Effects of angiopoietin-like protein 3 deficiency on postprandial lipid and lipoprotein metabolism

Journal of Lipid Research

Volumn 57, Issue 6, 2016, Pages 1097-1107

  Minicocci, Ilenia ^a   Tikka, Anna ^b   Poggiogalle, Eleonora ^a   Metso, Jari ^b   Montali, Anna ^a   Ceci, Fabrizio ^a   Labbadia, Giancarlo ^a   Fontana, Mario ^a   Costanzo, Alessia Di ^a   Maranghi, Marianna ^a   Rosano, Aldo ^c   Ehnholm, Christian ^b   Donini, Lorenzo Maria ^a   Jauhiainen, Matti ^b   Arca, Marcello ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^c ISFOL   (Italy)

Author keywords

Familial combined hypolipidemia; Free fatty acids; Postprandial lipid metabolism

Indexed keywords

3 HYDROXYBUTYRIC ACID; ANGIOPOIETIN; ANGIOPOIETIN LIKE PROTEIN 3; APOLIPOPROTEIN B48; FATTY ACID; LIPID; LIPOPROTEIN; UNCLASSIFIED DRUG; ANGPTL3 PROTEIN, HUMAN; TRIACYLGLYCEROL;

ADULT; AGED; ANGIOPOIETIN LIKE PROTEIN 3 DEFICIENCY; ANGPTL3 GENE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; GENE; GENE MUTATION; HETEROZYGOTE; HOMOZYGOTE; HUMAN; HYPERLIPIDEMIA; HYPOLIPEMIA; LIPID ANALYSIS; LIPID METABOLISM; LIPOPROTEIN METABOLISM; MALE; POSTPRANDIAL STATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; BLOOD; DEFICIENCY; GENETICS; HYPOBETALIPOPROTEINEMIA; MIDDLE AGED; MUTATION; PATHOLOGY;

ANGIOPOIETINS; APOLIPOPROTEIN B-48; FATTY ACIDS, NONESTERIFIED; FEMALE; HETEROZYGOTE; HOMOZYGOTE; HUMANS; HYPOBETALIPOPROTEINEMIAS; LIPIDS; LIPOPROTEINS; MALE; MIDDLE AGED; MUTATION; POSTPRANDIAL PERIOD; TRIGLYCERIDES;

EID: 84971542658     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P066183     Document Type: Article

References (52)

1. Sarwar, N., J. Danesh, G. Eiriksdottir, G. Sigurdsson, N. Wareham, S. Bingham, S. M. Boekholdt, K. T. Khaw, and V. Gudnason. 2007. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 115: 450-458.
2. Miller, M., N. J. Stone, C. Ballantyne, V. Bittner, M. H. Criqui, H. N. Ginsberg, A. C. Goldberg, W. J. Howard, M. S. Jacobson, P. M. Kris-Etherto, et al. 2011. Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation. 123: 2292-2333.
3. Rosenson, R. S., M. H. Davidson, B. J. Hirsh, S. Kathiresan, and D. Gaudet. 2014. Genetics and causality of triglyceride-rich lipoproteins in atherosclerotic cardiovascular disease. J. Am. Coll. Cardiol. 64: 2525-2540.
4. Mattijssen, F., and S. Kersten. 2012. Regulation of triglyceride metabolism by angiopoietin-like proteins. Biochim. Biophys. Acta. 1821: 782-789.
5. Kersten, S., S. Mandard, N. S. Tan, P. Escher, D. Metzger, P. Chambon, F. J. Gonzalez, B. Desvergne, and W. Wahli. 2000. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275: 28488-28493.
6. Ge, H., J. Y. Cha, H. Gopal, C. Harp, X. Yu, J. J. Repa, and C. Li. 2005. Differential regulation and properties of angiopoietin-like proteins 3 and 4. J. Lipid Res. 46: 1484-1490.
7. Inaba, T., M. Matsuda, M. Shimamura, N. Takei, N. Terasaka, Y. Ando, H. Yasumo, R. Koishi, M. Makishima, and I. Shimomura. 2003. Angiopoietin-like protein 3 mediates hypertriglyceridemia induced by the liver X receptor. J. Biol. Chem. 278: 21344-21351.
8. Inukai, K., Y. Nakashima, M. Watanabe, S. Kurihara, T. Awata, H. Katagiri, Y. Oka, and S. Katayama. 2004. ANGPTL3 is increased in both insulin-deficient and -resistant diabetic states. Biochem. Biophys. Res. Commun. 317: 1075-1079.
9. Yoshida, K., T. Shimizugawa, M. Ono, and H. Furukawa. 2002. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J. Lipid Res. 43: 1770-1772.
10. Shimizugawa, T., M. Ono, M. Shimamura, K. Yoshida, Y. Ando, R. Koishi, K. Ueda, T. Inaba, H. Minekura, T. Kohama, et al. 2002. ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase. J. Biol. Chem. 277: 33742-33748.
11. Wang, H., and R. H. Eckel. 2009. Lipoprotein lipase: from gene to obesity. Am. J. Physiol. Endocrinol. Metab. 297: E271-E288.
12. Köster, A., Y. B. Chao, M. Mosior, A. Ford, P. A. Gonzalez-DeWhitt, J. E. Hale, D. Li, Y. Qiu, C. C. Fraser, D. D. Yang, et al. 2005. Transgenic angiopoietin-like (angptl) 4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology. 146: 4943-4950.
13. Musunuru, K., J. P. Pirruccello, R. Do, G. M. Peloso, C. Guiducci, C. Sougnez, K. V. Garimella, S. Fisher, J. Abreu, A. J. Barry, et al. 2010. Exome sequencing, ANGPTL3 mutations, and familial combined hypolipidemia. N. Engl. J. Med. 363: 2220-2227.
14. Arca, M., I. Minicocci, and M. Maranghi. 2013. The angiopoietinlike protein 3: a hepatokine with expanding role in metabolism. Curr. Opin. Lipidol. 24: 313-320.
15. Tikka, A., J. Soronen, P. P. Laurila, J. Metso, C. Ehnholm, and M. Jauhiainen. 2014. 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: e00160.
16. Shimamura, M., M. Matsuda, H. Yasumo, M. Okazaki, K. Fujimoto, K. Kono, T. Shimizugawa, Y. Ando, R. Koishi, T. Kohama, et al. 2007. Angiopoietin-like protein3 regulates plasma HDL cholesterol through suppression of endothelial lipase. Arterioscler. Thromb. Vasc. Biol. 27: 366-372.
17. Robciuc, M. R., M. Maranghi, A. Lahikainen, D. Rader, A. Bensadoun, K. Öörni, J. Metso, I. Minicocci, E. Ciociola, F. Ceci, et al. 2013. Angptl3 deficiency is associated with increased insulin sensitivity, lipoprotein lipase activity, and decreased serum free fatty acids. Arterioscler. Thromb. Vasc. Biol. 33: 1706-1713.
18. Minicocci, I., A. Montali, M. R. Robciuc, F. Quagliarini, V. Censi, G. Labbadia, C. Gabiati, G. Pigna, M. L. Sepe, F. Pannozzo, et al. 2012. Mutations in the ANGPTL3 gene and familial combined hypolipidemia: a clinical and biochemical characterization. J. Clin. Endocrinol. Metab. 97: E1266-E1275.
19. Miles, J. M., and R. H. Nelson. 2007. Contribution of triglyceriderich lipoproteins to plasma free fatty acids. Horm. Metab. Res. 39: 726-729.
20. Rye, K. A., and P. J. Barter. 2004. Formation and metabolism of prebeta-migrating, lipid-poor apolipoprotein A-I. Arterioscler. Thromb. Vasc. Biol. 24: 421-428.
21. Centro di Ricerca per gli Alimenti e la Nutrizione, Rome, Italy. Accessed May, 5, 2015, at http://nut.entecra.it/646/tabelle-di- composizione-degli-alimenti.html.
22. Craig, C. L., A. L. Marshall, M. Sjöström, A. E. Bauman, M. L. Booth, B. E. Ainsworth, M. Pratt, U. Ekelund, A. Yngve, J. F. Sallis, et al. 2003. International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc. 35: 1381-1395.
23. Kyle, U. G., I. Bosaeus, A. D. De Lorenzo, P. Deurenberg, M. Elia, J. Manuel Gómez, B. Lilienthal Heitmann, L. Kent-Smith, J. C. Melchior, M. Pirlich, et al; ESPEN Working Group. 2004. Bioelectrical impedance analysis-part II: utilization in clinical practice. Clin. Nutr. 23: 1430-1453.
24. Sun, S. S., W. C. Chumlea, S. B. Heymsfield, H. C. Lukaski, D. Schoeller, K. Friedl, R. J. Kuczmarski, K. M. Flegal, C. L. Johnson, and V. S. Hubbard. 2003. Development of bioelectrical impedance analysis prediction equations for body composition with the use of a multicomponent model for use in epidemiologic surveys. Am. J. Clin. Nutr. 77: 331-340.
25. Kolovou, G. D., D. P. Mikhailidis, J. Kovar, D. Lairon, B. G. Nordestgaard, T. C. Ooi, P. Perez-Martinez, H. Bilianou, K. Anagnostopoulou, and G. Panotopoulos. 2011. Assessment and clinical relevance of non-fasting and postprandial triglycerides: an expert panel statement. Curr. Vasc. Pharmacol. 9: 258-270.
26. Lairon, D., J. Lopez-Miranda, and C. Willimas. 2007. Methodology for studying postprandial lipid metabolism. Eur. J. Clin. Nutr. 61: 1145-1161.
27. Demacker, P. N., M. P. Hectors, and A. F. Stalenhoef. 2000. Chylomicron processing in familial dysbetalipoproteinemia and familial combined hyperlipidemia studied with vitamin A and E as markers: a new physiological concept. Atherosclerosis. 149: 169-180.
28. Haugen, H. A., L-N. Chan, and F. Li. 2007. Indirect calorimetry: a practical guide for clinicians. Nutr. Clin. Pract. 22: 377-388.
29. Cunningham, J. J. 1990. Calculation of energy expenditure from indirect calorimetry: assessment of the Weir equation. Nutrition. 6: 222-223.
30. Levine, J. A. 2005. Measurement of energy expenditure. Public Health Nutr. 8: 1123-1132.
31. Arca, M., A. Montali, S. Valiante, F. Campagna, G. Pigna, V. Paoletti, R. Antonini, F. Barillà, G. Tanzilli, A. Vestri, et al. 2007. Usefulness of atherogenic dyslipidemia for predicting cardiovascular risk in patients with angiographically defined coronary artery disease. Am. J. Cardiol. 100: 1511-1516.
32. DeRuyter, M. G., and A. P. De Leenheer. 1978. Simultaneous determination of retinol and retinyl esters in serum or plasma by reversed-phase high performance liquid chromatography. Clin. Chem. 24: 1920-1923.
33. Kleemola, P., R. Freese, M. Jauhiainen, R. Pahlman, G. Alfthan, and M. Mutanen. 2002. Dietary determinants of serum paraoxonase activity in healthy humans. Atherosclerosis. 160: 425-432.
34. Jauhiainen, M., and C. Ehnholm. 2005. Determination of human plasma phospholipid transfer protein mass and activity. Methods. 36: 97-101.
35. Groener, J. E. J., R. W. Pelton, and G. M. Kostner. 1986. Improved estimation of cholesteryl ester transfer/exchange activity in serum or plasma. Clin. Chem. 32: 283-286.
36. Vikstedt, R., J. Metso, J. Hakala, V. M. Olkkonen, C. Ehnholm, and M. Jauhiainen. 2007. Cholesterol efflux from macrophage foam cells is enhanced by active phospholipid transfer protein through generation of two types of acceptor particles. Biochemistry. 46: 11979-11986.
37. Jackson, K. G., S. D. Poppitt, and A. M. Minihane. 2012. Postprandial lipemia and cardiovascular disease risk: interrelationships between dietary, physiological and genetic determinants. Atherosclerosis. 220: 22-33.
38. Minicocci, I., C. Prisco, A. Montali, A. Di Costanzo, G. Pigna, and M. Arca. 2015. Contribution of rare and common variants in low-density lipoprotein receptor (LDLR) and lipoprotein lipase (LPL) genes to familial combined hyperlipidemia (FCHL): a reappraisal by using a resequencing approach. Atherosclerosis. 242: 618-624.
39. Kersten, S. 2014. Physiological regulation of lipoprotein lipase. Biochim. Biophys. Acta. 1841: 919-933.
40. Cohn, J. S., E. J. Johnson, J. S. Millar, S. D. Cohn, R. W. Milne, Y. L. Marcel, R. M. Russell, and E. J. Schaefer. 1993. Contribution of apoB-48 and apoB-100 triglyceride-rich lipoproteins (TRL) to postprandial increases in the plasma concentration of TRL triglycerides and retinyl esters. J. Lipid Res. 34: 2033-2040.
41. Nosadini, R., A. Avogaro, R. Trevisan, E. Duner, C. Marescotti, E. Iori, C. Cobelli, and G. Toffolo. 1985. Acetoacetate and 3-hydroxybutyrate kinetics in obese and insulin-dependent diabetic humans. Am. J. Physiol. 248: R611-R620.
42. Matikainen, N., M. Adiels, S. Söderlund, S. Stennabb, T. Ahola, A. Hakkarainen, J. Borén, and M. R. Taskinen. 2014. Hepatic lipogenesis and a marker of hepatic lipid oxidation, predict postprandial responses of triglyceride-rich lipoproteins. Obesity (Silver Spring). 22: 1854-1859.
43. Gusarova, V., C. A. Alexa, Y. Wang, A. Rafique, J. H. Kim, D. Buckler, I. J. Mintah, L. M. Shihanian, J. C. Cohen, H. H. Hobbs, et al. 2015. ANGPTL3 blockade with a human monoclonal antibody reduces plasma lipids in dyslipidemic mice and monkeys. J. Lipid Res. 56: 1308-1317.
44. Barrows, B. R., M. T. Timlin, and E. J. Parks. 2005. Spillover of dietary fatty acids and use of serum nonesterified fatty acids for the synthesis of VLDL-triacylglycerol under two different feeding regimens. Diabetes. 54: 2668-2673.
45. Shimamura, M., M. Matsuda, S. Kobayashi, Y. Ando, M. Ono, R. Koishi, H. Furukawa, M. Makishima, and I. Shimomura. 2003. Angiopoietin-like protein 3, a hepatic secretory factor, activates lipolysis in adipocytes. Biochem. Biophys. Res. Commun. 301: 604-609.
46. Meijssen, S., M. Castro Cabezas, T. B. Twickler, H. Jansen, and D. W. Erkelens. 2000. In vivo evidence of defective postprandial and postabsorptive free fatty acid metabolism in familial combined hyperlipidemia. J. Lipid Res. 41: 1096-1102.
47. Wang, Y., M. C. McNutt, S. Banfi, M. G. Levin, W. L. Holland, V. Gusarova, J. Gromada, J. C. Cohen, and H. H. Hobbs. 2015. Hepatic ANGPTL3 regulates adipose tissue energy homeostasis. Proc. Natl. Acad. Sci. USA. 112: 11630-11635.
48. Wang, Y., V. Gusarova, S. Banfi, J. Gromada, J. C. Cohen, and H. H. Hobbs. 2015. Inactivation of ANGPTL3 reduces hepatic VLDLtriglyceride secretion. J. Lipid Res. 56: 1296-1307.
49. Zannis, V. I., P. Fotakis, G. Koukos, D. Kardassis, C. Ehnholm, M. Jauhiainen, and A. Chroni. 2015. HDL biogenesis, remodeling, and catabolism. Handb. Exp. Pharmacol. 224: 53-111.
50. Ono, M., T. Shimizugawa, M. Shimamura, K. Yoshida, C. Noji-Sakikawa, Y. Ando, R. Koish, and H. Furukawa. 2003. Protein region important for regulation of lipid metabolism in angiopoietin-like 3 (ANGPTL3): ANGPTL3 is cleaved and activated in vivo. J. Biol. Chem. 278: 41804-41809.
51. Haridas, P. A., J. Soronen, S. Sädevirta, R. Mysore, F. Quagliarini, A. Pasternack, J. Metso, J. Perttilä, M. Leivonen, C. M. Smas, et al. 2015. Regulation of angiopoietin-like proteins (ANGPTLs) 3 and 8 by insulin. J. Clin. Endocrinol. Metab. 100: E1299-E1307.
52. Arca, M. 2015. Alterations of intestinal lipoprotein metabolism in diabetes mellitus and metabolic syndrome. Atherosclerosis. 17: 12-16.