Overexpression of angiopoietin-like protein 4 protects against atherosclerosis development

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 7, 2013, Pages 1529-1537

  Georgiadi, Anastasia ^a   Wang, Yanan ^b   Stienstra, Rinke ^a,c   Tjeerdema, Nathanja ^b   Janssen, Aafke ^a   Stalenhoef, Anton ^c   Van Der Vliet, J Adam ^c   De Roos, Albert ^b   Tamsma, Jouke T ^b   Smit, Johannes W A ^b,c   Tan, Nguan Soon ^d   Müller, Michael ^a   Rensen, Patrick C N ^b   Kersten, Sander ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Atherosclerosis; Inflammation; Lipoprotein lipase; Lipoproteins; Macrophages

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE PROTEIN 4; APOLIPOPROTEIN E; OXIDIZED LOW DENSITY LIPOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATHEROSCLEROSIS; CAROTID ARTERY; CELL ADHESION; CELL STIMULATION; CHOLESTEROL BLOOD LEVEL; DISEASE COURSE; FOAM CELL; LIPOLYSIS; MACROPHAGE ACTIVATION; MESENTERY LYMPH NODE; METABOLIC SYNDROME X; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM;

ATHEROSCLEROSIS; INFLAMMATION; LIPOPROTEIN LIPASE; LIPOPROTEINS; MACROPHAGES;

ANGIOPOIETINS; ANIMALS; AORTA; AORTIC DISEASES; APOLIPOPROTEIN E3; ATHEROSCLEROSIS; CAROTID ARTERIES; CAROTID STENOSIS; CELL LINE; CHEMOTAXIS; CHOLESTEROL; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; FOAM CELLS; HUMANS; LIGANDS; LIPOPROTEINS, LDL; MACROPHAGE ACTIVATION; MACROPHAGES; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; TIME FACTORS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TRIGLYCERIDES; UP-REGULATION;

EID: 84879104907     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301698     Document Type: Article

References (39)

1. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145:341-355.
2. Steinberg D. Thematic review series: the pathogenesis of atherosclerosis: an interpretive history of the cholesterol controversy, part III: mechanistically defining the role of hyperlipidemia. J Lipid Res. 2005;46:2037-2051.
3. Boven LA, Van Meurs M, Van Zwam M, Wierenga-Wolf A, Hintzen RQ, Boot RG, Aerts JM, Amor S, Nieuwenhuis EE, Laman JD. Myelin-laden macrophages are anti-inflammatory, consistent with foam cells in multiple sclerosis. Brain. 2006;129(pt 2):517-526.
4. Prieur X, Mok CY, Velagapudi VR, Núñez V, Fuentes L, Montaner D, Ishikawa K, Camacho A, Barbarroja N, O'Rahilly S, Sethi JK, Dopazo J, Orešič M, Ricote M, Vidal-Puig A. Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice. Diabetes. 2011;60:797-809.
5. Bieghs V, Wouters K, van Gorp PJ, Gijbels MJ, de Winther MP, Binder CJ, Lütjohann D, Febbraio M, Moore KJ, van Bilsen M, Hofker MH, Shiri-Sverdlov R. Role of scavenger receptor A and CD36 in diet-induced nonalcoholic steatohepatitis in hyperlipidemic mice. Gastroenterology. 2010;138:2477-2486, 2486.e1.
6. Keane WF, Kasiske BL, O'Donnell MP. Lipids and progressive glomerulosclerosis. A model analogous to atherosclerosis. Am J Nephrol. 1988;8:261-271.
7. Rahman EU, Ruan XZ, Chana RS, Brunskill NJ, Gaya J, Powis SH, Varghese Z, Moorhead JF, Wheeler DC. Mesangial matrix-activated monocytes express functional scavenger receptors and accumulate intracellular lipid. Nephrol Dial Transplant. 2008;23:1876-1885.
8. Lichtenstein L, Mattijssen F, de Wit NJ, Georgiadi A, Hooiveld GJ, van der Meer R, He Y, Qi L, Köster A, Tamsma JT, Tan NS, Müller M, Kersten S. Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab. 2010;12:580-592.
9. Wang H, Eckel RH. Lipoprotein lipase: from gene to obesity. Am J Physiol Endocrinol Metab. 2009;297:E271-E288.
10. Lichtenstein L, Berbée JF, van Dijk SJ, van Dijk KW, Bensadoun A, Kema IP, Voshol PJ, Müller M, Rensen PC, Kersten S. Angptl4 upregulates cholesterol synthesis in liver via inhibition of LPL-and HL-dependent hepatic cholesterol uptake. Arterioscler Thromb Vasc Biol. 2007;27:2420-2427.
11. Sukonina V, Lookene A, Olivecrona T, Olivecrona G. Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc Natl Acad Sci U S A. 2006;103:17450-17455.
12. Köster A, Chao YB, Mosior M, Ford A, Gonzalez-DeWhitt PA, Hale JE, Li D, Qiu Y, Fraser CC, Yang DD, Heuer JG, Jaskunas SR, Eacho P. Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology. 2005;146:4943-4950.
13. Mandard S, Zandbergen F, van Straten E, Wahli W, Kuipers F, Müller M, Kersten S. The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem. 2006;281:934-944.
14. Xu A, Lam MC, Chan KW, Wang Y, Zhang J, Hoo RL, Xu JY, Chen B, Chow WS, Tso AW, Lam KS. Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc Natl Acad Sci U S A. 2005;102:6086-6091.
15. Yu X, Burgess SC, Ge H, Wong KK, Nassem RH, Garry DJ, Sherry AD, Malloy CR, Berger JP, Li C. Inhibition of cardiac lipoprotein utilization by transgenic overexpression of Angptl4 in the heart. Proc Natl Acad Sci U S A. 2005;102:1767-1772.
16. Lichtenstein L, Kersten S. Modulation of plasma TG lipolysis by angiopoietin-like proteins and GPIHBP1. Biochim Biophys Acta. 2010;1801:415-420.
17. 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;103:1697-1705.
18. Babaev VR, Patel MB, Semenkovich CF, Fazio S, Linton MF. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptor-deficient mice. J Biol Chem. 2000;275:26293-26299.
19. van Vlijmen BJ, van den Maagdenberg AM, Gijbels MJ, van der Boom H, 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.
20. Delerive P, Furman C, Teissier E, Fruchart J, Duriez P, Staels B. Oxidized phospholipids activate PPARalpha in a phospholipase A2-dependent manner. FEBS Lett. 2000;471:34-38.
21. Nagy L, Tontonoz P, Alvarez JG, Chen H, Evans RM. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell. 1998;93:229-240.
22. Vosper H, Patel L, Graham TL, Khoudoli GA, Hill A, Macphee CH, Pinto I, Smith SA, Suckling KE, Wolf CR, Palmer CN. The peroxisome proliferator-activated receptor delta promotes lipid accumulation in human macrophages. J Biol Chem. 2001;276:44258-44265.
23. Gianturco SH, Bradley WA, Gotto AM Jr., Morrisett JD, Peavy DL. Hypertriglyceridemic very low density lipoproteins induce triglyceride synthesis and accumulation in mouse peritoneal macrophages. J Clin Invest. 1982;70:168-178.
24. Ishiyama J, Taguchi R, Akasaka Y, Shibata S, Ito M, Nagasawa M, Murakami K. Unsaturated FAs prevent palmitate-induced LOX-1 induction via inhibition of ER stress in macrophages. J Lipid Res. 2011;52:299-307.
25. Saraswathi V, Hasty AH. The role of lipolysis in mediating the proinflammatory effects of very low density lipoproteins in mouse peritoneal macrophages. J Lipid Res. 2006;47:1406-1415.
26. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, Tontonoz P. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell. 2001;7:161-171.
27. van den Maagdenberg AM, Hofker MH, Krimpenfort PJ, de Bruijn I, van Vlijmen B, van der Boom H, Havekes LM, Frants RR. Transgenic mice carrying the apolipoprotein E3-Leiden gene exhibit hyperlipoproteinemia. J Biol Chem. 1993;268:10540-10545.
28. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res. 2004;95:858-866.
29. Han KH, Chang MK, Boullier A, Green SR, Li A, Glass CK, Quehenberger O. Oxidized LDL reduces monocyte CCR2 expression through pathways involving peroxisome proliferator-activated receptor gamma. J Clin Invest. 2000;106:793-802.
30. Adachi H, Fujiwara Y, Kondo T, et al. Angptl 4 deficiency improves lipid metabolism, suppresses foam cell formation and protects against atherosclerosis. Biochem Biophys Res Commun. 2009;379:806-811.
31. Nilsson SK, Anderson F, Ericsson M, Larsson M, Makoveichuk E, Lookene A, Heeren J, Olivecrona G. Triacylglycerol-rich lipoproteins protect lipoprotein lipase from inactivation by ANGPTL3 and ANGPTL4. Biochim Biophys Acta. 2012;1821:1370-1378.
32. Hendriks WL, van der Boom H, van Vark LC, Havekes LM. Lipoprotein lipase stimulates the binding and uptake of moderately oxidized low-density lipoprotein by J774 macrophages. Biochem J. 1996;314 (pt 2):563-568.
33. Ichikawa T, Liang J, Kitajima S, Koike T, Wang X, Sun H, Morimoto M, Shikama H, Watanabe T, Yamada N, Fan J. Macrophage-derived lipoprotein lipase increases aortic atherosclerosis in cholesterol-fed Tg rabbits. Atherosclerosis. 2005;179:87-95.
34. Wilson K, Fry GL, Chappell DA, Sigmund CD, Medh JD. Macrophagespecific expression of human lipoprotein lipase accelerates atherosclerosis in transgenic apolipoprotein e knockout mice but not in C57BL/6 mice. Arterioscler Thromb Vasc Biol. 2001;21:1809-1815.
35. Takahashi M, Yagyu H, Tazoe F, Nagashima S, Ohshiro T, Okada K, Osuga J, Goldberg IJ, Ishibashi S. Macrophage lipoprotein lipase modulates the development of atherosclerosis but not adiposity. J Lipid Res. 2013;54:1124-1134.
36. Van Eck M, Zimmermann R, Groot PH, Zechner R, Van Berkel TJ. Role of macrophage-derived lipoprotein lipase in lipoprotein metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol. 2000;20:E53-E62.
37. Gustafsson M, Levin M, Skålén K, Perman J, Fridén V, Jirholt P, Olofsson SO, Fazio S, Linton MF, Semenkovich CF, Olivecrona G, Borén J. Retention of low-density lipoprotein in atherosclerotic lesions of the mouse: evidence for a role of lipoprotein lipase. Circ Res. 2007;101:777-783.
38. Miller YI, Viriyakosol S, Worrall DS, Boullier A, Butler S, Witztum JL. Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Biol. 2005;25:1213-1219.
39. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11:155-161.