Macrophage lipoprotein lipase modulates the development of atherosclerosis but not adiposity

Journal of Lipid Research

Volumn 54, Issue 4, 2013, Pages 1124-1134

  Takahashi, Manabu ^a   Yagyu, Hiroaki ^a   Tazoe, Fumiko ^a   Nagashima, Shuichi ^a   Ohshiro, Taichi ^a   Okada, Kenta ^a   Osuga, Jun Ichi ^a   Goldberg, Ira J ^b   Ishibashi, Shun ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Apolipoprotein E; CD36; Foam cell; Knockout mice

Indexed keywords

APOLIPOPROTEIN E; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; CHOLESTEROL ESTER; LIPOPROTEIN LIPASE; MESSENGER RNA; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CELL LEVEL; CONTROLLED STUDY; CRE LOXP GENE; DIET THERAPY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; EPIDIDYMIS FAT; FAT MASS; GENE; GENE EXPRESSION; GENE LOSS; GENE TARGETING; GENETIC ASSOCIATION; HYPERCHOLESTEROLEMIA; INCUBATION TIME; INFLAMMATION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OBESITY; PATHOGENESIS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; TREATMENT DURATION; WESTERN TYPE DIET;

ADIPOSITY; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOTTING, NORTHERN; CARNITINE O-PALMITOYLTRANSFERASE; LIPOPROTEIN LIPASE; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84875841604     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M035568     Document Type: Article

References (46)

1. Libby, P., Y. Okamoto, V. Z. Rocha, and E. Folco. 2010. Infl ammation in atherosclerosis: transition from theory to practice. Circ. J. 74 : 213-220.
2. Weisberg, S. P., D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante, Jr. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112 : 1796-1808.
3. Li, Y., R. F. Schwabe, T. DeVries-Seimon, P. M. Yao, M. C. Gerbod-Giannone, A. R. Tall, R. J. Davis, R. Flavell, D. A. Brenner, and I. Tabas. 2005. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-Alpha and interleukin-6: model of NF-kappaB-And map kinase-dependent infl ammation in advanced atherosclerosis. J. Biol. Chem. 280 : 21763-21772.
4. Erbay, E., V. R. Babaev, J. R. Mayers, L. Makowski, K. N. Charles, M. E. Snitow, S. Fazio, M. M. Wiest, S. M. Watkins, M. F. Linton, et al. 2009. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 15 : 1383-1391.
5. Fessler, M. B., L. L. Rudel, and J. M. Brown. 2009. Toll-like receptor signaling links dietary fatty acids to the metabolic syndrome. Curr. Opin. Lipidol. 20 : 379-385.
6. Suganami, T., J. Nishida, and Y. Ogawa. 2005. A paracrine loop between adipocytes and macrophages aggravates infl ammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler. Thromb. Vasc. Biol. 25 : 2062-2068.
7. Xu, H., G. T. Barnes, Q. Yang, G. Tan, D. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia, et al. 2003. Chronic infl ammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112 : 1821-1830.
8. Voss, C. V., B. S. Davies, S. Tat, P. Gin, L. G. Fong, C. Pelletier, C. D. Mottler, A. Bensadoun, A. P. Beigneux, and S. G. Young. 2011. Mutations in lipoprotein lipase that block binding to the endothelial cell transporter GPIHBP1. Proc. Natl. Acad. Sci. USA. 108 : 7980-7984.
9. Goldberg, I. J. 1996. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J. Lipid Res. 37 : 693-707.
10. Santamarina-Fojo, S., and K. A. Dugi. 1994. Structure, function and role of lipoprotein lipase in lipoprotein metabolism. Curr. Opin. Lipidol. 5 : 117-125.
11. Shimada, M., S. Ishibashi, T. Inaba, H. Yagyu, K. Harada, J. I. Osuga, K. Ohashi, Y. Yazaki, and N. Yamada. 1996. Suppression of diet-induced atherosclerosis in low density lipoprotein receptor knockout mice overexpressing lipoprotein lipase. Proc. Natl. Acad. Sci. USA. 93 : 7242-7246.
12. Yagyu, H., S. Ishibashi, Z. Chen, J. Osuga, M. Okazaki, S. Perrey, T. Kitamine, M. Shimada, K. Ohashi, K. Harada, et al. 1999. Overexpressed lipoprotein lipase protects against atherosclerosis in apolipoprotein E knockout mice. J. Lipid Res. 40 : 1677-1685.
13. Tsutsumi, K., Y. Inoue, A. Shima, K. Iwasaki, M. Kawamura, and T. Murase. 1993. The novel compound NO-1886 increases lipoprotein lipase activity with resulting elevation of high density lipoprotein cholesterol, and long-term administration inhibits atherogenesis in the coronary arteries of rats with experimental atherosclerosis. J. Clin. Invest. 92 : 411-417.
14. Tsutsumi, K., Y. Inoue, A. Shima, and T. Murase. 1995. Correction of hypertriglyceridemia with low high-density lipoprotein cholesterol by the novel compound NO-1886, a lipoprotein lipase-promoting agent, in STZ-induced diabetic rats. Diabetes. 44 : 414-417.
15. Beisiegel, U. 1996. New aspects on the role of plasma lipases in lipoprotein catabolism and atherosclerosis. Atherosclerosis. 124 : 1-8.
16. Ishibashi, S., N. Yamada, H. Shimano, N. Mori, H. Mokuno, T. Gotohda, M. Kawakami, T. Murase, and F. Takaku. 1990. Apolipoprotein E and lipoprotein lipase secreted from human monocyte-derived macrophages modulate very low density lipoprotein uptake. J. Biol. Chem. 265 : 3040-3047.
17. Babaev, V. R., S. Fazio, L. A. Gleaves, K. J. Carter, C. F. Semenkovich, and M. F. Linton. 1999. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in vivo. J. Clin. Invest. 103 : 1697-1705.
18. Van Eck, M., R. Zimmermann, P. H. Groot, R. Zechner, and T. J. Van Berkel. 2000. Role of macrophage-derived lipoprotein lipase in lipoprotein metabolism and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 20 : E53-E62.
19. Linton, M. F., and S. Fazio. 1999. Macrophages, lipoprotein metabolism, and atherosclerosis: insights from murine bone marrow transplantation studies. Curr. Opin. Lipidol. 10 : 97-105.
20. Weinstock, P. H., S. Levak-Frank, L. C. Hudgins, H. Radner, J. M. Friedman, R. Zechner, and J. L. Breslow. 1997. Lipoprotein lipase controls fatty acid entry into adipose tissue, but fat mass is preserved by endogenous synthesis in mice defi cient in adipose tissue lipoprotein lipase. Proc. Natl. Acad. Sci. USA. 94 : 10261-10266.
21. Augustus, A., H. Yagyu, G. Haemmerle, A. Bensadoun, R. K. Vikramadithyan, S. Y. Park, J. K. Kim, R. Zechner, and I. J. Goldberg. 2004. Cardiac-specifi c knock-out of lipoprotein lipase alters plasma lipoprotein triglyceride metabolism and cardiac gene expression. J. Biol. Chem. 279 : 25050-25057.
22. Clausen, B. E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Forster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8 : 265-277.
23. Yagyu, H., T. Kitamine, J. Osuga, R. Tozawa, Z. Chen, Y. Kaji, T. Oka, S. Perrey, Y. Tamura, K. Ohashi, et al. 2000. Absence of ACAT-1 attenuates atherosclerosis but causes dry eye and cutaneous xanthomatosis in mice with congenital hyperlipidemia. J. Biol. Chem. 275 : 21324-21330.
24. Usui, S., Y. Hara, S. Hosaki, and M. Okazaki. 2002. A new on-line dual enzymatic method for simultaneous quantifi cation of cholesterol and triglycerides in lipoproteins by HPLC. J. Lipid Res. 43 : 805-814.
25. Yagyu, H., G. Chen, M. Yokoyama, K. Hirata, A. Augustus, Y. Kako, T. Seo, Y. Hu, E. P. Lutz, M. Merkel, et al. 2003. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J. Clin. Invest. 111 : 419-426.
26. Hocquette, J. F., B. Graulet, and T. Olivecrona. 1998. Lipoprotein lipase activity and mRNA levels in bovine tissues. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 121 : 201-212.
27. Tangirala, R. K., E. M. Rubin, and W. Palinski. 1995. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-defi cient and apolipoprotein E-defi cient mice. J. Lipid Res. 36 : 2320-2328.
28. Paigen, B., A. Morrow, P. A. Holmes, D. Mitchell, and R. A. Williams. 1987. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 68 : 231-240.
29. Spann, N. J., L. X. Garmire, J. G. McDonald, D. S. Myers, S. B. Milne, N. Shibata, D. Reichart, J. N. Fox, I. Shaked, D. Heudobler, et al. 2012. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and infl ammatory responses. Cell. 151 : 138-152.
30. Babaev, V. R., M. B. Patel, C. F. Semenkovich, S. Fazio, and M. F. Linton. 2000. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptordefi cient mice. J. Biol. Chem. 275 : 26293-26299.
31. Olafsen, T., S. G. Young, B. S. Davies, A. P. Beigneux, V. E. Kenanova, C. Voss, G. Young, K. P. Wong, R. H. Barnes 2nd, Y. Tu, et al. 2010. Unexpected expression pattern for glycosylphosphatidylinositol-Anchored HDL-binding protein 1 (GPIHBP1) in mouse tissues revealed by positron emission tomography scanning. J. Biol. Chem. 285 : 39239-39248.
32. Beisiegel, U., W. Weber, and G. Bengtsson-Olivecrona. 1991. Lipoprotein lipase enhances the binding of chylomicrons to low density lipoprotein receptor-related protein. Proc. Natl. Acad. Sci. USA. 88 : 8342-8346.
33. Rumsey, S. C., J. C. Obunike, Y. Arad, R. J. Deckelbaum, and I. J. Goldberg. 1992. Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fi broblasts and macrophages. J. Clin. Invest. 90 : 1504-1512.
34. Tabas, I., Y. Li, R. W. Brocia, S. W. Xu, T. L. Swenson, and K. J. Williams. 1993. 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. 268 : 20419-20432.
35. Li, L., and G. Renier. 2007. Adipocyte-derived lipoprotein lipase induces macrophage activation and monocyte adhesion: role of fatty acids. Obesity (Silver Spring). 15 : 2595-2604.
36. Saraswathi, V., and A. H. Hasty. 2006. The role of lipolysis in mediating the proinfl ammatory effects of very low density lipoproteins in mouse peritoneal macrophages. J. Lipid Res. 47 : 1406-1415.
37. Febbraio, M., E. A. Podrez, J. D. Smith, D. P. Hajjar, S. L. Hazen, H. F. Hoff, K. Sharma, and R. L. Silverstein. 2000. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105 : 1049-1056.
38. Marleau, S., D. Harb, K. Bujold, R. Avallone, K. Iken, Y. Wang, A. Demers, M. G. Sirois, M. Febbraio, R. L. Silverstein, et al. 2005. EP 80317, a ligand of the CD36 scavenger receptor, protects apolipoprotein E-defi cient mice from developing atherosclerotic lesions. FASEB J. 19 : 1869-1871.
39. Moore, K. J., V. V. Kunjathoor, S. L. Koehn, J. J. Manning, A. A. Tseng, J. M. Silver, M. McKee, and M. W. Freeman. 2005. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J. Clin. Invest. 115 : 2192-2201.
40. Coburn, C. T., F. F. Knapp, Jr. ., M. Febbraio, A. L. Beets, R. L. Silverstein, and N. A. Abumrad. 2000. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J. Biol. Chem. 275 : 32523-32529.
41. Ricote, M., J. S. Welch, and C. K. Glass. 2000. Regulation of macrophage gene expression by the peroxisome proliferator-Activated receptor-gamma. Horm. Res. 54 : 275-280.
42. Chandak, P. G., B. Radovic, E. Afl aki, D. Kolb, M. Buchebner, E. Frohlich, C. Magnes, F. Sinner, G. Haemmerle, R. Zechner, et al. 2010. Effi cient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase. J. Biol. Chem. 285 : 20192-20201.
43. Yin, B., J. D. Loike, Y. Kako, P. H. Weinstock, J. L. Breslow, S. C. Silverstein, and I. J. Goldberg. 1997. Lipoprotein lipase regulates Fc receptor-mediated phagocytosis by macrophages maintained in glucose-defi cient medium. J. Clin. Invest. 100 : 649-657.
44. Schrijvers, D. M., G. R. De Meyer, A. G. Herman, and W. Martinet. 2007. Phagocytosis in atherosclerosis: molecular mechanisms and implications for plaque progression and stability. Cardiovasc. Res. 73 : 470-480.
45. Thorp, E., D. Cui, D. M. Schrijvers, G. Kuriakose, and I. Tabas. 2008. Mertk receptor mutation reduces efferocytosis effi ciency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/-mice. Arterioscler. Thromb. Vasc. Biol. 28 : 1421-1428.
46. Ostlund-Lindqvist, A. M., S. Gustafson, P. Lindqvist, J. L. Witztum, and J. A. Little. 1983. Uptake and degradation of human chylomicrons by macrophages in culture. Role of lipoprotein lipase. Arteriosclerosis. 3 : 433-440.