The role of ANGPTL3 in controlling lipoprotein metabolism

Endocrine

Volumn 52, Issue 2, 2016, Pages 187-193

  Tikka, Anna ^a   Jauhiainen, Matti ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

ANGPTL3; FHBL2; Lipoprotein metabolism; LPL; Triglycerides

Indexed keywords

LIPOPROTEIN LIPASE; ANGIOPOIETIN; ANGPTL3 PROTEIN, HUMAN; LIPOPROTEIN;

ADIPOSE TISSUE; ANGPTL3 GENE; ENZYME ACTIVITY; FAMILIAL HYPERLIPEMIA; GENE; GENE FUNCTION; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; LIPOPROTEIN METABOLISM; LIPOPROTEIN SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEQUENCE ANALYSIS; ADULT; AGED; FEMALE; GENETICS; HYPOBETALIPOPROTEINEMIA; LIPID METABOLISM; MALE; METABOLISM; MIDDLE AGED; PHYSIOLOGY;

ADULT; AGED; ANGIOPOIETINS; FEMALE; HUMANS; HYPOBETALIPOPROTEINEMIAS; LIPID METABOLISM; LIPOPROTEINS; MALE; MIDDLE AGED;

EID: 84954149862     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-015-0838-9     Document Type: Review

References (54)

1. T.G. Redgrave, Chylomicrons, in Lipoproteins in Health and Disease, ed. by D.J. Betteridge, D.R. Illingworth, J. Shepherd (Arnold, London, 1999), pp. 31–54
2. H.N. Ginsberg, J.L. Dixon, I.J. Goldberg, Illingworth, J. Shepherd, VLDL/LDL cascade system: assembly, secretion and intravascular metabolism of apoprotein B-containing lipoproteins, in Lipoproteins in Health and Disease, ed. by D.J. Betteridge (Arnold, London, 1999), pp. 55–70
3. C.J. Packard, J. Shepher, Physiology of the lipoprotein transport system: an overview of lipoprotein metabolism, in Lipoproteins in Health and Disease, ed. by D.J. Betteridge, D.R. Illingworth, J. Shepherd (Arnold, London, 1999), pp. 17–30
4. I.J. Goldberg, R.H. Eckel, N.A. Abumrad, Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways. J Lipid Res. 50, S86–S90 (2009)
5. A.R. Tall, L. Yvan-Charvet, N. Terasaka, T. Pagler, N. Wang, HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab. 7(5), 365–375 (2008)
6. C. Willer et al., Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat. Genet. 40(2), 161–169 (2008)
7. S. Kathiresan, O. Melander, C. Guiducci, A. Surti, NP. Burtt, MJ. Rieder, GM. Cooper, C. Roos, BF. Voight, AS. Havulinna, B. Wahlstrand, T. Hedner, D. Corella, ES. Tai, JM. Ordovas, G. Berglund, E. Vartiainen, P. Jousilahti, B. Hedblad, MR. Taskinen, C. Newton-Cheh, V. Salomaa, L. Peltonen, L. Groop, DM. Altshuler, M. Orho-Melander, Sixnew loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat. Genet. 40(2),189–97 (2008). Erratum in: Nat. Genet. 40(11):1384 (2008)
8. N. Woolf, Pathology of atherosclerosis, in Lipoproteins in Health and Disease, ed. by D.J. Betteridge, D.R. Illingworth, J. Shepherd (Arnold, London, 1999), pp. 533–540
9. B.G. Nordestgaard, M. Benn, P. Schnohr, A. Tybjaerg-Hansen, Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. JAMA 298(3), 299–308 (2007)
10. H.L. Staniak, W. Salgado Filho, M.H. Miname, I.M. Benseñor, P.A. Lotufo, R. Sharovsky, C.E. Rochitte, R.D. Bittencourt, R.D. Santos, Association between postprandialtriglycerides and coronary artery disease detected by coronary computed tomography angiography. Atherosclerosis 233(2), 381–386 (2014)
11. R.C. Oh, J.B. Lanier, Management of hypertriglyceridemia. Am Fam. Physician. 75(9), 1365–1371 (2007)
12. T. Hato, M. Tabata, Y. Oike, The role of angiopoietin-like proteins in angiogenesis and metabolism. Trends Cardiovasc. Med. 18, 6–14 (2008)
13. D. Conklin, D. Gilbertson, D.W. Taft, M.F. Maurer, T.E. Whitmore, D.L. Smith, K.M. Walker, L.H. Chen, S. Wattler, M. Nehls, K.B. Lewis, Identification of a mammalian angiopoietin-related protein expressed specifically in liver. Genomics 62(3), 477–482 (1999)
14. M. Ono, T. Shimizugawa, M. Shimamura, K. Yoshida, C. Noji-Sakikawa, Y. Ando, R. Koishi, 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(43), 41804–41809 (2003)
15. L. Shan, X.C. Yu, Z. Liu, Y. Hu, L.T. Sturgis, M.L. Miranda, Q. Liu, The angiopoietin-like proteins ANGPTL3 and ANGPTL4 inhibit lipoprotein lipase activity through distinct mechanisms. J Biol. Chem. 284(3), 1419–1424 (2009)
16. G. Camenisch, M.T. Pisabarro, D. Sherman, J. Kowalski, M. Nagel, P. Hass, M.H. Xie, A. Gurney, S. Bodary, X.H. Liang, K. Clark, M. Beresini, N. Ferrara, H.P. Gerber, ANGPTL3 stimulates endothelial cell adhesion and migration via integrin alpha vbeta 3 and induces blood vessel formation in vivo. J Biol. Chem. 277(19), 17281–17290 (2002)
17. W. Jin, X. Wang, J.S. Millar, T. Quertermous, G.H. Rothblat, J.M. Glick, D.J. Rader, Hepatic proprotein convertases modulate HDL metabolism. Cell Metab. 6(2), 129–136 (2007)
18. F. Quagliarini, Y. Wang, J. Kozlitina, N.V. Grishin, R. Hyde, E. Boerwinkle, D.M. Valenzuela, A.J. Murphy, J.C. Cohen, H.H. Hobbs, Atypical angiopoietin-like protein that regulates ANGPTL3. Proc. Natl. Acad. Sci. USA 109(48), 19751–19756 (2012)
19. Z. Fu, F. Yao, A.B. Abou-Samra, R. Zhang, Lipasin, thermoregulated in brown fat, is a novel but atypical member of the angiopoietin-like protein family. Biochem. Biophys. Res. Commun. 430(3), 1126–1131 (2013)
20. R. Zhang, A.B. Abou-Samra, A dual role of lipasin (betatrophin) in lipid metabolism and glucose homeostasis: consensus and controversy. Cardiovasc. Diabetol. 13, 133 (2014)
21. R. Koishi, Y. Ando, M. Ono, M. Shimamura, H. Yasumo, T. Fujiwara, H. Horikoshi, H. Furukawa, Angptl3 regulates lipid metabolism in mice. Nat. Genet. 30(2), 151–157 (2002)
22. T. Shimizugawa, M. Ono, M. Shimamura, K. Yoshida, Y. Ando, R. Koishi, K. Ueda, T. Inaba, H. Minekura, T. Kohama, H. Furukawa, ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase. J. Biol. Chem. 277(37), 33742–33748 (2002)
23. Y. Ando, T. Shimizugawa, S. Takeshita, M. Ono, M. Shimamura, R. Koishi, H. Furukawa, A decreased expression of angiopoietin-like 3 is protective against atherosclerosis in apoE-deficient mice. J. Lipid Res. 44(6), 1216–1223 (2003)
24. T.M. Teslovich, K. Musunuru et al., Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466(7307), 707–713 (2010)
25. S. Romeo, W. Yin, J. Kozlitina, L.A. Pennacchio, E. Boerwinkle, H.H. Hobbs, J.C. Cohen, Rare loss-of-function mutations in ANGPTL family members contribute to plasma triglyceride levels in humans. J Clin. Invest. 119(1), 70–79 (2009)
26. I. Minicocci, A. Montali, M.R. Robciuc, F. Quagliarini, V. Censi, G. Labbadia, C. Gabiati, G. Pigna, M.L. Sepe, F. Pannozzo, D. Lütjohann, S. Fazio, M. Jauhiainen, C. Ehnholm, M. Arca, Mutations in the ANGPTL3 gene and familial combined hypolipidemia: a clinical and biochemical characterization. J. Clin. Endocrinol. Metab. 97(7), E1266–E1275 (2012)
27. K. Musunuru et al., Exome sequencing, ANGPTL3 mutations, and familial combined hypolipidemia. N. Engl. J. Med. 363, 2220–2227 (2010)
28. M. Arca, I. Minicocci, M. Maranghi, The angiopoietin-like protein 3: a hepatokine with expanding role in metabolism. Curr. Opin. Lipidol. 24(4), 313–320 (2013)
29. J.M. Martín-Campos, R. Roig, C. Mayoral, S. Martinez, G. Marti, J.A. Arroyo, J. Julve, F. Blano-Vaca, Identification of a novel mutation in the ANGPTL3 gene in two families diagnosed of familial hypobetalipoproteinemia without APOB mutation. Clin. Chim. Acta. 413, 552–555 (2012)
30. L. Pisciotta et al., Characterization of three kindred with familial combined hypolipidemia due to loss of function mutations of ANGPTL3. Cardiovasc. Genet. 5, 42–50 (2012)
31. D. Noto, A.B. Cefalù, V. Valenti, F. Fayer, E. Pinotti, M. Ditta, R. Spina, G. Vigna, P. Yue, S. Kathiresan, P. Tarugi, M.R. Averna, Prevalence of ANGPTL3 and APOB gene mutations in subjects with combined hypolipidemia. Arterioscler. Thromb. Vasc. Biol. 32(3), 805–809 (2012)
32. K. Hirata, H.L. Dichek, J.A. Cioffi, S.Y. Choi, N.J. Leeper, L. Quintana, G.S. Kronmal, A.D. Cooper, T. Quertermous, Cloning of a unique lipase from endothelial cells extends the lipase gene family. J. Biol. Chem. 274(20), 14170–14175 (1999)
33. M.G. McCoy, G.S. Sun, D. Marchadier, C. Maugeais, J.M. Glick, D.J. Rader, Characterization of the lipolytic activity of endothelial lipase. J. Lipid Res. 43, 921–929 (2002)
34. M.R. Robciuc, M. Maranghi, A. Lahikainen, D. Rader, A. Bensadoun, K. Öörni, J. Metso, I. Minicocci, E. Ciociola, F. Ceci, A. Montali, M. Arca, C. Ehnholm, M. Jauhiainen, Angptl3 deficiency is associated with increased insulin sensitivity, lipoprotein lipase activity, and decreased serum free fatty acids. Arterioscler. Thromb. VascBiol. 33(7), 1706–1713 (2013)
35. J. Liu, H. Afroza, D.J. Rader, W. Jin, Angiopoietin-like protein 3 inhibits lipoprotein lipase activity through enhancing its cleavage by proprotein convertases. J. Biol. Chem. 285(36), 27561–27570 (2010)
36. 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, I. Shimomura, Angiopoietin-like protein3 regulates plasma HDL cholesterol through suppression of endothelial lipase. Arterioscler. Thromb. Vasc. Biol. 27(2), 366–372 (2007)
37. Y. Wang, M.C. McNutt, S. Banfi, M.G. Levin, W.L. Holland, V. Gusarova, J. Gromada, J.C. Cohen, H.H. Hobbs, Hepatic ANGPTL3 regulates adipose tissue energy homeostasis. Proc. Natl. Acad. Sci. USA 112(37), 11630–11635 (2015)
38. Y. Wang, V. Gusarova, S. Banfi, J. Gromada, J.C. Cohen, H.H. Hobbs, Inactivation of ANGPTL3 reduces hepatic VLDL-triglyceride secretion. J. Lipid Res. 56(7), 1296–1307 (2015)
39. M. Jaye, K.J. Lynch, J. Krawiec, D. Marchadier, C. Maugeais, K. Doan, V. South, D. Amin, M. Perrone, D.J. Rader, A novel endothelial-derived lipase that modulates HDL metabolism. Nat. Genet. 21(4), 424–428 (1999)
40. J.W. Gofman, W. Young, R. Tandy, Ischemic heart disease, atherosclerosis, and longevity. Circulation 34(4), 679–697 (1966)
41. R.E. Duncan, M. Ahmadian, K. Jaworski, E. Sarkadi-Nagy, H.S. Sul, Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27, 79–101 (2007)
42. M.C. Moore, K.C. Coate, J.J. Winnick, Z. An, A.D. Cherrington, Regulation of hepatic glucose uptake and storage in vivo. Adv. Nutr. 3(3), 286–294 (2012)
43. M. Adiels, J. Westerbacka, A. Soro-Paavonen, A.M. Häkkinen, S. Vehkavaara, M.J. Caslake, C. Packard, S.O. Olofsson, H. Yki-Järvinen, M.R. Taskinen, J. Borén, Acute suppression of VLDL1 secretion rate by insulin is associated with hepatic fat content and insulin resistance. Diabetologia 50(11), 2356–2365 (2007)
44. A. Tikka, J. Soronen, P.P. Laurila, J. Metso, C. Ehnholm, M. Jauhiainen, Silencing of ANGPTL 3 (angiopoietin-like protein 3) in human hepatocytes results in decreased expression of gluconeogenic genes and reduced triacylglycerol-rich VLDL secretion upon insulin stimulation. Biosci. Rep. 34(6), e00160 (2014)
45. M. Baranowski, Biological role of liver X receptors. J. Physiol. Pharmacol. 59(Suppl 7), 31–55 (2008)
46. S.D. Lee, P. Tontonoz, Liver X receptors at the intersection of lipid metabolism and atherogenesis. Atherosclerosis 242(1), 29–36 (2015)
47. B.A. Laffitte, L.C. Chao, J. Li, R. Walczak, S. Hummasti, S.B. Josephm, A. Castrillo, D.C. Wilpitz, D.J. Mangelsdorf, J.L. Collins, E. Saez, P. Tontonoz, Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. USA 100(9), 5419–5424 (2003)
48. R. Kaplan, T. Zhang, M. Hernandez, R.X. Gan, S.D. Wright, M.G. Waters, T.Q. Cai, Regulation of the angiopoietin-like protein 3 gene by LXR. J. Lipid Res. 44(1), 136–143 (2003)
49. T. Inaba, M. Matsuda, M. Shimamura, N. Takei, N. Terasaka, Y. Ando, H. Yasumo, R. Koishi, M. Makishima, I. Shimomura, Angiopoietin-like protein 3 mediates hypertriglyceridemia induced by the liver X receptor. J. Biol. Chem. 278(24), 21344–21351 (2003)
50. S.M. Choi, D.F. Tucker, D.N. Gross, R.M. Easton, L.M. DiPilato, A.S. Dean, B.R. Monks, M.J. Birnbaum, Insulin regulates adipocyte lipolysis via an Akt-independent signaling pathway. Mol. Cell Biol. 30(21), 5009–5020 (2010)
51. M. Shimamura, M. Matsuda, S. Kobayashi, Y. Ando, M. Ono, R. Koishi, H. Furukawa, M. Makishima, I. Shimomura, Angiopoietin-like protein 3, a hepatic secretory factor, activates lipolysis in adipocytes. Biochem. Biophys. Res. Commun. 301(2), 604–609 (2003)
52. F.K. Welty, Hypobetalipoproteinemia and abetalipoproteinemia. Curr. Opin. Lipidol. 25(3), 161–168 (2014)
53. J.I. Pulai, R.J. Neuman, A.W. Groenewegen, J. Wu, G. Schonfeld, Genetic heterogeneity in familial hypobetalipoproteinemia: linkage and non-linkage to the apoB gene in Caucasian families. Am. J. Med. Genet. 76, 79–86 (1998)
54. V. Gusarova, C.A. Alexa, Y. Wang, A. Rafique, J.H. Kim, D. Buckler, I.J. Mintah, L.M. Shihanian, J.C. Cohen, H.H. Hobbs, Y. Xin, D.M. Valenzuela, A.J. Murphy, G.D. Yancopoulos, J. Gromada, ANGPTL3 blockade with a human monoclonal antibody reduces plasma lipids in dyslipidemic mice and monkeys. J. Lipid Res. 56(7), 1308–1317 (2015)