Human apolipoprotein C-III - A new intrahepatic protein factor promoting assembly and secretion of very low density lipoproteins

Cardiovascular and Hematological Disorders - Drug Targets

Volumn 12, Issue 2, 2012, Pages 133-140

  Yao, Zemin ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

ApoC3; Atherosclerosis; Hyperalphalipoproteinemia; Hypotriglyceridemia; VLDL

Indexed keywords

APOLIPOPROTEIN C3; FAT DROPLET; GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ARTICLE; ATHEROSCLEROSIS; FRAMESHIFT MUTATION; GENETIC ASSOCIATION; HUMAN; HYPERTRIGLYCERIDEMIA; LIPOLYSIS; LIVER MICROSOME; MISSENSE MUTATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN HOMEOSTASIS; PROTEIN SECRETION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; APOLIPOPROTEIN C-III; HUMANS; LIPOPROTEINS, VLDL; LIVER;

EID: 84874928399     PISSN: 1871529X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1871529X11202020133     Document Type: Article

References (55)

1. Olofsson, S.O.; Boren, J. Apolipoprotein B: a clinically important apolipoprotein which assembles atherogenic lipoproteins and promotes the development of atherosclerosis. J. Intern. Med., 2005, 258, 395-410.
2. Pollin, T.I.; Damcott, C.M.; Shen, H.; Ott, S.H.; Shelton, J.; Horenstein, R.B.; Post, W.; McLenithan, J.C.; Bielak, L.F.; Peyser, P.A.; Mitchell, B.D.; Miller, M.; O'Connell, J.R.; Shuldiner, A.R. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science, 2008, 322, 1702-1705.
3. Ito, Y.; Azrolan, N.; O'Connell, A.; Walsh, A.; Breslow, J.L. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science, 1990, 249, 790-793.
4. Maeda, N.; Li, H.; Lee, D.; Oliver, P.; Quarfordt, S.H.; Osada, J. Targeted disruption of the apolipoprotein C-III gene in mice results in hypotriglyceridemia and protection from postprandial hypertriglyceridemia. J. Biol. Chem., 1994, 269, 23610-23616.
5. Cohn, J.S.; Tremblay, M.; Batal, R.; Jacques, H.; Rodriguez, C.; Steiner, G.; Mamer, O.; Davignon, J. Increased apoC-III production is a characteristic feature of patients with hypertriglyceridemia. Atherosclerosis, 2004, 177, 137-145.
6. Zheng, C.; Khoo, C.; Ikewaki, K.; Sacks, F.M. Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions. J. Lipid Res., 2007, 48, 1190-1203.
7. Qin, W.; Sundaram, M.; Wang, Y.; Zhou, H.; Zhong, S.; Chang, C.-C.; Manhas, S.; Yao, E.F.; Parks, R.J.; McFie, P.J.; Stone, S.J.; Jiang, Z.J.; Wang, C.; Figeys, D.; Jia, W.; Yao, Z. Missense Mutation in APOC3 within the C-terminal Lipid-binding Domain of Human apoC-III Results in Impaired Assembly and Secretion of Triacylglycerol-rich Very Low Density Lipoproteins. EVIDENCE THAT APOC-III PLAYS A MAJOR ROLE IN THE FORMATION OF LIPID PRECURSORS WITHIN THE MICROSOMAL LUMEN. J. Biol. Chem., 2011, 286, 27769-27780
8. Sundaram, M.; Zhong, S.; Bou Khalil, M.; Zhou, H.; Jiang, Z.J.; Zhao, Y.; Iqbal, J.; Hussain, M.M.; Figeys, D.; Wang, Y.; Yao, Z. Functional analysis of the missense APOC3 mutation Ala23Thr associated with human hypotriglyceridemia. J. Lipid Res., 2010, 51, 1524-1534.
9. Sundaram, M.; Zhong, S.; Bou Khalil, M.; Links, P.H.; Zhao, Y.; Iqbal, J.; Hussain, M.M.; Parks, R.J.; Wang, Y.; Yao, Z. Expression of apolipoprotein C-III in McA-RH7777 cells enhances VLDL assembly and secretion under lipid-rich conditions. J. Lipid Res., 2010, 51, 150-161.
10. Sundaram, M.; Yao, Z. Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr. Metab. (Lond), 2010, 7, 35.
11. Quiroga, A.D.; Lehner, R. Role of endoplasmic reticulum neutral lipid hydrolases. Trends Endocrinol. Metab., 2011, 22, 218-225.
12. Tran, K.; Wang, Y.; DeLong, C.J.; Cui, Z.; Yao, Z. The assembly of very low density lipoproteins in rat hepatoma McA-RH7777 cells is inhibited by phospholipase A2 antagonists. J. Biol. Chem., 2000, 275, 25023-25030.
13. Tran, K.; Sun F.; Cui, Z.; Thorne-Tjomsland, G.; St Germain, C.; Lapierre, L.R.; McLeod, R.S.; Jamieson, J.C.; Yao, Z. Attenuated secretion of very low density lipoproteins from McA-RH7777 cells treated with eicosapentaenoic acid is associated with impaired utilization of triacylglycerol synthesized via phospholipid remodeling. Biochim. Biophys. Acta, 2006, 1761, 463-473.
14. Farese, R.V.; Jr, Walther, T.C. Lipid droplets finally get a little RE-S-P-E-C-T. Cell, 139: 855-860.
15. Gilham, D.; Lehner, R. The physiological role of triacylglycerol hydrolase in lipid metabolism. Rev. Endocr. Metab Disord., 2009, 5, 303-309.
16. Magnusson, B.; Asp, L.; Bostrom, P.; Ruiz, M.; Stillemark-Billton, P.; Linden, D.; Boren, J.; Olofsson S.-O. Adipocyte differentiation-related protein promotes fatty acid storage in cytosolic triglycerides and inhibits secretion of very low-density lipoproteins. Arterioscler. Thromb. Vasc. Biol., 2006, 26, 1566-1571.
17. Ye, J.; Li, J.Z.; Liu, Y.; Li, X.; Yang, T.; Ma, X.; Li, Q.; Yao, Z.; Li, P. Cideb, an ER-and lipid droplet-associated protein, mediates VLDL lipidation and maturation by interacting with apolipoprotein B. Cell Metab., 2009, 9, 177-190.
18. Schonfeld, G. Familial hypobetalipoproteinemia: a review. J. Lipid Res., 2003, 44, 878-883.
19. Yao, Z.; McLeod, R.S. Synthesis and secretion of hepatic apolipoprotein B-containing lipoproteins. Biochim. Biophys. Acta, 1994, 1212, 152-166.
20. McLeod, R.S.; Zhao, Y.; Selby, S.L.; Westerlund, J.; Yao, Z. Carboxyl-terminal truncation impairs lipid recruitment by apolipoprotein B100 but does not affect secretion of the truncated apolipoprotein B-containing lipoproteins. J. Biol. Chem., 1994, 269, 2852-2862.
21. Jiang, Z.G.; Gantz, D.; Bullitt, E.; McKnight, C.J. Defining lipidinteracting domains in the N-terminal region of apolipoprotein B. Biochemistry, 2006, 45, 11799-11808.
22. Burnett, J.R.; Shan, J.; Miskie, B.A.; Whitfield, A.J.; Yuan, J.; Tran, K.; McKnight, C.J.; Hegele, R.A.; Yao, Z. A novel nontruncating APOB gene mutation, R463W, causes familial hypobetalipoproteinemia. J. Biol. Chem., 2003, 278, 13442-13452.
23. Burnett, J.R.; Zhong, S.; Jiang, Z.J.; Hooper, A.J.; Fisher, E.A.; McLeod, R.S.; Zhao, Y.; Barrett, P.H.; Hegele, R.A.; van Bockxmeer, F.M.; Zhang, H.; Vance, D.E.; McKnight, C.J.; Yao, Z. Missense mutations in APOB within the betaalpha1 domain of human APOB-100 result in impaired secretion of ApoB and ApoBcontaining lipoproteins in familial hypobetalipoproteinemia. J. Biol. Chem., 2007, 282, 24270-24283.
24. Zhong, S.; Magnolo, A.L.; Sundaram, M.; Zhou, H.; Yao, E.F.; Di Leo, E.; Loria, P.; Wang, S.; Bamji-Mirza, M.; Wang, L.; McKnight, C.J.; Figeys, D.; Wang, Y.; Tarugi, P.; Yao, Z. Nonsynonymous mutations within APOB in human familial hypobetalipoproteinemia: evidence for feedback inhibition of lipogenesis and postendoplasmic reticulum degradation of apolipoprotein B. J. Biol. Chem., 2010, 285, 6453-6464.
25. Hussain, M.M.; Shi, J.; Dreizen, P. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res., 2003, 44, 22-32.
26. Wang, Y.; Tran, K.; Yao, Z. The activity of microsomal triglyceride transfer protein is essential for accumulation of triglyceride within microsomes in McA-RH7777 cells. A unified model for the assembly of very low density lipoproteins. J. Biol. Chem., 1999, 274, 27793-27800.
27. Gusarova, V.; Brodsky, J.L.; Fisher, E.A. Apolipoprotein B100 exit from the endoplasmic reticulum (ER) is COPII-dependent, and its lipidation to very low density lipoprotein occurs post-ER. J. Biol. Chem., 2003, 278, 48051-48058.
28. Gusarova, V.; Seo, J.; Sullivan, M.L.; Watkins, S.C.; Brodsky, J.L.; Fisher, E.A. Golgi-associated maturation of very low density lipoproteins involves conformational changes in apolipoprotein B, but is not dependent on apolipoprotein E. J. Biol. Chem., 2007, 282, 19453-19462.
29. Tran, K.; Thorne-Tjomsland, G.; DeLong, C.J.; Cui, Z.; Shan, J.; Burton, L.; Jamieson, J.C.; Yao, Z. Intracellular assembly of very low density lipoproteins containing apolipoprotein B100 in rat hepatoma McA-RH7777 cells. J. Biol. Chem., 2002, 277, 31187-31200.
30. Gangabadage, C.S.; Zdunek, J.; Tessari, M.; Nilsson, S.; Olivecrona, G.; Wijmenga, S.S. Structure and Dynamics of Human Apolipoprotein CIII. J. Biol. Chem., 2008, 283, 17416-17427.
31. Ginsberg, H.N.; Brown, W.V. Apolipoprotein CIII: 42 years old and even more interesting. Arterioscler. Thromb. Vasc. Biol., 2011, 31, 471-473.
32. Jong, M.C.; Hofker, M.H.; Havekes, L.M. Role of ApoCs in lipoprotein metabolism: functional differences between ApoC1, ApoC2, and ApoC3. Arterioscler. Thromb. Vasc. Biol., 1999, 19, 472-484.
33. Aalto-Setala, K.; Weinstock, P.H.; Bisgaier, C.L.; Wu, L.; Smith, J.D.; Breslow, J.L. Further characterization of the metabolic properties of triglyceride-rich lipoproteins from human and mouse apoC-III transgenic mice. J. Lipid Res., 1996, 37, 1802-1811.
34. Cohn, J.S.; Patterson, B.W.; Uffelman, K.D.; Davignon, J.; Steiner, G. Rate of production of plasma and very-low-density lipoprotein (VLDL) apolipoprotein C-III is strongly related to the concentration and level of production of VLDL triglyceride in male subjects with different body weights and levels of insulin sensitivity. J. Clin. Endocrinol. Metab., 2004, 89, 3949-3955.
35. Liu, H.; Labeur, C.; Xu, C.F.; Ferrell, R.; Lins, L.; Brasseur, R.; Rosseneu, M.; Weiss, K.M.; Humphries, S.E.; Talmud, P.J. Characterization of the lipid-binding properties and lipoprotein lipase inhibition of a novel apolipoprotein C-III variant Ala23Thr. J. Lipid Res., 2000, 41, 1760-1771.
36. von Eckardstein, A.; Holz, H.; Sandkamp, M.; Weng, W.; Funke, H.; Assmann, G. Apolipoprotein C-III(Lys58-Glu). Identification of an apolipoprotein C-III variant in a family with hyperalphalipoproteinemia. J. Clin. Invest., 1991, 87, 1724-1731.
37. Sparrow, J.T.; Gotto, A.M. Jr, Morrisett, J.D. Chemical synthesis and biochemical properties of peptide fragments of apolipoproteinalanine. Proc. Natl. Acad. Sci. USA, 1973, 70, 2124-2128.
38. Sparrow, J.T.; Pownall, H.J.; Hsu, F.J.; Blumenthal, L.D.; Culwell, A.R.; Gotto, A.M. Lipid binding by fragments of apolipoprotein CIII-1 obtained by thrombin cleavage. Biochemistry, 1977, 16, 5427-5431.
39. Lins, L.; Flore, C.; Chapelle, L.; Talmud, P.J.; Thomas, A.; Brasseur, R. Lipid-interacting properties of the N-terminal domain of human apolipoprotein C-III. Protein Eng., 2002, 15, 513-520.
40. Liu, H.; Talmud, P.J.; Lins, L.; Brasseur, R.; Olivecrona, G.; Peelman, F.; Vandekerckhove, J.; Rosseneu, M.; Labeur, C. Characterization of recombinant wild type and site-directed mutations of apolipoprotein C-III: lipid binding, displacement of ApoE, and inhibition of lipoprotein lipase. Biochemistry, 2000, 39, 9201-9212.
41. Petersen, K.F.; Dufour, S.; Hariri, A.; Nelson-Williams, C.; Foo, J.N.; Zhang, X.M.; Dziura, J.; Lifton, R.P.; Shulman, G.I. Apolipoprotein C3 gene variants in nonalcoholic fatty liver disease. N. Engl. J. Med., 2010, 362, 1082-1089.
42. Altomonte, J.; Cong, L.; Harbaran, S.; Richter, A.; Xu, J.; Meseck, M.; Dong, H.H. Foxo1 mediates insulin action on apoC-III and triglyceride metabolism. J. Clin. Invest., 2004, 114, 1493-1503.
43. Hernandez, C.; Molusky, M.; Li, Y.; Li, S.; Lin, J.D. Regulation of hepatic ApoC3 expression by PGC-1beta mediates hypolipidemic effect of nicotinic acid. Cell Metab., 2010, 12, 411-419.
44. Caron, S.; Verrijken, A.; Mertens, I.; Samanez, C.H.; Mautino, G.; Haas, J.T.; Duran-Sandoval, D.; Prawitt, J.; Francque, S.; Vallez, E.; Muhr-Tailleux, A.; Berard, I.; Kuipers, F.; Kuivenhoven, J.A.; Biddinger, S.B.; Taskinen, M.R.; Van Gaal L.; Staels, B. 2011. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol., 2011, 31, 513-519.
45. Batal, R.; Tremblay, M.; Barrett, P.H.; Jacques, H.; Fredenrich, A.; Mamer, O.; Davignon, J.; Cohn, J.S. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. J. Lipid Res., 2000, 41, 706-718.
46. Chan, D.C.; Nguyen, M.N.; Watts, G.F.; Barrett, P.H. Plasma apolipoprotein C-III transport in centrally obese men: associations with very low-density lipoprotein apolipoprotein B and highdensity lipoprotein apolipoprotein A-I metabolism. J. Clin. Endocrinol. Metab., 2008, 93, 557-564.
47. Zheng, C.; Khoo, C.; Furtado, J.; Ikewaki, K.; Sacks, F.M. Dietary monounsaturated fat activates metabolic pathways for triglyceriderich lipoproteins that involve apolipoproteins E and C-III. Am. J. Clin. Nutr., 2008, 88, 272-281.
48. Chan, D.C.; Watts, G.F.; Nguyen, M.N.; Barrett, P.H. Apolipoproteins C-III and A-V as predictors of very-low-density lipoprotein triglyceride and apolipoprotein B-100 kinetics. Arterioscler. Thromb. Vasc. Biol., 2006, 26, 590-596.
49. Ginsberg, H.N.; Ramakrishnan, R. Kinetic studies of the metabolism of rapidly exchangeable apolipoproteins may leave investigators and readers with exchangeable results. Arterioscler. Thromb. Vasc. Biol., 2008, 28, 1685-1686.
50. Sacks, F.M.; Zheng, C.; Cohn, J.S. Complexities of plasma apolipoprotein C-III metabolism. J. Lipid Res., 2011, 52, 1067-1070.
51. Ginsberg, H.N.; Ramakrishnan, R. Investigations of apoC-III metabolism using stable isotopes: what information can you acquire and how can you interpret your results? J. Lipid Res., 2011, 52, 1071-1072.
52. Aalto-Setala, K.; Fisher, E.A.; Chen, X.; Chajek-Shaul, T.; Hayek, T.; Zechner, R.; Walsh, A.; Ramakrishnan, R.; Ginsberg, H.N.; Breslow, J.L. Mechanism of hypertriglyceridemia in human apolipoprotein (apo) CIII transgenic mice. Diminished very low density lipoprotein fractional catabolic rate associated with increased apo CIII and reduced apo E on the particles. J. Clin. Invest., 1992, 90, 1889-1900.
53. Jong, M.C.; Rensen, P.C.; Dahlmans, V.E.; van der Boom, H.; van Berkel, T.J.; Havekes, L.M. 2001. Apolipoprotein C-III deficiency accelerates triglyceride hydrolysis by lipoprotein lipase in wildtype and apoE knockout mice. J. Lipid Res., 2001, 42, 1578-1585.
54. Duivenvoorden, I.; Teusink, B.; Rensen, P.C.; Romijn, J.A.; Havekes, L.M.; Voshol, P.J. Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice. Diabetes, 2005, 54, 664-671.
55. Pavlic, M.; Valero, R.; Duez, H.; Xiao, C.; Szeto, L.; Patterson, B.W.; Lewis, G.F. Triglyceride-rich lipoprotein-associated apolipoprotein C-III production is stimulated by plasma free fatty acids in humans. Arterioscler. Thromb. Vasc. Biol., 2008, 28, 1660-1665.