J Clin Invest. 1994;93:2014-2021.
14. Watanabe Y, Inaba T, Shimano H, Gotoda T, Yamamoto K, Mokuno H, Sato H, Yazaki Y, Yamada N. Induction of LDL receptor-related protein during the differentiation of monocyte-macrophages. Possible involvement in the atherosclerotic process. Arterioscler Thromb. 1994;14:1000-1006.
15. Spijkers PP, Da Costa MP, Westein E, Gahmberg CG, Zwaginga JJ, Lenting PJ. LDL-Receptor related protein regulates {beta}2-integrin mediated leukocyte adhesion. Blood. 2004;105:170-177.
16. Zhu H, Takahashi Y, Xu W, Kawajiri H, Murakami T, Yamamoto M, Iseki S, Iwasaki T, Hattori H, Yoshimoto T. Low density lipoprotein receptor-related protein-mediated membrane translocation of 12/15-lipoxygenase is required for oxidation of low density lipoprotein by macrophages. J Biol Chem. 2003;278:13350-13355.
17. Xu W, Takahashi Y, Sakashita T, Iwasaki T, Hattori H, Yoshimoto T. Low density lipoprotein receptor-related protein is required for macrophage-mediated oxidation of low density lipoprotein by 12/15-lipoxygenase. J Biol Chem. 2001;276:36454-36459.
18. Llorente-Cortes V, Martinez-Gonzalez J, Badimon L. LDL receptor-related protein mediates uptake of aggregated LDL in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2000;20:1572-1579.
19. Kuchenhoff A, Harrach-Ruprecht B, Robenek H. Interaction of apo E-containing lipoproteins with the LDL receptor-related protein LRP. Am J Physiol. 1997;272:C369-C382.
20. Fujioka Y, Cooper AD, Fong LG. Multiple processes are involved in the uptake of chylomicron remnants by mouse peritoneal macrophages. J Lipid Res. 1998;39:2339-2349.
21. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8:265-277.
22. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258:468-471.
23. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest. 1993;92:883-893.
24. Sambrook J, Fritsch E, Maniatis T. Molecular cloning: a laboratory manual, 2nd Edition. Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press; 1989.
25. Boesten LS, Zadelaar AS, van Nieuwkoop A, Gijbels MJ, de Winther MP, Havekes LM, Van Vlijmen BJ. Tumor necrosis factor-alpha promotes atherosclerotic lesion progression in APOE*3-Leiden transgenic mice. Cardiovasc Res. 2005;66:179-185.
26. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987;68:231-240.
27. Van Vlijmen BJ, van den Maagdenberg AM, Gijbels MJ, van der BH, HogenEsch H, Frants RR, Hofker MH, Havekes LM. Diet-induced hyperlipoproteinemia and atherosclerosis in apolipoprotein E3-Leiden transgenic mice. J Clin Invest. 1994;93:1403-1410.
28. Lijnen HR. Metalloproteinases in development and progression of vascular disease. Pathophysiol Haemost Thromb. 2003;33:275-281.
29. Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler Thromb. 1991;11:1223-1230.
30. Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, Stanley KK. 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.
31. Rezaee F, Gijbels M, Offerman E, Verheijen J. Genetic deletion of tissue-type plasminogen activator (t-PA) in APOE3-Leiden mice reduces progression of cholesterol-induced atherosclerosis. Thromb Haemost. 2003;90:710-716.
32. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D. Plasminogen activator inhibitor-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood. 2000;96:4212-4215.
33. Ananyeva NM, Kouiavskaia DV, Shima M, Saenko EL. Intrinsic pathway of blood coagulation contributes to thrombogenicity of atherosclerotic plaque. Blood. 2002;99:4475-4485.
34. Methia N, Andre P, Denis CV, Economopoulos M, Wagner DD. Localized reduction of atherosclerosis in von Willebrand factor-deficient mice. Blood. 2001;98:1424-1428.
35. Steins MB, Padro T, Li CX, Mesters RM, Ostermann H, Hammel D, Scheld HH, Berdel WE, Kienast J. Overexpression of tissue-type plasminogen activator in atherosclerotic human coronary arteries. Atherosclerosis. 1999;145:173-180.