The regulation of ApoB metabolism by insulin

Trends in Endocrinology and Metabolism

Volumn 24, Issue 8, 2013, Pages 391-397

  Haas, Mary E ^a   Attie, Alan D ^b   Biddinger, Sudha B ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apolipoprotein B; Cardiovascular disease; Diabetes; Insulin; Selective insulin resistance; Very low density lipoprotein (VLDL)

Indexed keywords

APOLIPOPROTEIN B; INSULIN; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEOHEPARAN SULFATE;

HORMONAL REGULATION; HUMAN; LIVER METABOLISM; METABOLIC REGULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW;

EID: 84880934579     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2013.04.001     Document Type: Review

References (98)

1. Bornfeldt K.E., Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab. 2011, 14:575-585.
2. Gerstein H.C., et al. Effects of intensive glucose lowering in type 2 diabetes. N. Engl. J. Med. 2008, 358:2545-2559.
3. Stocker R., Keaney J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 2004, 84:1381-1478.
4. Collins R., et al. MRC/BHF Heart Protection Study of cholesterol-lowering with simvastatin in 5963 people with diabetes: a randomised placebo-controlled trial. Lancet 2003, 361:2005-2016.
5. Semenkovich C.F., et al. Disorders of lipid metabolism. Williams Textbook of Endocrinology 2011, 1633-1674. Elsevier/Saunders. 12th edn. S. Mehmed, R.H. Williams (Eds.).
6. Blasiole D.A., et al. The physiological and molecular regulation of lipoprotein assembly and secretion. Mol. Biosyst. 2007, 3:608-619.
7. Bamba V., Rader D.J. Obesity and atherogenic dyslipidemia. Gastroenterology 2007, 132:2181-2190.
8. Teusink B., et al. Contribution of fatty acids released from lipolysis of plasma triglycerides to total plasma fatty acid flux and tissue-specific fatty acid uptake. Diabetes 2003, 52:614-620.
9. Biddinger S.B., Kahn C.R. From mice to men: insights into the insulin resistance syndromes. Annu. Rev. Physiol. 2006, 68:123-158.
10. Li S., et al. Bifurcation of insulin signaling pathway in rat liver: mTORC1 required for stimulation of lipogenesis, but not inhibition of gluconeogenesis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3441-3446.
11. Choi S.H., Ginsberg H.N. Increased very low density lipoprotein (VLDL) secretion, hepatic steatosis, and insulin resistance. Trends Endocrinol. Metab. 2011, 22:353-363.
12. Dashti N., et al. Effects of oleate and insulin on the production rates and cellular mRNA concentrations of apolipoproteins in HepG2 cells. J. Lipid Res. 1989, 30:1365-1373.
13. Karimian Pour N., Adeli K. Insulin silences apolipoprotein B mRNA translation by inducing intracellular traffic into cytoplasmic RNA granules. Biochemistry 2011, 50:6942-6950.
14. Parker R., Sheth U. P bodies and the control of mRNA translation and degradation. Mol. Cell 2007, 25:635-646.
15. Sidiropoulos K.G., et al. Insulin inhibition of apolipoprotein B mRNA translation is mediated via the PI-3 kinase/mTOR signaling cascade but does not involve internal ribosomal entry site (IRES) initiation. Arch. Biochem. Biophys. 2007, 465:380-388.
16. Fisher E.A., Ginsberg H.N. Complexity in the secretory pathway: the assembly and secretion of apolipoprotein B-containing lipoproteins. J. Biol. Chem. 2002, 277:17377-17380.
17. Kamagate A., et al. FoxO1 mediates insulin-dependent regulation of hepatic VLDL production in mice. J. Clin. Invest. 2008, 118:2347-2364.
18. Bartels E.D., et al. Hepatic expression of microsomal triglyceride transfer protein and in vivo secretion of triglyceride-rich lipoproteins are increased in obese diabetic mice. Diabetes 2002, 51:1233-1239.
19. Sparks J.D., et al. Acute suppression of apo B secretion by insulin occurs independently of MTP. Biochem. Biophys. Res. Commun. 2011, 406:252-256.
20. Lin M.C., et al. Microsomal triglyceride transfer protein (MTP) regulation in HepG2 cells: insulin negatively regulates MTP gene expression. J. Lipid Res. 1995, 36:1073-1081.
21. Qiu W., et al. Overexpression of the endoplasmic reticulum 60 protein ER-60 downregulates apoB100 secretion by inducing its intracellular degradation via a nonproteasomal pathway: evidence for an ER-60-mediated and pCMB-sensitive intracellular degradative pathway. Biochemistry 2004, 43:4819-4831.
22. Morand J., et al. Proteomic profiling of hepatic endoplasmic reticulum-associated proteins in an animal model of insulin resistance and metabolic dyslipidemia. J. Biol. Chem. 2005, 280:17626-17633.
23. Pan M., et al. The late addition of core lipids to nascent apolipoprotein B100, resulting in the assembly and secretion of triglyceride-rich lipoproteins, is independent of both microsomal triglyceride transfer protein activity and new triglyceride synthesis. J. Biol. Chem. 2002, 277:4413-4421.
24. Brown A.M., Gibbons G.F. Insulin inhibits the maturation phase of VLDL assembly via a phosphoinositide 3-kinase-mediated event. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1656-1661.
25. Pollin T., et al. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science 2008, 322:1702-1705.
26. Ooi E.M.M., et al. Apolipoprotein C-III: understanding an emerging cardiovascular risk factor. Clin. Sci. 2008, 114:611-624.
27. Sundaram M., et al. Functional analysis of the missense APOC3 mutation Ala23Thr associated with human hypotriglyceridemia. J. Lipid Res. 2010, 51:1524-1534.
28. Aalto-Setälä K., et al. 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.
29. Caron S., et al. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol. 2011, 31:513-519.
30. Hernandez C., et al. Regulation of hepatic ApoC3 expression by PGC-1β mediates hypolipidemic effect of nicotinic acid. Cell Metab. 2010, 12:411-419.
31. Florez H., et al. Increased apolipoprotein C-III levels associated with insulin resistance contribute to dyslipidemia in normoglycemic and diabetic subjects from a triethnic population. Atherosclerosis 2006, 188:134-141.
32. Sparks J.D., et al. Insulin-mediated inhibition of apolipoprotein B secretion requires an intracellular trafficking event and phosphatidylinositol 3-kinase activation: studies with brefeldin A and wortmannin in primary cultures of rat hepatocytes. Biochem. J. 1996, 313(Pt 2):567-574.
33. Andreo U., et al. Insulin-stimulated degradation of Apolipoprotein B100: roles of class II phosphatidylinositol-3-kinase and autophagy. PLoS ONE 2013, 8:e57590.
34. Strong A., et al. Hepatic sortilin regulates both apolipoprotein B secretion and LDL catabolism. J. Clin. Invest. 2012, 122:2807-2816.
35. Chamberlain J.M., et al. Insulin suppression of apolipoprotein B in McArdle RH7777 cells involves increased sortilin 1 interaction and lysosomal targeting. Biochem. Biophys. Res. Commun. 2013, 430:66-71.
36. Hermey G. The Vps10p-domain receptor family. Cell. Mol. Life Sci. 2009, 66:2677-2689.
37. Dubé J.B., et al. Sortilin: an unusual suspect in cholesterol metabolism: from GWAS identification to in vivo biochemical analyses, sortilin has been identified as a novel mediator of human lipoprotein metabolism. Bioessays 2011, 33:430-437.
38. Ai D., et al. Activation of ER stress and mTORC1 suppresses hepatic sortilin-1 levels in obese mice. J. Clin. Invest. 2012, 122:20-22.
39. Williams K.J., et al. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins, Roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J. Biol. Chem. 1992, 267:13284-132892.
40. Sundaram M., Yao Z. Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr. Metab. 2010, 7:35.
41. Mazzone T., et al. In vivo stimulation of low-density lipoprotein degradation by insulin. Diabetes 1984, 33:333-338.
42. Howard B.V., et al. Integrated study of low density lipoprotein metabolism and very low density lipoprotein metabolism in non-insulin-dependent diabetes. Metabolism 1987, 36:870-877.
43. Kissebah A.H., et al. Plasma low density lipoprotein transport kinetics in noninsulin-dependent diabetes mellitus. J. Clin. Invest. 1983, 71:655-667.
44. Steinberg D. The LDL modification hypothesis of atherogenesis: an update. J. Lipid Res. 2009, 50(Suppl.):S376-S381.
45. Vergès B. Lipid modification in type 2 diabetes: the role of LDL and HDL. Fundam. Clin. Pharmacol. 2009, 23:681-685.
46. Adeli K., Lewis G.F. Intestinal lipoprotein overproduction in insulin-resistant states. Curr. Opin. Lipidol. 2008, 19:221-228.
47. Brown M.S., Goldstein J.L. Regulation of the activity of the low density lipoprotein receptor in human fibroblasts. Cell 1975, 6:307-316.
48. Chait A., et al. Regulatory role of insulin in the degradation of low density lipoprotein by cultured human skin fibroblasts. Biochim. Biophys. Acta 1978, 529:292-299.
49. Wade D.P., et al. Regulation of low-density-lipoprotein-receptor mRNA by insulin in human hepatoma Hep G2 cells. Eur. J. Biochem. 1989, 181:727-731.
50. Costet P., et al. Hepatic PCSK9 expression is regulated by nutritional status via insulin and sterol regulatory element-binding protein 1c. J. Biol. Chem. 2006, 281:6211-6218.
51. Niesen M., et al. Diabetes alters LDL receptor and PCSK9 expression in rat liver. Arch. Biochem. Biophys. 2008, 470:111-115.
52. Han S., et al. Hepatic insulin signaling regulates VLDL secretion and atherogenesis in mice. J. Clin. Invest. 2009, 119:1029-1041.
53. Biddinger S.B., et al. Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 2008, 7:125-134.
54. Lundasen T., et al. Leptin induces the hepatic high density lipoprotein receptor scavenger receptor B type I (SR-BI) but not cholesterol 7alpha-hydroxylase (Cyp7a1) in leptin-deficient (ob/ob) mice. J. Biol. Chem. 2003, 278:43224-43228.
55. Lambert G., et al. The PCSK9 decade. J. Lipid Res. 2012, 53:2515-2524.
56. Stein E., Mellis S. Effect of a monoclonal antibody to PCSK9 on LDL cholesterol. N. Engl. J. Med. 2012, 366:1108-1118.
57. Lillis A.P., et al. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol. Rev. 2008, 88:887-918.
58. Rohlmann A., et al. Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J. Clin. Invest. 1998, 101:689-695.
59. Laatsch A., et al. Insulin stimulates hepatic low density lipoprotein receptor-related protein 1 (LRP1) to increase postprandial lipoprotein clearance. Atherosclerosis 2009, 204:105-111.
60. Ko K.W., et al. The insulin-stimulated cell surface presentation of low density lipoprotein receptor-related protein in 3T3-L1 adipocytes is sensitive to phosphatidylinositide 3-kinase inhibition. Biochemistry 2001, 40:752-759.
61. Jedrychowski M.P., et al. Proteomic analysis of GLUT4 storage vesicles reveals LRP1 to be an important vesicle component and target of insulin signaling. J. Biol. Chem. 2010, 285:104-114.
62. Bovenschen N., et al. Elevated plasma factor VIII in a mouse model of low-density lipoprotein receptor-related protein deficiency. Blood 2003, 101:3933-3939.
63. Basford J.E., et al. Hepatic deficiency of low density lipoprotein receptor-related protein-1 reduces high density lipoprotein secretion and plasma levels in mice. J. Biol. Chem. 2011, 286:13079-13087.
64. Williams K.J., Chen K. Recent insights into factors affecting remnant lipoprotein uptake. Curr. Opin. Lipidol. 2010, 21:218-228.
65. Chen K., Williams K.J. Molecular mediators for raft-dependent endocytosis of syndecan-1, a highly conserved, multifunctional receptor. J. Biol. Chem. 2013, 288:13988-13999.
66. Stanford K.I., et al. Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J. Clin. Invest. 2009, 119:3236-3245.
67. MacArthur J.M., et al. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J. Clin. Invest. 2007, 117:153-164.
68. Kjellén L., et al. Reduced sulfation of liver heparan sulfate in experimentally diabetic rats. Diabetes 1983, 32:337-342.
69. Bishop J.R., et al. Insulin-dependent diabetes mellitus in mice does not alter liver heparan sulfate. J. Biol. Chem. 2010, 285:14658-14662.
70. Ebara T., et al. Delayed catabolism of apoB-48 lipoproteins due to decreased heparan sulfate proteoglycan production in diabetic mice. J. Clin. Invest. 2000, 105:1807-1818.
71. Williams K.J., et al. Loss of heparan N-sulfotransferase in diabetic liver: role of angiotensin II. Diabetes 2005, 54:1116-1122.
72. Chen K., et al. Type 2 diabetes in mice induces hepatic overexpression of sulfatase 2, a novel factor that suppresses uptake of remnant lipoproteins. Hepatology 2010, 52:1957-1967.
73. Hassing H.C., et al. Inhibition of hepatic sulfatase-2 in vivo: a novel strategy to correct diabetic dyslipidemia. Hepatology 2012, 55:1746-1753.
74. Yen F.T., et al. Molecular cloning of a lipolysis-stimulated remnant receptor expressed in the liver. J. Biol. Chem. 1999, 274:13390-13398.
75. +/Akita:apoE-deficient mice exhibit exaggerated hypercholesterolemia and atherosclerosis. Am. J. Physiol. Endocrinol. Metab. 2011, 301:E145-E154.
76. Narvekar P., et al. Liver-specific loss of lipolysis-stimulated lipoprotein receptor triggers systemic hyperlipidemia in mice. Diabetes 2009, 58:1040-1049.
77. Mendivil C.O., et al. Metabolism of very-low-density lipoprotein and low-density lipoprotein containing apolipoprotein C-III and not other small apolipoproteins. Arterioscler. Thromb. Vasc. Biol. 2010, 30:239-245.
78. Musunuru K., et al. From noncoding variant to phenotype via SORT1 at the 1p13 cholesterol locus. Nature 2010, 466:714-719.
79. Khamzina L., et al. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 2005, 146:1473-1481.
80. Haas J.T., et al. Hepatic insulin signaling is required for obesity-dependent expression of SREBP-1c mRNA but not for feeding-dependent expression. Cell Metab. 2012, 15:873-884.
81. Sørensen L.P., et al. Basal and insulin mediated VLDL-triglyceride kinetics in type 2 diabetic men. Diabetes 2011, 60:88-96.
82. Lewis G.F., et al. Effects of acute hyperinsulinemia on VLDL triglyceride and VLDL apoB production in normal weight and obese individuals. Diabetes 1993, 42:833-842.
83. Adiels M., et al. Overproduction of large VLDL particles is driven by increased liver fat content in man. Diabetologia 2006, 49:755-765.
84. Cummings M.H., et al. Increased hepatic secretion of very-low-density lipoprotein apolipoprotein B-100 in NIDDM. Diabetologia 1995, 38:959-967.
85. Duvillard L., et al. Metabolic abnormalities of apolipoprotein B-containing lipoproteins in non-insulin-dependent diabetes: a stable isotope kinetic study. Eur. J. Clin. Invest. 2000, 30:685-694.
86. Kissebah A.H., et al. Integrated regulation of very low density lipoprotein triglyceride and apolipoprotein-B kinetics in non-insulin-dependent diabetes mellitus. Diabetes 1982, 31:217-225.
87. Brown M., Goldstein J. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 2008, 7:95-96.
88. Stillemark-Billton P., et al. Relation of the size and intracellular sorting of apoB to the formation of VLDL 1 and VLDL 2. J. Lipid Res. 2005, 46:104-114.
89. Wu X., et al. Evidence for a lack of regulation of the assembly and secretion of apolipoprotein B-containing lipoprotein from HepG2 cells by cholesteryl ester. J. Biol. Chem. 1994, 269:12375-12382.
90. Adiels M., et al. Overproduction of VLDL1 driven by hyperglycemia is a dominant feature of diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1697-1703.
91. Vergès B. New insight into the pathophysiology of lipid abnormalities in type 2 diabetes. Diabetes Metab. 2005, 31:429-439.
92. Mooradian A. Dyslipidemia in type 2 diabetes mellitus. Nat. Clin. Pract. Endocrinol. Metab. 2009, 5:150-159.
93. Sugden M.C., et al. Regulation of hepatic lipogenesis in starved and diabetic animals by thyroid hormone. Biosci. Rep. 1981, 1:757-764.
94. Taskinen M.R., Nikkilä E.A. Lipoprotein lipase activity of adipose tissue and skeletal muscle in insulin-deficient human diabetes. Relation to high-density and very-low-density lipoproteins and response to treatment. Diabetologia 1979, 17:351-356.
95. Nikkilä E.A., Kekki M. Plasma triglyceride transport kinetics in diabetes mellitus. Metabolism 1973, 22:1-22.
96. Pérez A., et al. Lipoprotein compositional abnormalities in type I diabetes: effect of improved glycaemic control. Diabetes Res. Clin. Pract. 1997, 36:83-90.
97. Lopes-Virella M.F., et al. Plasma lipids and lipoproteins in young insulin-dependent diabetic patients: relationship with control. Diabetologia 1981, 21:216-223.
98. Sniderman A.D., et al. Hypertriglyceridemic hyperapoB in type 2 diabetes. Diabetes Care 2002, 25:579-582.