Angiopoietin-like proteins as therapeutic targets for cardiovascular disease: focus on lipid disorders

References

• Quagliarini F, Wang Y, Kozlitina J, et al. Atypical angiopoietin-like protein that regulates ANGPTL3. Proc Natl Acad Sci U S A. 2012;109(48):19751–19756.
   PubMed Web of Science ®Google Scholar
• Dewey FE, Gusarova V, Dunbar RL, et al. Genetic and pharmacologic inactivation of ANGPTL3 and cardiovascular disease. N Engl J Med. 2017;377(3):211–221.
   PubMed Web of Science ®Google Scholar
• Dewey FE, Gusarova V, O’Dushlaine C, et al. Inactivating variants in ANGPTL4 and risk of coronary artery disease. N Engl J Med. 2016;374(12):1123–1133.
   PubMed Web of Science ®Google Scholar
• Santulli G. Angiopoietin-like proteins: a comprehensive look. Front Endocrinol (Lausanne). 2014;5:4.
   PubMed Web of Science ®Google Scholar
• Dhanabal M, LaRochelle WJ, Jeffers M, et al. Angioarrestin: an antiangiogenic protein with tumor-inhibiting properties. Cancer Res. 2002;62(13):3834–3841.
   PubMed Web of Science ®Google Scholar
• Udhane SS, Pandey AV, Hofer G, et al. Retinoic acid receptor beta and angiopoietin-like protein 1 are involved in the regulation of human androgen biosynthesis. Sci Rep. 2015;5:10132.
   PubMed Web of Science ®Google Scholar
• Doi Y, Ninomiya T, Hirakawa Y, et al. Angiopoietin-like protein 2 and risk of type 2 diabetes in a general Japanese population: the hisayama study. Diabetes Care. 2013;36(1):98–100.
   PubMed Web of Science ®Google Scholar
• Hata J, Mukai N, Nagata M, et al. Serum angiopoietin-like protein 2 is a novel risk factor for cardiovascular disease in the community: the hisayama study. Arterioscler Thromb Vasc Biol. 2016;36(8):1686–1691.
   PubMed Web of Science ®Google Scholar
• Ortega-Senovilla H, Schaefer-Graf U, Meitzner K, et al. Decreased concentrations of the lipoprotein lipase inhibitor angiopoietin-like protein 4 and increased serum triacylglycerol are associated with increased neonatal fat mass in pregnant women with gestational diabetes mellitus. J Clin Endocrinol Metab. 2013;98(8):3430–3437.
   PubMed Web of Science ®Google Scholar
• Yoshida K, Shimizugawa T, Ono M, et al. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J Lipid Res. 2002;43(11):1770–1772.
   PubMed Web of Science ®Google Scholar
• Zeng L, Dai J, Ying K, et al. Identification of a novel human angiopoietin-like gene expressed mainly in heart. J Hum Genet. 2003;48(3):0159.
   Web of Science ®Google Scholar
• Varagnolo L, Lin Q, Obier N, et al. PRC2 inhibition counteracts the culture-associated loss of engraftment potential of human cord blood-derived hematopoietic stem and progenitor cells. Sci Rep. 2015;5:12319.
   PubMed Web of Science ®Google Scholar
• Oike Y, Yasunaga K, Ito Y, et al. Angiopoietin-related growth factor (AGF) promotes epidermal proliferation, remodeling, and regeneration. Proc Natl Acad Sci U S A. 2003;100(16):9494–9499.
   PubMed Web of Science ®Google Scholar
• Erkan G, Muratoglu S, Ercin U, et al. Angiopoietin-like protein 2 and angiopoietin-like protein 6 levels in patients with nonalcoholic fatty liver disease. Arch Med Sci. 2018;14(4):781–787.
   PubMed Web of Science ®Google Scholar
• Cinkajzlova A, Lacinova Z, Klouckova J, et al. Angiopoietin-like protein 6 in patients with obesity, type 2 diabetes mellitus, and anorexia nervosa: the influence of very low-calorie diet, bariatric surgery, and partial realimentation. Endocr Res. 2017;42(1):22–30.
   PubMed Web of Science ®Google Scholar
• Peek R, van Gelderen BE, Bruinenberg M, et al. Molecular cloning of a new angiopoietinlike factor from the human cornea. Invest Ophthalmol Vis Sci. 1998;39(10):1782–1788.
   PubMed Web of Science ®Google Scholar
• Lopez-Yrigoyen M, Yang C-T, Fidanza A, et al. Genetic programming of macrophages generates an in vitro model for the human erythroid island niche. Nat Commun. 2019;10(1):881.
   PubMedGoogle Scholar
• Fu Z, Yao F, Abou-Samra AB, et al. Lipasin, thermoregulated in brown fat, is a novel but atypical member of the angiopoietin-like protein family. Biochem Biophys Res Commun. 2013;430(3):1126–1131.
   PubMed Web of Science ®Google Scholar
• Nilsson A, Landin B, Schotz MC. Hydrolysis of chylomicron arachidonate and linoleate ester bonds by lipoprotein lipase and hepatic lipase. J Lipid Res. 1987;28(5):510–517.
   PubMed Web of Science ®Google Scholar
• Esenabhalu VE, Cerimagic M, Malli R, et al. Tissue-specific expression of human lipoprotein lipase in the vascular system affects vascular reactivity in transgenic mice. Br J Pharmacol. 2002;135(1):143–154.
   PubMed Web of Science ®Google Scholar
• Davies BS, Beigneux AP, Barnes RH, et al. GPIHBP1 is responsible for the entry of lipoprotein lipase into capillaries. Cell Metab. 2010;12(1):42–52.
   PubMed Web of Science ®Google Scholar
• Arora R, Nimonkar AV, Baird D, et al. Structure of lipoprotein lipase in complex with GPIHBP1. Proc Natl Acad Sci U S A. 2019;116(21):10360–10365.
   PubMed Web of Science ®Google Scholar
• Goulbourne CN, Gin P, Tatar A, et al. The GPIHBP1-LPL complex is responsible for the margination of triglyceride-rich lipoproteins in capillaries. Cell Metab. 2014;19(5):849–860.
   PubMed Web of Science ®Google Scholar
• Allan CM, Larsson M, Jung RS, et al. Mobility of “HSPG-bound” LPL explains how LPL is able to reach GPIHBP1 on capillaries. J Lipid Res. 2017;58(1):216–225.
   PubMed Web of Science ®Google Scholar
• van Tilbeurgh H, Roussel A, Lalouel JM, et al. Lipoprotein lipase. Molecular model based on the pancreatic lipase x-ray structure: consequences for heparin binding and catalysis. J Biol Chem. 1994;269(6):4626–4633.
   PubMed Web of Science ®Google Scholar
• Birrane G, Beigneux AP, Dwyer B, et al. Structure of the lipoprotein lipase-GPIHBP1 complex that mediates plasma triglyceride hydrolysis. Proc Natl Acad Sci U S A. 2019;116(5):1723–1732.
   PubMed Web of Science ®Google Scholar
• Kim SY, Park SM, Lee S-T. Apolipoprotein C-II is a novel substrate for matrix metalloproteinases. Biochem Biophys Res Commun. 2006;339(1):47–54.
   PubMed Web of Science ®Google Scholar
• Brocca S, Secundo F, Ossola M, et al. Sequence of the lid affects activity and specificity of Candida rugosa lipase isoenzymes. Protein Sci. 2003;12(10):2312–2319.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Nakajima T, Inoue I. Molecular modeling of the dimeric structure of human lipoprotein lipase and functional studies of the carboxyl-terminal domain. Eur J Biochem. 2002;269(18):4701–4710.
   PubMedGoogle Scholar
• Beigneux AP, Allan CM, Sandoval NP, et al. Lipoprotein lipase is active as a monomer. Proc Natl Acad Sci U S A. 2019;116(13):6319–6328.
   PubMed Web of Science ®Google Scholar
• Ahmad Z, Banerjee P, Hamon S, et al. Inhibition of angiopoietin-like protein 3 with a monoclonal antibody reduces triglycerides in hypertriglyceridemia. Circulation. 2019;140(6):470–486.
   PubMed Web of Science ®Google Scholar
• Tirosh A, Rudich A, Shochat T, et al. Changes in triglyceride levels and risk for coronary heart disease in young men. Ann Intern Med. 2007;147(6):377–385.
   PubMed Web of Science ®Google Scholar
• Wittrup HH, Tybjaerg-Hansen A, Nordestgaard BG. Lipoprotein lipase mutations, plasma lipids and lipoproteins, and risk of ischemic heart disease. A meta-analysis. Circulation. 1999;99(22):2901–2907.
   PubMed Web of Science ®Google Scholar
• Sarwar N, Danesh J, Eiriksdottir G, et al. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 2007;115(4):450–458.
   PubMed Web of Science ®Google Scholar
• Teslovich TM, Musunuru K, Smith AV, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010;466(7307):707–713.
   PubMed Web of Science ®Google Scholar
• Lettre G, Palmer CD, Young T, et al. Genome-wide association study of coronary heart disease and its risk factors in 8,090 African Americans: the NHLBI CARe project. PLoS Genet. 2011;7(2):e1001300.
   PubMed Web of Science ®Google Scholar
• Mailly F, Tugrul Y, Reymer PWA, et al. A common variant in the gene for lipoprotein lipase (Asp9–>asn) . Functional implications and prevalence in normal and hyperlipidemic subjects. Arterioscler Thromb Vasc Biol. 1995;15(4):468–478.
   PubMed Web of Science ®Google Scholar
• Stitziel NO, et al. Coding variation in ANGPTL4, LPL, and SVEP1 and the risk of coronary disease. N Engl J Med. 2016;374(12):1134–1144.
   PubMed Web of Science ®Google Scholar
• Khera AV, Won -H-H, Peloso GM, et al. Association of rare and common variation in the lipoprotein lipase gene with coronary artery disease. JAMA. 2017;317(9):937–946.
   PubMed Web of Science ®Google Scholar
• Varbo A, Benn M, Tybjærg-Hansen A, et al. Response: lipoprotein subclass profiling reveals pleiotropy in the genetic variants of lipid risk factors for coronary heart disease: a note on Mendelian randomization studies. J Am Coll Cardiol. 2013;62(20):1908–1909.
   PubMed Web of Science ®Google Scholar
• Gagne SE, Larson M, Pimstone S, et al. A common truncation variant of lipoprotein lipase (Ser447X) confers protection against coronary heart disease: the framingham offspring study. Clin Genet. 1999;55(6):450–454.
   PubMed Web of Science ®Google Scholar
• Groenemeijer BE, Hallman MD, Reymer PW, et al. Genetic variant showing a positive interaction with beta-blocking agents with a beneficial influence on lipoprotein lipase activity, HDL cholesterol, and triglyceride levels in coronary artery disease patients. The Ser447-stop substitution in the lipoprotein lipase gene. REGRESS study group. Circulation. 1997;95(12):2628–2635.
   PubMed Web of Science ®Google Scholar
• Stitziel NO, Khera AV, Wang X, et al. ANGPTL3 deficiency and protection against coronary artery disease. J Am Coll Cardiol. 2017;69(16):2054–2063.
   PubMed Web of Science ®Google Scholar
• Shan L, Yu X-C, Liu Z, et al. The angiopoietin-like proteins ANGPTL3 and ANGPTL4 inhibit lipoprotein lipase activity through distinct mechanisms. J Biol Chem. 2009;284(3):1419–1424.
   PubMed Web of Science ®Google Scholar
• Gao T, Jin K, Chen P, et al. Circulating betatrophin correlates with triglycerides and postprandial glucose among different glucose tolerance statuses–a case-control study. PLoS One. 2015;10(8):e0133640.
   PubMed Web of Science ®Google Scholar
• Conklin D, Gilbertson D, Taft DW, et al. Identification of a mammalian angiopoietin-related protein expressed specifically in liver. Genomics. 1999;62(3):477–482.
   PubMed Web of Science ®Google Scholar
• Romeo S, Yin W, Kozlitina J, et al. Rare loss-of-function mutations in ANGPTL family members contribute to plasma triglyceride levels in humans. J Clin Invest. 2009;119(1):70–79.
   PubMed Web of Science ®Google Scholar
• Nidhina Haridas PA, Soronen J, Sädevirta S, et al. Regulation of angiopoietin-like proteins (ANGPTLs) 3 and 8 by insulin. J Clin Endocrinol Metab. 2015;100(10):E1299–307.
   PubMed Web of Science ®Google Scholar
• Wang Y, McNutt MC, Banfi S, et al. Hepatic ANGPTL3 regulates adipose tissue energy homeostasis. Proc Natl Acad Sci U S A. 2015;112(37):11630–11635.
   PubMed Web of Science ®Google Scholar
• Koishi R, Ando Y, Ono M, et al. Angptl3 regulates lipid metabolism in mice. Nat Genet. 2002;30(2):151–157.
   PubMed Web of Science ®Google Scholar
• Shimamura M, Matsuda M, Kobayashi S, et al. Angiopoietin-like protein 3, a hepatic secretory factor, activates lipolysis in adipocytes. Biochem Biophys Res Commun. 2003;301(2):604–609.
   PubMed Web of Science ®Google Scholar
• Shimizugawa T, Ono M, Shimamura M, et al. ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase. J Biol Chem. 2002;277(37):33742–33748.
   PubMed Web of Science ®Google Scholar
• Jaye M, Lynch KJ, Krawiec J, et al. A novel endothelial-derived lipase that modulates HDL metabolism. Nat Genet. 1999;21(4):424–428.
   PubMed Web of Science ®Google Scholar
• Hirata K, Dichek HL, Cioffi JA, et al. Cloning of a unique lipase from endothelial cells extends the lipase gene family. J Biol Chem. 1999;274(20):14170–14175.
   PubMed Web of Science ®Google Scholar
• Kersten S, Mandard S, Tan NS, et al. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem. 2000;275(37):p. 28488–93.
   PubMed Web of Science ®Google Scholar
• Yoon JC, Chickering TW, Rosen ED, et al. Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol Cell Biol. 2000;20(14):5343–5349.
   PubMed Web of Science ®Google Scholar
• Kim I, KIM H-G, KIM H, et al. Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem J. 2000;346(3):603–610.
   PubMedGoogle Scholar
• Aryal B, Singh AK, Zhang X, et al. Absence of ANGPTL4 in adipose tissue improves glucose tolerance and attenuates atherogenesis. JCI Insight. 2018;3(6).
   PubMed Web of Science ®Google Scholar
• Ingerslev B, Hansen JS, Hoffmann C, et al. Angiopoietin-like protein 4 is an exercise-induced hepatokine in humans, regulated by glucagon and cAMP. Mol Metab. 2017;6(10):1286–1295.
   PubMed Web of Science ®Google Scholar
• Catoire M, Alex S, Paraskevopulos N, et al. Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proc Natl Acad Sci U S A. 2014;111(11):E1043–52.
   PubMed Web of Science ®Google Scholar
• Lee E-C, Desai U, Gololobov G, et al. 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. 2009;284(20):13735–13745.
   PubMed Web of Science ®Google Scholar
• Ren G, Kim JY, Smas CM. Identification of RIFL, a novel adipocyte-enriched insulin target gene with a role in lipid metabolism. Am J Physiol Endocrinol Metab. 2012;303(3):E334–51.
   PubMed Web of Science ®Google Scholar
• Zhang R. Lipasin, a novel nutritionally-regulated liver-enriched factor that regulates serum triglyceride levels. Biochem Biophys Res Commun. 2012;424(4):786–792.
   PubMed Web of Science ®Google Scholar
• Kovrov O, Kristensen KK, Larsson E, et al. On the mechanism of angiopoietin-like protein 8 for control of lipoprotein lipase activity. J Lipid Res. 2019;60(4):783–793.
   PubMed Web of Science ®Google Scholar
• Gusarova V, Banfi S, Alexa-Braun CA, et al. ANGPTL8 blockade with a monoclonal antibody promotes triglyceride clearance, energy expenditure, and weight loss in mice. Endocrinology. 2017;158(5):1252–1259.
   PubMed Web of Science ®Google Scholar
• Haller JF, Mintah IJ, Shihanian LM, et al. ANGPTL8 requires ANGPTL3 to inhibit lipoprotein lipase and plasma triglyceride clearance. J Lipid Res. 2017;58(6):1166–1173.
   PubMed Web of Science ®Google Scholar
• Chi X, Britt EC, Shows HW, et al. ANGPTL8 promotes the ability of ANGPTL3 to bind and inhibit lipoprotein lipase. Mol Metab. 2017;6(10):1137–1149.
   PubMed Web of Science ®Google Scholar
• Siddiqa A, Ahmad J, Ali A, et al. Structural characterization of ANGPTL8 (betatrophin) with its interacting partner lipoprotein lipase. Comput Biol Chem. 2016;61:210–220.
   PubMed Web of Science ®Google Scholar
• Camenisch G, Pisabarro MT, Sherman D, et al. ANGPTL3 stimulates endothelial cell adhesion and migration via integrin alpha vbeta 3 and induces blood vessel formation in vivo. J Biol Chem. 2002;277(19):17281–17290.
   PubMed Web of Science ®Google Scholar
• La Paglia L, Listì A, Caruso S, et al. Potential role of ANGPTL4 in the cross talk between metabolism and cancer through PPAR signaling pathway. PPAR Res. 2017;2017:8187235.
   PubMed Web of Science ®Google Scholar
• Oteng A-B, Ruppert PMM, Boutens L, et al. Characterization of ANGPTL4 function in macrophages and adipocytes using Angptl4-knockout and Angptl4-hypomorphic mice. J Lipid Res. 2019;60(10):1741–1754.
   PubMed Web of Science ®Google Scholar
• Kirsch N, Chang L-S, Koch S, et al. Angiopoietin-like 4 is a wnt signaling antagonist that promotes LRP6 turnover. Dev Cell. 2017;43(1):71–82 e6.
   PubMed Web of Science ®Google Scholar
• Dijk W, Ruppert PMM, Oost LJ, et al. Angiopoietin-like 4 promotes the intracellular cleavage of lipoprotein lipase by PCSK3/furin in adipocytes. J Biol Chem. 2018;293(36):14134–14145.
   PubMed Web of Science ®Google Scholar
• Gutgsell AR, Ghodge SV, Bowers AA, et al. Mapping the sites of the lipoprotein lipase (LPL)-angiopoietin-like protein 4 (ANGPTL4) interaction provides mechanistic insight into LPL inhibition. J Biol Chem. 2019;294(8):2678–2689.
   PubMed Web of Science ®Google Scholar
• Liu J, Afroza H, Rader DJ, et al. Angiopoietin-like protein 3 inhibits lipoprotein lipase activity through enhancing its cleavage by proprotein convertases. J Biol Chem. 2010;285(36):27561–27570.
   PubMed Web of Science ®Google Scholar
• van der Kolk BW, Vink RG, Jocken JWE, et al. Effect of diet-induced weight loss on angiopoietin-like protein 4 and adipose tissue lipid metabolism in overweight and obese humans. Physiol Rep. 2018;6(13):e13735.
   PubMed Web of Science ®Google Scholar
• Dijk W, Beigneux AP, Larsson M, et al. Angiopoietin-like 4 promotes intracellular degradation of lipoprotein lipase in adipocytes. J Lipid Res. 2016;57(9):1670–1683.
   PubMed Web of Science ®Google Scholar
• Glazer NL. Exome sequencing links gene mutation in angiopoietin-like protein 3 with low-density lipoprotein cholesterol. Circ Cardiovasc Genet. 2011;4(1):100–101.
   PubMedGoogle Scholar
• Costet P, Cariou B, Lambert G, et al. Hepatic PCSK9 expression is regulated by nutritional status via insulin and sterol regulatory element-binding protein 1c. J Biol Chem. 2006;281(10):6211–6218.
   PubMed Web of Science ®Google Scholar
• Morelli MB, Wang X, Santulli G. Functional role of gut microbiota and PCSK9 in the pathogenesis of diabetes mellitus and cardiovascular disease. Atherosclerosis. 2019;289:176–178.
   PubMed Web of Science ®Google Scholar
• Ai D, Chen C, Han S, et al. Regulation of hepatic LDL receptors by mTORC1 and PCSK9 in mice. J Clin Invest. 2012;122(4):1262–1270.
   PubMed Web of Science ®Google Scholar
• Inukai K, Nakashima Y, Watanabe M, et al. ANGPTL3 is increased in both insulin-deficient and -resistant diabetic states. Biochem Biophys Res Commun. 2004;317(4):1075–1079.
   PubMed Web of Science ®Google Scholar
• Lichtenstein L, Berbée JFP, van Dijk SJ, et al. Angptl4 upregulates cholesterol synthesis in liver via inhibition of LPL- and HL-dependent hepatic cholesterol uptake. Arterioscler Thromb Vasc Biol. 2007;27(11):2420–2427.
   PubMed Web of Science ®Google Scholar
• Baranowski T, Kralisch S, Bachmann A, et al. Serum levels of the adipokine fasting-induced adipose factor/angiopoietin-like protein 4 depend on renal function. Horm Metab Res. 2011;43(2):117–120.
   PubMed Web of Science ®Google Scholar
• Koliwad SK, Kuo T, Shipp LE, et al. Angiopoietin-like 4 (ANGPTL4, fasting-induced adipose factor) is a direct glucocorticoid receptor target and participates in glucocorticoid-regulated triglyceride metabolism. J Biol Chem. 2009;284(38):25593–25601.
   PubMed Web of Science ®Google Scholar
• Kaddatz K, Adhikary T, Finkernagel F, et al. Transcriptional profiling identifies functional interactions of TGF beta and PPAR beta/delta signaling: synergistic induction of ANGPTL4 transcription. J Biol Chem. 2010;285(38):29469–29479.
   PubMed Web of Science ®Google Scholar
• Kuo TC, Tan C-T, Chang Y-W, et al. Angiopoietin-like protein 1 suppresses SLUG to inhibit cancer cell motility. J Clin Invest. 2013;123(3):1082–1095.
   PubMed Web of Science ®Google Scholar
• Wang Y, Quagliarini F, Gusarova V, et al. Mice lacking ANGPTL8 (Betatrophin) manifest disrupted triglyceride metabolism without impaired glucose homeostasis. Proc Natl Acad Sci U S A. 2013;110(40):16109–16114.
   PubMed Web of Science ®Google Scholar
• Fu Z, Abou-Samra AB, Zhang R. A lipasin/Angptl8 monoclonal antibody lowers mouse serum triglycerides involving increased postprandial activity of the cardiac lipoprotein lipase. Sci Rep. 2015;5:18502.
   PubMed Web of Science ®Google Scholar
• Chen S, Feng M, Zhang S, et al. Angptl8 mediates food-driven resetting of hepatic circadian clock in mice. Nat Commun. 2019;10(1):3518.
   PubMedGoogle Scholar
• Zhang R. The ANGPTL3-4-8 model, a molecular mechanism for triglyceride trafficking. Open Biol. 2016;6(4):150272.
   PubMed Web of Science ®Google Scholar
• Fu Z, Berhane F, Fite A, et al. Elevated circulating lipasin/betatrophin in human type 2 diabetes and obesity. Sci Rep. 2014;4:5013.
   PubMed Web of Science ®Google Scholar
• Rong Guo X, et al. ANGPTL8/betatrophin alleviates insulin resistance via the Akt-GSK3beta or Akt-FoxO1 pathway in HepG2 cells. Exp Cell Res. 2016;345(2):158–167.
   PubMed Web of Science ®Google Scholar
• Lee J, Hong S-W, Park SE, et al. AMP-activated protein kinase suppresses the expression of LXR/SREBP-1 signaling-induced ANGPTL8 in HepG2 cells. Mol Cell Endocrinol. 2015;414:148–155.
   PubMed Web of Science ®Google Scholar
• Tseng Y-H, Ke P-Y, Liao C-J, et al. Chromosome 19 open reading frame 80 is upregulated by thyroid hormone and modulates autophagy and lipid metabolism. Autophagy. 2014;10(1):20–31.
   PubMed Web of Science ®Google Scholar
• Lartey LJ, Werneck-de-Castro JP, O-Sullivan I, et al. Coupling between nutrient availability and thyroid hormone activation. J Biol Chem. 2015;290(51):30551–30561.
   PubMed Web of Science ®Google Scholar
• DiStefano JK. Angiopoietin-like 8 (ANGPTL8) expression is regulated by miR-143-3p in human hepatocytes. Gene. 2019;681:1–6.
   PubMed Web of Science ®Google Scholar
• Mysore R, Ortega FJ, Latorre J, et al. MicroRNA-221-3p regulates angiopoietin-like 8 (ANGPTL8) expression in adipocytes. J Clin Endocrinol Metab. 2017;102(11):4001–4012.
   PubMed Web of Science ®Google Scholar
• Kuwajima M, Foster DW, McGarry JD. Regulation of lipoprotein lipase in different rat tissues. Metabolism. 1988;37(6):597–601.
   PubMed Web of Science ®Google Scholar
• Kersten S, Lichtenstein L, Steenbergen E, et al. Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids. Arterioscler Thromb Vasc Biol. 2009;29(6):969–974.
   PubMed Web of Science ®Google Scholar
• Minicocci I, Montali A, Robciuc MR, et al. Mutations in the ANGPTL3 gene and familial combined hypolipidemia: a clinical and biochemical characterization. J Clin Endocrinol Metab. 2012;97(7):E1266–75.
   PubMed Web of Science ®Google Scholar
• Pisciotta L, Favari E, Magnolo L, et al. Characterization of three kindreds with familial combined hypolipidemia caused by loss-of-function mutations of ANGPTL3. Circ Cardiovasc Genet. 2012;5(1):42–50.
   PubMedGoogle Scholar
• Helgadottir A, Gretarsdottir S, Thorleifsson G, et al. Variants with large effects on blood lipids and the role of cholesterol and triglycerides in coronary disease. Nat Genet. 2016;48(6):634–639.
   PubMed Web of Science ®Google Scholar
• Musunuru K, Pirruccello JP, Do R, et al. Exome sequencing, ANGPTL3 mutations, and familial combined hypolipidemia. N Engl J Med. 2010;363(23):2220–2227.
   PubMed Web of Science ®Google Scholar
• Minicocci I, Tikka A, Poggiogalle E, et al. Effects of angiopoietin-like protein 3 deficiency on postprandial lipid and lipoprotein metabolism. J Lipid Res. 2016;57(6):1097–1107.
   PubMed Web of Science ®Google Scholar
• Graham MJ, Lee RG, Brandt TA, et al. Cardiovascular and metabolic effects of ANGPTL3 antisense oligonucleotides. N Engl J Med. 2017;377(3):222–232.
   PubMed Web of Science ®Google Scholar
• Peloso GM, Auer P, Bis J, et al. Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks. Am J Hum Genet. 2014;94(2):223–232.
   PubMed Web of Science ®Google Scholar
• Romeo S, Pennacchio LA, Fu Y, et al. Population-based resequencing of ANGPTL4 uncovers variations that reduce triglycerides and increase HDL. Nat Genet. 2007;39(4):513–516.
   PubMed Web of Science ®Google Scholar
• Smart-Halajko MC, Kelley-Hedgepeth A, Montefusco MC, et al. 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. 2011;12:89.
   PubMed Web of Science ®Google Scholar
• Talmud PJ, Smart M, Presswood E, et al. ANGPTL4 E40K and T266M: effects on plasma triglyceride and HDL levels, postprandial responses, and CHD risk. Arterioscler Thromb Vasc Biol. 2008;28(12):2319–2325.
   PubMed Web of Science ®Google Scholar
• Folsom AR, Peacock JM, Demerath E, et al. Variation in ANGPTL4 and risk of coronary heart disease: the atherosclerosis risk in communities study. Metabolism. 2008;57(11):1591–1596.
   PubMed Web of Science ®Google Scholar
• Gusarova V, O’Dushlaine C, Teslovich TM, et al. Genetic inactivation of ANGPTL4 improves glucose homeostasis and is associated with reduced risk of diabetes. Nat Commun. 2018;9(1):2252.
   PubMed Web of Science ®Google Scholar
• Gusarova V, Alexa CA, Wang Y, et al. ANGPTL3 blockade with a human monoclonal antibody reduces plasma lipids in dyslipidemic mice and monkeys. J Lipid Res. 2015;56(7):1308–1317.
   PubMed Web of Science ®Google Scholar
• Wang Y, Gusarova V, Banfi S, et al. Inactivation of ANGPTL3 reduces hepatic VLDL-triglyceride secretion. J Lipid Res. 2015;56(7):1296–1307.
   PubMed Web of Science ®Google Scholar
• Gaudet D, Gipe DA, Pordy R, et al. ANGPTL3 inhibition in homozygous familial hypercholesterolemia. N Engl J Med. 2017;377(3):296–297.
   Google Scholar
• Desai U, Lee E-C, Chung K, et al. 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. 2007;104(28):11766–11771.
   PubMed Web of Science ®Google Scholar
• Lichtenstein L, Mattijssen F, de Wit NJ, et al. Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab. 2010;12(6):580–592.
   PubMed Web of Science ®Google Scholar
• Chadwick AC, Evitt NH, Lv W, et al. Reduced blood lipid levels with in vivo CRISPR-cas9 base editing of ANGPTL3. Circulation. 2018;137(9):975–977.
   PubMed Web of Science ®Google Scholar
• 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(4):806–811.
   PubMed Web of Science ®Google Scholar
• Alghanim G, Qaddoumi MG, Alhasawi N, et al. Higher levels of ANGPTL5 in the circulation of subjects with obesity and type 2 diabetes are associated with insulin resistance. Front Endocrinol (Lausanne). 2019;10:495.
   PubMed Web of Science ®Google Scholar
• Vatner DF, Goedeke L, Camporez J-PG, et al. Angptl8 antisense oligonucleotide improves adipose lipid metabolism and prevents diet-induced NAFLD and hepatic insulin resistance in rodents. Diabetologia. 2018;61(6):1435–1446.
   PubMed Web of Science ®Google Scholar