Regulation of triglyceride metabolism by Angiopoietin-like proteins

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 5, 2012, Pages 782-789

  Mattijssen, Frits ^a   Kersten, Sander ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Angiopoietin like proteins; Lipoprotein lipase; PPARs; Triglycerides

Indexed keywords

ANGIOPOIETIN; LIPOPROTEIN LIPASE; LIVER X RECEPTOR; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; TRIACYLGLYCEROL;

CELL PROTECTION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME INHIBITION; FATTY ACID METABOLISM; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HUMAN; HYPERTRIGLYCERIDEMIA; LIPID METABOLISM; LIPOPROTEIN METABOLISM; LIPOTOXICITY; MISSENSE MUTATION; NONHUMAN; OBESITY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION REGULATION; TRIACYLGLYCEROL BLOOD LEVEL;

ANGIOPOIETINS; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; LIPOPROTEIN LIPASE; LIPOPROTEINS, VLDL; LIVER; MICE; MICE, KNOCKOUT; TRIGLYCERIDES;

MUS;

EID: 84859161516     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2011.10.010     Document Type: Review

References (85)

1. M. Tabata, T. Kadomatsu, S. Fukuhara, K. Miyata, Y. Ito, M. Endo, T. Urano, H.J. Zhu, H. Tsukano, H. Tazume, K. Kaikita, K. Miyashita, T. Iwawaki, M. Shimabukuro, K. Sakaguchi, T. Ito, N. Nakagata, T. Yamada, H. Katagiri, M. Kasuga, Y. Ando, H. Ogawa, N. Mochizuki, H. Itoh, T. Suda, and Y. Oike Angiopoietin-like protein 2 promotes chronic adipose tissue inflammation and obesity-related systemic insulin resistance Cell Metab. 10 2009 178 188
2. M. Kitazawa, M. Nagano, K.H. Masumoto, Y. Shigeyoshi, T. Natsume, and S. Hashimoto Angiopoietin-like 2, a circadian gene, improves type 2 diabetes through potentiation of insulin sensitivity in mice adipocytes Endocrinology 152 2011 2558 2567
3. C.J. Willer, S. Sanna, A.U. Jackson, A. Scuteri, L.L. Bonnycastle, R. Clarke, S.C. Heath, N.J. Timpson, S.S. Najjar, H.M. Stringham, J. Strait, W.L. Duren, A. Maschio, F. Busonero, A. Mulas, G. Albai, A.J. Swift, M.A. Morken, N. Narisu, D. Bennett, S. Parish, H. Shen, P. Galan, P. Meneton, S. Hercberg, D. Zelenika, W.M. Chen, Y. Li, L.J. Scott, P.A. Scheet, J. Sundvall, R.M. Watanabe, R. Nagaraja, S. Ebrahim, D.A. Lawlor, Y. Ben-Shlomo, G. Davey-Smith, A.R. Shuldiner, R. Collins, R.N. Bergman, M. Uda, J. Tuomilehto, A. Cao, F.S. Collins, E. Lakatta, G.M. Lathrop, M. Boehnke, D. Schlessinger, K.L. Mohlke, and G.R. Abecasis Newly identified loci that influence lipid concentrations and risk of coronary artery disease Nat. Genet. 40 2008 161 169
4. S. Kathiresan, O. Melander, C. Guiducci, A. Surti, N.P. Burtt, M.J. Rieder, G.M. Cooper, C. Roos, B.F. Voight, A.S. Havulinna, B. Wahlstrand, T. Hedner, D. Corella, E.S. Tai, J.M. Ordovas, G. Berglund, E. Vartiainen, P. Jousilahti, B. Hedblad, M.R. Taskinen, C. Newton-Cheh, V. Salomaa, L. Peltonen, L. Groop, D.M. Altshuler, and M. Orho-Melander Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans Nat. Genet. 40 2008 189 197
5. S. Kathiresan, C.J. Willer, G.M. Peloso, S. Demissie, K. Musunuru, E.E. Schadt, L. Kaplan, D. Bennett, Y. Li, T. Tanaka, B.F. Voight, L.L. Bonnycastle, A.U. Jackson, G. Crawford, A. Surti, C. Guiducci, N.P. Burtt, S. Parish, R. Clarke, D. Zelenika, K.A. Kubalanza, M.A. Morken, L.J. Scott, H.M. Stringham, P. Galan, A.J. Swift, J. Kuusisto, R.N. Bergman, J. Sundvall, M. Laakso, L. Ferrucci, P. Scheet, S. Sanna, M. Uda, Q. Yang, K.L. Lunetta, J. Dupuis, P.I. de Bakker, C.J. O'Donnell, J.C. Chambers, J.S. Kooner, S. Hercberg, P. Meneton, E.G. Lakatta, A. Scuteri, D. Schlessinger, J. Tuomilehto, F.S. Collins, L. Groop, D. Altshuler, R. Collins, G.M. Lathrop, O. Melander, V. Salomaa, L. Peltonen, M. Orho-Melander, J.M. Ordovas, M. Boehnke, G.R. Abecasis, K.L. Mohlke, and L.A. Cupples Common variants at 30 loci contribute to polygenic dyslipidemia Nat. Genet. 41 2009 56 65
6. R.A. Hegele, M.R. Ban, N. Hsueh, B.A. Kennedy, H. Cao, G.Y. Zou, S. Anand, S. Yusuf, M.W. Huff, and J. Wang A polygenic basis for four classical Fredrickson hyperlipoproteinemia phenotypes that are characterized by hypertriglyceridemia Hum. Mol. Genet. 18 2009 4189 4194
7. T.M. Teslovich, K. Musunuru, A.V. Smith, A.C. Edmondson, I.M. Stylianou, M. Koseki, J.P. Pirruccello, S. Ripatti, D.I. Chasman, C.J. Willer, C.T. Johansen, S.W. Fouchier, A. Isaacs, G.M. Peloso, M. Barbalic, S.L. Ricketts, J.C. Bis, Y.S. Aulchenko, G. Thorleifsson, M.F. Feitosa, J. Chambers, M. Orho-Melander, O. Melander, T. Johnson, X. Li, X. Guo, M. Li, Y. Shin Cho, M. Jin Go, Y. Jin Kim, J.Y. Lee, T. Park, K. Kim, X. Sim, R. Twee-Hee Ong, D.C. Croteau-Chonka, L.A. Lange, J.D. Smith, K. Song, J. Hua Zhao, X. Yuan, J. Luan, C. Lamina, A. Ziegler, W. Zhang, R.Y. Zee, A.F. Wright, J.C. Witteman, J.F. Wilson, G. Willemsen, H.E. Wichmann, J.B. Whitfield, D.M. Waterworth, N.J. Wareham, G. Waeber, P. Vollenweider, B.F. Voight, V. Vitart, A.G. Uitterlinden, M. Uda, J. Tuomilehto, J.R. Thompson, T. Tanaka, I. Surakka, H.M. Stringham, T.D. Spector, N. Soranzo, J.H. Smit, J. Sinisalo, K. Silander, E.J. Sijbrands, A. Scuteri, J. Scott, D. Schlessinger, S. Sanna, V. Salomaa, J. Saharinen, C. Sabatti, A. Ruokonen, I. Rudan, L.M. Rose, R. Roberts, M. Rieder, B.M. Psaty, P.P. Pramstaller, I. Pichler, M. Perola, B.W. Penninx, N.L. Pedersen, C. Pattaro, A.N. Parker, G. Pare, B.A. Oostra, C.J. O'Donnell, M.S. Nieminen, D.A. Nickerson, G.W. Montgomery, T. Meitinger, R. McPherson, M.I. McCarthy, W. McArdle, D. Masson, N.G. Martin, F. Marroni, M. Mangino, P.K. Magnusson, G. Lucas, R. Luben, R.J. Loos, M.L. Lokki, G. Lettre, C. Langenberg, L.J. Launer, E.G. Lakatta, R. Laaksonen, K.O. Kyvik, F. Kronenberg, I.R. Konig, K.T. Khaw, J. Kaprio, L.M. Kaplan, A. Johansson, M.R. Jarvelin, A.C. Janssens, E. Ingelsson, W. Igl, G. Kees Hovingh, J.J. Hottenga, A. Hofman, A.A. Hicks, C. Hengstenberg, I.M. Heid, C. Hayward, A.S. Havulinna, N.D. Hastie, T.B. Harris, T. Haritunians, A.S. Hall, U. Gyllensten, C. Guiducci, L.C. Groop, E. Gonzalez, C. Gieger, N.B. Freimer, L. Ferrucci, J. Erdmann, P. Elliott, K.G. Ejebe, A. Doring, A.F. Dominiczak, S. Demissie, P. Deloukas, E.J. de Geus, U. de Faire, G. Crawford, F.S. Collins, Y.D. Chen, M.J. Caulfield, H. Campbell, N.P. Burtt, L.L. Bonnycastle, D.I. Boomsma, S.M. Boekholdt, R.N. Bergman, I. Barroso, S. Bandinelli, C.M. Ballantyne, T.L. Assimes, T. Quertermous, D. Altshuler, M. Seielstad, T.Y. Wong, E.S. Tai, A.B. Feranil, C.W. Kuzawa, L.S. Adair, H.A. Taylor Jr., I.B. Borecki, S.B. Gabriel, J.G. Wilson, H. Holm, U. Thorsteinsdottir, V. Gudnason, R.M. Krauss, K.L. Mohlke, J.M. Ordovas, P.B. Munroe, J.S. Kooner, A.R. Tall, R.A. Hegele, J.J. Kastelein, E.E. Schadt, J.I. Rotter, E. Boerwinkle, D.P. Strachan, V. Mooser, K. Stefansson, M.P. Reilly, N.J. Samani, H. Schunkert, L.A. Cupples, M.S. Sandhu, P.M. Ridker, D.J. Rader, C.M. van Duijn, L. Peltonen, G.R. Abecasis, M. Boehnke, and S. Kathiresan Biological, clinical and population relevance of 95 loci for blood lipids Nature 466 2010 707 713
8. A. Angelakopoulou, T. Shah, R. Sofat, S. Shah, D.J. Berry, J. Cooper, J. Palmen, I. Tzoulaki, A. Wong, B.J. Jefferis, N. Maniatis, F. Drenos, B. Gigante, R. Hardy, R.C. Laxton, K. Leander, A. Motterle, I.A. Simpson, L. Smeeth, A. Thomson, C. Verzilli, D. Kuh, H. Ireland, J. Deanfield, M. Caulfield, C. Wallace, N. Samani, P.B. Munroe, M. Lathrop, F.G. Fowkes, M. Marmot, P.H. Whincup, J.C. Whittaker, U. de Faire, M. Kivimaki, M. Kumari, E. Hypponen, C. Power, S.E. Humphries, P.J. Talmud, J. Price, R.W. Morris, S. Ye, J.P. Casas, and A.D. Hingorani Comparative analysis of genome-wide-association studies signals for lipids, diabetes, and coronary heart disease: Cardiovascular Biomarker Genetics Collaboration Eur. Heart J. 2011 [Electronic publication ahead of print]
9. S. Romeo, W. Yin, J. Kozlitina, L.A. Pennacchio, E. Boerwinkle, H.H. Hobbs, and J.C. Cohen Rare loss-of-function mutations in ANGPTL family members contribute to plasma triglyceride levels in humans J. Clin. Invest. 119 2009 70 79
10. K. Musunuru, J.P. Pirruccello, R. Do, G.M. Peloso, C. Guiducci, C. Sougnez, K.V. Garimella, S. Fisher, J. Abreu, A.J. Barry, T. Fennell, E. Banks, L. Ambrogio, K. Cibulskis, A. Kernytsky, E. Gonzalez, N. Rudzicz, J.C. Engert, M.A. DePristo, M.J. Daly, J.C. Cohen, H.H. Hobbs, D. Altshuler, G. Schonfeld, S.B. Gabriel, P. Yue, and S. Kathiresan Exome sequencing, ANGPTL3 mutations, and familial combined hypolipidemia N. Engl. J. Med. 363 2010 2220 2227
11. S. Hatsuda, T. Shoji, K. Shinohara, E. Kimoto, K. Mori, S. Fukumoto, H. Koyama, M. Emoto, and Y. Nishizawa Association between plasma angiopoietin-like protein 3 and arterial wall thickness in healthy subjects J. Vasc. Res. 44 2007 61 66
12. M. Shimamura, M. Matsuda, H. Yasumo, M. Okazaki, K. Fujimoto, K. Kono, T. Shimizugawa, Y. Ando, R. Koishi, T. Kohama, N. Sakai, K. Kotani, R. Komuro, T. Ishida, K. Hirata, S. Yamashita, H. Furukawa, and I. Shimomura Angiopoietin-like protein3 regulates plasma HDL cholesterol through suppression of endothelial lipase Arterioscler. Thromb. Vasc. Biol. 27 2007 366 372
13. K. Nakajima, J. Kobayashi, H. Mabuchi, T. Nakano, Y. Tokita, T. Nagamine, S. Imamura, M. Ai, S. Otokozawa, and E.F. Schaefer Association of angiopoietin-like protein 3 with hepatic triglyceride lipase and lipoprotein lipase activities in human plasma Ann. Clin. Biochem. 47 2010 423 431
14. M.R. Robciuc, E. Tahvanainen, M. Jauhiainen, and C. Ehnholm Quantitation of serum angiopoietin-like proteins 3 and 4 in a Finnish population sample J. Lipid Res. 51 2010 824 831
15. R. Koishi, Y. Ando, M. Ono, M. Shimamura, H. Yasumo, T. Fujiwara, H. Horikoshi, and H. Furukawa Angptl3 regulates lipid metabolism in mice Nat. Genet. 30 2002 151 157
16. A. Koster, Y.B. Chao, M. Mosior, A. Ford, P.A. Gonzalez-DeWhitt, J.E. Hale, D. Li, Y. Qiu, C.C. Fraser, D.D. Yang, J.G. Heuer, S.R. Jaskunas, and P. Eacho Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism Endocrinology 146 2005 4943 4950
17. T. Shimizugawa, M. Ono, M. Shimamura, K. Yoshida, Y. Ando, R. Koishi, K. Ueda, T. Inaba, H. Minekura, T. Kohama, and H. Furukawa ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase J. Biol. Chem. 277 2002 33742 33748
18. M. Ono, T. Shimizugawa, M. Shimamura, K. Yoshida, C. Noji-Sakikawa, Y. Ando, R. Koishi, and H. Furukawa Protein region important for regulation of lipid metabolism in angiopoietin-like 3 (ANGPTL3): ANGPTL3 is cleaved and activated in vivo J. Biol. Chem. 278 2003 41804 41809
19. L. Shan, X.C. Yu, Z. Liu, Y. Hu, L.T. Sturgis, M.L. Miranda, and Q. Liu The angiopoietin-like proteins ANGPTL3 and ANGPTL4 inhibit lipoprotein lipase activity through distinct mechanisms J. Biol. Chem. 284 2009 1419 1424
20. J. Liu, H. Afroza, D.J. Rader, and W. Jin Angiopoietin-like protein 3 inhibits lipoprotein lipase activity through enhancing its cleavage by proprotein convertases J. Biol. Chem. 285 2010 27561 27570
21. W.K. Sonnenburg, D. Yu, E.C. Lee, W. Xiong, G. Gololobov, B. Key, J. Gay, N. Wilganowski, Y. Hu, S. Zhao, M. Schneider, Z.M. Ding, B.P. Zambrowicz, G. Landes, D.R. Powell, and U. Desai GPIHBP1 stabilizes lipoprotein lipase and prevents its inhibition by angiopoietin-like 3 and angiopoietin-like 4 J. Lipid Res. 50 2009 2421 2429
22. M.H. Yau, Y. Wang, K.S. Lam, J. Zhang, D. Wu, and A. Xu A highly conserved motif within the NH2-terminal coiled-coil domain of angiopoietin-like protein 4 confers its inhibitory effects on lipoprotein lipase by disrupting the enzyme dimerization J. Biol. Chem. 284 2009 11942 11952
23. W. Jin, X. Wang, J.S. Millar, T. Quertermous, G.H. Rothblat, J.M. Glick, and D.J. Rader Hepatic proprotein convertases modulate HDL metabolism Cell Metab. 6 2007 129 136
24. K.T. Schjoldager, M.B. Vester-Christensen, E.P. Bennett, S.B. Levery, T. Schwientek, W. Yin, O. Blixt, and H. Clausen O-glycosylation modulates proprotein convertase activation of angiopoietin-like protein 3: possible role of polypeptide GalNAc-transferase-2 in regulation of concentrations of plasma lipids J. Biol. Chem. 285 2010 36293 36303
25. H. Ge, J.Y. Cha, H. Gopal, C. Harp, X. Yu, J.J. Repa, and C. Li Differential regulation and properties of angiopoietin-like proteins 3 and 4 J. Lipid Res. 46 2005 1484 1490
26. R. Kaplan, T. Zhang, M. Hernandez, F.X. Gan, S.D. Wright, M.G. Waters, and T.Q. Cai Regulation of the angiopoietin-like protein 3 gene by LXR J. Lipid Res. 44 2003 136 143
27. T. Inaba, M. Matsuda, M. Shimamura, N. Takei, N. Terasaka, Y. Ando, H. Yasumo, R. Koishi, M. Makishima, and I. Shimomura Angiopoietin-like protein 3 mediates hypertriglyceridemia induced by the liver X receptor J. Biol. Chem. 278 2003 21344 21351
28. K. Matsusue, A. Miyoshi, S. Yamano, and F.J. Gonzalez Ligand-activated PPARbeta efficiently represses the induction of LXR-dependent promoter activity through competition with RXR Mol. Cell. Endocrinol. 256 2006 23 33
29. C. Pramfalk, P. Parini, U. Gustafsson, S. Sahlin, and M. Eriksson Effects of high-dose statin on the human hepatic expression of genes involved in carbohydrate and triglyceride metabolism J. Intern. Med. 269 2011 333 339
30. K. Inukai, Y. Nakashima, M. Watanabe, S. Kurihara, T. Awata, H. Katagiri, Y. Oka, and S. Katayama ANGPTL3 is increased in both insulin-deficient and -resistant diabetic states Biochem. Biophys. Res. Commun. 317 2004 1075 1079
31. M. Shimamura, M. Matsuda, Y. Ando, R. Koishi, H. Yasumo, H. Furukawa, and I. Shimomura Leptin and insulin down-regulate angiopoietin-like protein 3, a plasma triglyceride-increasing factor Biochem. Biophys. Res. Commun. 322 2004 1080 1085
32. C. Fugier, J.J. Tousaint, X. Prieur, M. Plateroti, J. Samarut, and P. Delerive The lipoprotein lipase inhibitor ANGPTL3 is negatively regulated by thyroid hormone J. Biol. Chem. 281 2006 11553 11559
33. B. Lu, A. Moser, J.K. Shigenaga, C. Grunfeld, and K.R. Feingold The acute phase response stimulates the expression of angiopoietin like protein 4 Biochem. Biophys. Res. Commun. 391 2010 1737 1741
34. S. Romeo, L.A. Pennacchio, Y. Fu, E. Boerwinkle, A. Tybjaerg-Hansen, H.H. Hobbs, and J.C. Cohen Population-based resequencing of ANGPTL4 uncovers variations that reduce triglycerides and increase HDL Nat. Genet. 39 2007 513 516
35. P.J. Talmud, M. Smart, E. Presswood, J.A. Cooper, V. Nicaud, F. Drenos, J. Palmen, M.G. Marmot, S.M. Boekholdt, N.J. Wareham, K.T. Khaw, M. Kumari, and S.E. Humphries ANGPTL4 E40K and T266M: effects on plasma triglyceride and HDL levels, postprandial responses, and CHD risk Arterioscler. Thromb. Vasc. Biol. 28 2008 2319 2325
36. J.A. Nettleton, K.A. Volcik, E.W. Demerath, E. Boerwinkle, and A.R. Folsom Longitudinal changes in triglycerides according to ANGPTL4[E40K] genotype and longitudinal body weight change in the atherosclerosis risk in communities study Ann. Epidemiol. 18 2008 842 846
37. H. Staiger, F. Machicao, R. Werner, A. Guirguis, M. Weisser, N. Stefan, A. Fritsche, and H.U. Haring Genetic variation within the ANGPTL4 gene is not associated with metabolic traits in white subjects at an increased risk for type 2 diabetes mellitus Metabolism 57 2008 637 643
38. V. Legry, S. Bokor, D. Cottel, L. Beghin, G. Catasta, E. Nagy, M. Gonzalez-Gross, A. Spinneker, P. Stehle, D. Molnar, L.A. Moreno, P. Amouyel, J. Dallongeville, and A. Meirhaeghe Associations between common genetic polymorphisms in angiopoietin-like proteins 3 and 4 and lipid metabolism and adiposity in European adolescents and adults J. Clin. Endocrinol. Metab. 94 2009 5070 5077
39. M.C. Smart-Halajko, A. Kelley-Hedgepeth, M.C. Montefusco, J.A. Cooper, A. Kopin, J.M. McCaffrey, A. Balasubramanyam, H.J. Pownall, D.M. Nathan, I. Peter, P.J. Talmud, and G.S. Huggins ANGPTL4 variants E40K and T266M are associated with lower fasting triglyceride levels in Non-Hispanic White Americans from the Look AHEAD Clinical Trial BMC Med. Genet. 12 2011 89
40. M.C. Smart-Halajko, M.R. Robciuc, J.A. Cooper, M. Jauhiainen, M. Kumari, M. Kivimaki, K.T. Khaw, S.M. Boekholdt, N.J. Wareham, T.R. Gaunt, I.N. Day, P.S. Braund, C.P. Nelson, A.S. Hall, N.J. Samani, S.E. Humphries, C. Ehnholm, and P.J. Talmud The relationship between plasma angiopoietin-like protein 4 levels, angiopoietin-like protein 4 genotype, and coronary heart disease risk Arterioscler. Thromb. Vasc. Biol. 30 2010 2277 2282
41. D. Stejskal, M. Karpisek, H. Reutova, V. Humenanska, M. Petzel, P. Kusnierova, I. Vareka, R. Varekova, and P. Stejskal Angiopoietin-like protein 4: development, analytical characterization, and clinical testing of a new ELISA Gen. Physiol. Biophys. 27 2008 59 63
42. H. Staiger, C. Haas, J. Machann, R. Werner, M. Weisser, F. Schick, F. Machicao, N. Stefan, A. Fritsche, and H.U. Haring Muscle-derived angiopoietin-like protein 4 is induced by fatty acids via peroxisome proliferator-activated receptor (PPAR)-delta and is of metabolic relevance in humans Diabetes 58 2009 579 589
43. M.R. Robciuc, J. Naukkarinen, A. Ortega-Alonso, H. Tyynismaa, T. Raivio, A. Rissanen, J. Kaprio, C. Ehnholm, M. Jauhiainen, and K.H. Pietilainen Serum angiopoietin-like 4 protein levels and expression in adipose tissue are inversely correlated with obesity in monozygotic twins J. Lipid Res. 52 2011 1575 1582
44. S. Mandard, F. Zandbergen, E. van Straten, W. Wahli, F. Kuipers, M. Muller, and S. Kersten The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity J. Biol. Chem. 281 2006 934 944
45. X. Yu, S.C. Burgess, H. Ge, K.K. Wong, R.H. Nassem, D.J. Garry, A.D. Sherry, C.R. Malloy, J.P. Berger, and C. Li Inhibition of cardiac lipoprotein utilization by transgenic overexpression of Angptl4 in the heart Proc. Natl. Acad. Sci. U. S. A. 102 2005 1767 1772
46. A. Georgiadi, L. Lichtenstein, T. Degenhardt, M.V. Boekschoten, M. van Bilsen, B. Desvergne, M. Muller, and S. Kersten Induction of cardiac Angptl4 by dietary fatty acids is mediated by peroxisome proliferator-activated receptor beta/delta and protects against fatty acid-induced oxidative stress Circ. Res. 106 2010 1712 1721
47. U. Desai, E.C. Lee, K. Chung, C. Gao, J. Gay, B. Key, G. Hansen, D. Machajewski, K.A. Platt, A.T. Sands, M. Schneider, I. Van Sligtenhorst, A. Suwanichkul, P. Vogel, N. Wilganowski, J. Wingert, B.P. Zambrowicz, G. Landes, and D.R. Powell Lipid-lowering effects of anti-angiopoietin-like 4 antibody recapitulate the lipid phenotype found in angiopoietin-like 4 knockout mice Proc. Natl. Acad. Sci. U. S. A. 104 2007 11766 11771
48. E.C. Lee, U. Desai, G. Gololobov, S. Hong, X. Feng, X.C. Yu, J. Gay, N. Wilganowski, C. Gao, L.L. Du, J. Chen, Y. Hu, S. Zhao, L. Kirkpatrick, M. Schneider, B.P. Zambrowicz, G. Landes, D.R. Powell, and W.K. Sonnenburg Identification of a new functional domain in angiopoietin-like 3 (ANGPTL3) and angiopoietin-like 4 (ANGPTL4) involved in binding and inhibition of lipoprotein lipase (LPL) J. Biol. Chem. 284 2009 13735 13745
49. K. Yoshida, T. Shimizugawa, M. Ono, and H. Furukawa Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase J. Lipid Res. 43 2002 1770 1772
50. L.M. Sanderson, T. Degenhardt, A. Koppen, E. Kalkhoven, B. Desvergne, M. Muller, and S. Kersten Peroxisome proliferator-activated receptor beta/delta (PPARbeta/delta) but not PPARalpha serves as a plasma free fatty acid sensor in liver Mol. Cell. Biol. 29 2009 6257 6267
51. L. Lichtenstein, J.F. Berbee, S.J. van Dijk, K.W. van Dijk, A. Bensadoun, I.P. Kema, P.J. Voshol, M. Muller, P.C. Rensen, and S. Kersten Angptl4 upregulates cholesterol synthesis in liver via inhibition of LPL- and HL-dependent hepatic cholesterol uptake Arterioscler. Thromb. Vasc. Biol. 27 2007 2420 2427
52. V. Sukonina, A. Lookene, T. Olivecrona, and G. Olivecrona Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue Proc. Natl. Acad. Sci. U. S. A. 103 2006 17450 17455
53. X. Lei, F. Shi, D. Basu, A. Huq, S. Routhier, R. Day, and W. Jin Proteolytic processing of angiopoietin-like protein 4 by proprotein convertases modulates its inhibitory effects on lipoprotein lipase activity J. Biol. Chem. 286 2011 15747 15756
54. L. Lichtenstein, F. Mattijssen, N.J. de Wit, A. Georgiadi, G.J. Hooiveld, R. van der Meer, Y. He, L. Qi, A. Koster, J.T. Tamsma, N.S. Tan, M. Muller, and S. Kersten Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages Cell Metab. 12 2010 580 592
55. Y.H. Yang, Y. Wang, K.S. Lam, M.H. Yau, K.K. Cheng, J. Zhang, W. Zhu, D. Wu, and A. Xu Suppression of the Raf/MEK/ERK signaling cascade and inhibition of angiogenesis by the carboxyl terminus of angiopoietin-like protein 4 Arterioscler. Thromb. Vasc. Biol. 28 2008 835 840
56. C. Chomel, A. Cazes, C. Faye, M. Bignon, E. Gomez, C. Ardidie-Robouant, A. Barret, S. Ricard-Blum, L. Muller, S. Germain, and C. Monnot Interaction of the coiled-coil domain with glycosaminoglycans protects angiopoietin-like 4 from proteolysis and regulates its antiangiogenic activity FASEB J. 23 2009 940 949
57. W. Yin, S. Romeo, S. Chang, N.V. Grishin, H.H. Hobbs, and J.C. Cohen Genetic variation in ANGPTL4 provides insights into protein processing and function J. Biol. Chem. 284 2009 13213 13222
58. H. Ge, G. Yang, L. Huang, D.L. Motola, T. Pourbahrami, and C. Li Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4 J. Biol. Chem. 279 2004 2038 2045
59. Y.Y. Goh, M. Pal, H.C. Chong, P. Zhu, M.J. Tan, L. Punugu, C.R. Lam, Y.H. Yau, C.K. Tan, R.L. Huang, S.M. Tan, M.B. Tang, J.L. Ding, S. Kersten, and N.S. Tan Angiopoietin-like 4 interacts with integrins beta1 and beta5 to modulate keratinocyte migration Am. J. Pathol. 177 2010 2791 2803
60. Y.Y. Goh, M. Pal, H.C. Chong, P. Zhu, M.J. Tan, L. Punugu, C.K. Tan, R.L. Huang, S.K. Sze, M.B. Tang, J.L. Ding, S. Kersten, and N.S. Tan Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing J. Biol. Chem. 285 2010 32999 33009
61. H. Ge, G. Yang, X. Yu, T. Pourbahrami, and C. Li Oligomerization state-dependent hyperlipidemic effect of angiopoietin-like protein 4 J. Lipid Res. 45 2004 2071 2079
62. L.C. Clement, C. Avila-Casado, C. Mace, E. Soria, W.W. Bakker, S. Kersten, and S.S. Chugh Podocyte-secreted angiopoietin-like-4 mediates proteinuria in glucocorticoid-sensitive nephrotic syndrome Nat. Med. 17 2011 117 122
63. S. Kersten, L. Lichtenstein, E. Steenbergen, K. Mudde, H.F. Hendriks, M.K. Hesselink, P. Schrauwen, and M. Muller Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids Arterioscler. Thromb. Vasc. Biol. 29 2009 969 974
64. S. Kersten, S. Mandard, N.S. Tan, P. Escher, D. Metzger, P. Chambon, F.J. Gonzalez, B. Desvergne, and W. Wahli Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene J. Biol. Chem. 275 2000 28488 28493
65. F. Zandbergen, S. van Dijk, M. Muller, and S. Kersten Fasting-induced adipose factor/angiopoietin-like protein 4: a potential target for dyslipidemia? Future Lipidol. 1 2006 227 236
66. J.C. Yoon, T.W. Chickering, E.D. Rosen, B. Dussault, Y. Qin, A. Soukas, J.M. Friedman, W.E. Holmes, and B.M. Spiegelman Peroxisome proliferator- activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation Mol. Cell. Biol. 20 2000 5343 5349
67. T.T. Schug, D.C. Berry, N.S. Shaw, S.N. Travis, and N. Noy Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors Cell 129 2007 723 733
68. M. Rieck, W. Meissner, S. Ries, S. Muller-Brusselbach, and R. Muller Ligand-mediated regulation of peroxisome proliferator-activated receptor (PPAR) beta/delta: a comparative analysis of PPAR-selective agonists and all-trans retinoic acid Mol. Pharmacol. 74 2008 1269 1277
69. S. Naruhn, W. Meissner, T. Adhikary, K. Kaddatz, T. Klein, B. Watzer, S. Muller-Brusselbach, and R. Muller 15-hydroxyeicosatetraenoic acid is a preferential peroxisome proliferator-activated receptor beta/delta agonist Mol. Pharmacol. 77 2010 171 184
70. P.S. Palkar, M.G. Borland, S. Naruhn, C.H. Ferry, C. Lee, U.H. Sk, A.K. Sharma, S. Amin, I.A. Murray, C.R. Anderson, G.H. Perdew, F.J. Gonzalez, R. Muller, and J.M. Peters Cellular and pharmacological selectivity of the peroxisome proliferator-activated receptor-beta/delta antagonist GSK3787 Mol. Pharmacol. 78 2010 419 430
71. S. Mandard, F. Zandbergen, N.S. Tan, P. Escher, D. Patsouris, W. Koenig, R. Kleemann, A. Bakker, F. Veenman, W. Wahli, M. Muller, and S. Kersten The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment J. Biol. Chem. 279 2004 34411 34420
72. M. Heinaniemi, J.O. Uski, T. Degenhardt, and C. Carlberg Meta-analysis of primary target genes of peroxisome proliferator-activated receptors Genome Biol. 8 2007 R147
73. K. Kaddatz, T. Adhikary, F. Finkernagel, W. Meissner, S. Muller-Brusselbach, and R. Muller Transcriptional profiling identifies functional interactions of TGF beta and PPAR beta/delta signaling: synergistic induction of ANGPTL4 transcription J. Biol. Chem. 285 2010 29469 29479
74. J. Stockert, T. Adhikary, K. Kaddatz, F. Finkernagel, W. Meissner, S. Muller-Brusselbach, and R. Muller Reverse crosstalk of TGFbeta and PPARbeta/delta signaling identified by transcriptional profiling Nucleic Acids Res. 39 2011 119 131
75. T. Yamada, N. Ozaki, Y. Kato, Y. Miura, and Y. Oiso Insulin downregulates angiopoietin-like protein 4 mRNA in 3T3-L1 adipocytes Biochem. Biophys. Res. Commun. 347 2006 1138 1144
76. S.K. Koliwad, T. Kuo, L.E. Shipp, N.E. Gray, F. Backhed, A.Y. So, R.V. Farese Jr., and J.C. Wang Angiopoietin-like 4 (ANGPTL4, fasting-induced adipose factor) is a direct glucocorticoid receptor target and participates in glucocorticoid-regulated triglyceride metabolism J. Biol. Chem. 284 2009 25593 25601
77. L.F. Drager, J. Li, M.K. Shin, C. Reinke, N.R. Aggarwal, J.C. Jun, S. Bevans-Fonti, C. Sztalryd, S.M. O'Byrne, O. Kroupa, G. Olivecrona, W.S. Blaner, and V.Y. Polotsky Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea Eur. Heart J. 2011 [Electronic publication ahead of print]
78. F. Backhed, J.K. Manchester, C.F. Semenkovich, and J.I. Gordon Mechanisms underlying the resistance to diet-induced obesity in germ-free mice Proc. Natl. Acad. Sci. U. S. A. 104 2007 979 984
79. C.K. Fleissner, N. Huebel, M.M. Abd El-Bary, G. Loh, S. Klaus, and M. Blaut Absence of intestinal microbiota does not protect mice from diet-induced obesity Br. J. Nutr. 104 2010 919 929
80. L. Aronsson, Y. Huang, P. Parini, M. Korach-Andre, J. Hakansson, J.A. Gustafsson, S. Pettersson, V. Arulampalam, and J. Rafter Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4) PLoS One 5 2010
81. V. Legry, L. Goumidi, M. Huyvaert, D. Cottel, J. Ferrieres, D. Arveiler, A. Bingham, A. Wagner, J.B. Ruidavets, P. Ducimetiere, P. Amouyel, and A. Meirhaeghe Association between angiopoietin-like 6 (ANGPTL6) gene polymorphisms and metabolic syndrome-related phenotypes in the French MONICA Study Diabetes Metab. 35 2009 287 292
82. J. Namkung, S.B. Koh, I.D. Kong, J.W. Choi, and B.I. Yeh Serum levels of angiopoietin-related growth factor are increased in metabolic syndrome Metabolism 60 2011 564 568
83. T. Ebert, A. Bachmann, U. Lossner, J. Kratzsch, M. Bluher, M. Stumvoll, and M. Fasshauer Serum levels of angiopoietin-related growth factor in diabetes mellitus and chronic hemodialysis Metabolism 58 2009 547 551
84. Y. Oike, M. Akao, K. Yasunaga, T. Yamauchi, T. Morisada, Y. Ito, T. Urano, Y. Kimura, Y. Kubota, H. Maekawa, T. Miyamoto, K. Miyata, S. Matsumoto, J. Sakai, N. Nakagata, M. Takeya, H. Koseki, Y. Ogawa, T. Kadowaki, and T. Suda Angiopoietin-related growth factor antagonizes obesity and insulin resistance Nat. Med. 11 2005 400 408
85. Y. Oike, M. Akao, Y. Kubota, and T. Suda Angiopoietin-like proteins: potential new targets for metabolic syndrome therapy Trends Mol. Med. 11 2005 473 479