The role of the LDL receptor in apolipoprotein B secretion

Journal of Clinical Investigation

Volumn 105, Issue 4, 2000, Pages 521-531

  Twisk, Jaap ^a,b   Gillian Daniel, Donald L ^a   Tebon, Angie ^a   Wang, Lin ^a,c   Barrett, P Hugh R ^d   Attie, Alan ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; LIPOPROTEIN METABOLISM; LIPOPROTEIN SECRETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM;

EID: 0034003980     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/jci8623     Document Type: Article

References (89)

1. Langer, T., Stober, W., and Levy, R.I. 1972. The metabolism of LDL in familial type II hyperlipidemia. J. Clin. Invest. 51:1528-1536.
2. Bilheimer, D.W., Stone N.J., and Grundy, S.M. 1979. Metabolic studies in familial hypercholesterolemia. Evidence for a gene-dosage effect in vivo. J. Clin. Invest. 64:524-533.
3. Pittman, R.C., et al. 1982. Tissue sites of degradation of low density lipoprotein in normal rabbits and in a receptor-negative mutant strain (WHHL rabbit). J. Biol. Chem. 257:7994-8000.
4. Brown, M.S., and Goldstein, J.L. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232:34-47.
5. Packard, C.J., et al. 1976. Low density lipoprotein metabolism in a family of familial hypercholesterolemic patients. Metabolism. 25:995-1006.
6. Soutar, A.K., Myant, N.B., and Thompson, G.R. 1977. Simultaneous measurement of apolipoprotein B turnover in very-low- and low-density lipoproteins in familial hypercholesterolaemia. Atherosclerosis. 28:247-256.
7. James, R.W., et al. 1989. Apolipoprotein B metabolism in homozygous familial hyperholesterolemia. J. Lipid Res. 30:159-169.
8. Havel, R.J., and Kane, J.P. 1995. Introduction: structure and metabolism of plasma lipoproteins. In The metabolic and molecular bases of inherited disease. Volume II. C.R. Scriver, A.L. Beaudet, W.S. Sly, and D. Valle, editors. McGraw-Hill. New York, NY, 1841-1851.
9. Bilheimer, D.W., Watanabe, Y., and Kita, T. 1982. Impaired receptor-mediated catabolism of low density lipoprotein in the WHHL rabbit, an animal model of familial hypercholesterolemia. Proc. Natl. Acad. Sci. USA. 79:3305-3309.
10. Endo, A. 1992. The discovery and development of HMG-CoA reductase inhibitors J. Lipid Res. 33:1569-1582.
11. Ma, P.T., et al. 1986 Mevinolin, an inhibitor of cholesterol synthesis, induces mRNA low density lipoprotein receptor in livers of hamsters and rabbits. Proc. Natl. Acad. Sci. USA. 83:8370-8374.
12. Uauy, R., Vega, G.L., Grundy, S.M., and Bilheimer, D.M. 1988. Lovastatin therapy in receptor-negative homozygous familial hypercholesterolemia: lack of effect on low-density lipoprotein concentration or turnover. J. Pediatr. 113:387-392.
13. Grundy, S.M., and Vega, G.L. 1985. Influence of mevinolin on metabolism of love density lipoprotein in primary moderate hypercholesterolemia. J. Lipid Res. 26:1464-1475.
14. Arad, Y., Ramakrishnan, R., and Ginsberg, H.N. 1990. Lovastatin therapy reduces low density lipoprotein apoB levels in subjects with combined hyperlipidemia by reducing the production of apoB-containing lipoproteins: implications for the pathophysiology of apoB production. J. Lipid Res. 31:567-582.
15. Cuchel, M., et al. 1997. Lovastatin decreases de novo cholesterol synthesis and LDL apo B-100 production rares in combined-hyperlipidemic males. Arterioscler. Thromb. Vasc. Biol. 17:1910-1917.
16. Huff, M.W., Telford, D.E., Woodcroft, K., and Strong, W.L.P. 1985. Mevinolin and cholestryramine inhibit the direct synthesis of low density lipoprotein apolipoprotein B in miniature pigs. J. Lipid Res. 26:1175-1186.
17. Auerbach, B.J., Krause, B.R., Bisgaier, C.L., and Newton, R.S. 1995. Comparative effects of HMG-CoA reductase inhibitors on apo-B production in the casein-fed rabbit: atorvastatin versus lovastatin. Atherosclerosis. 115:173-180.
18. Huff, M.W., and Burnett, J.R. 1997. 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors and hepatic apolipoprotein B secretion. Curr. Opin. Lipidol. 8:138-145.
19. Borchardt, R.A., and Davis, R.A. 1987. Intrahepatic assembly of very low density lipoprotenis. Rate of transport out of the endoplasmic reticulum determines rare of secretion. J. Biol. Chem. 262:16394-16402.
20. Dixon, J.L., and Ginsberg, H.N. 1993. Regulation of hepatic secretion of apolipoprotein B-containing lipoproteins: information obtained from cultured liver cells. J. Lipid Res. 34:167-179.
21. Yao, Z., Tran, K., and McLeod, R.S. 1997. Intracellular degradation of newly synthesized apolipoprotein B. J. Lipid Res. 38;1937-1953.
22. Williams, K.J., Broci, R.W., and Fisher, E.A. 1990. The unstirred water layer as a site of control of apolipoprotein B secretion. J. Biol. Chem. 265:16741-16744.
23. Ishibashi, S., et al. 1993. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92:883-893.
24. Ishibashi, S., et al. 1994. Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J. Clin. Invest. 93:1885-1893.
25. Shimano, H., et al. 1996. Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J. Clin. Invest. 98:1575-1584.
26. Horton, J.D., Shimano, H., Hamilton, R.L., Brown, M.S., and Goldstern, J.L. 1999. Disruption of LDL receptor gene in transgenic SREBP-1a mice unmasks hyperlipidemia resulting from production of lipid-rich VLDL. J. Clin. Invest. 103:1067-1076.
27. Gaw, A., Mancini, F.P., and Ishibashi, S. 1995. Rapid genotyping of low-density-lipoprotein receptor knockout mice using a polymerase chain-reaction technique. Lab. Anim. 29:447-449.
28. Princen, H.M.G., Huijsmans, C.M.G., Kuipers, F., Vonk, R., and Kempen, H.J.M. 1986. Ketoconazole blocks bile acid synthesis in hepatocyte monolayer cultures and in vivo in rat by inhibiting cholesterol 7a-hydroxylase. J. Clin. Invest. 78:1064-1071.
29. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-686.
30. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
31. Wilcox, L.J., Barrett, P.H., and Huff, M.W. 1999. Differential regulation of apolipoprotein B secretion from HepG2 cells by two HMG-CoA reductase inhibitors, atorvastatin and simvastatin. J. Lipid Res. 40:1078-1089.
32. Gianturco, S.H., and Bradley, W.A. 1986. The role of apolipoprotein processing in receptor recognition of VLDL. Methods Enzymol. 129:319-344.
33. Bligh, E.G., and Dyer, W.J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
34. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
35. Hussain, M.M., Zhao, Y., Kancha, R.K., Blackhart, B.D., and Yao, Z. 1995. Characterization of recombinant human ApoB-48-containing lipoproteins in rat hepatoma McA-RH7777 cells transfected with ApoB-48 cDNA: overexpression of ApoB-48 decreases synthesis of endogenous ApoB-100. Arterioscler. Thromb. Vasc. Biol. 15:485-494.
36. Fort, P.H., et al. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate dehydrogenase multigenic family. Nucleic Acids Res. 13:1431-1442.
37. Krawczyk, Z., and Wu, C. 1987. Isolation of RNA for dot hybridization by heparin-DNase I treatment of whole cell lysate. Anal. Biochem. 162:156-159.
38. Seoane, J., et al. 1996. Glucose 6-phosphate produced by glucokinase, but not hexokinase I, promotes the activation of hepatic glycogen synthase. J. Biol. Chem. 271:23756-23760.
39. Chan, L., Chang, B.H.J., Nakamuta, M., Li, W.H., and Smith, L.C. 1997. Apobec-1 and apolipoprotein B mRNA editing. Biochim. Biophys. Acta. 1345:1126.
40. Greeve, J., Altkemper, I., Dieterich, J.H., Greten, H., and Windler, E. 1993. Apolipoprotein B mRNA editing in 12 different mammalian species: hepatic expression is reflected in low concentrations of apoB-contaming plasma lipoproteins. J. Lipid Res. 34:1367-1383.
41. Higuchi, K., Kitagawa, K., Kogishi, K., and Takeda, T. 1992. Developmental and age-related changes in apolipoprotein B mRNA editing in mice. J. Lipid Res. 33:1753-1764.
42. Gibson, J.C., et al. 1987. Plasma lipoprotein distribution of apolipoprotein E in familial hypercholesterolemia. Arteriosclerosis. 7:401-407.
43. Thompson, G.R., Naoumova, R.P., and Watts, G.F. 1996. Role of cholesterol in regulating apolipoprotein B secretion by the liver. J. Lipid Res. 37:439-447.
44. Wetterau, J.R., Lin, M.C., and Jamil, H. 1997. Microsomal triglyceride transfer protein. Biochim. Biophys. Acta. 1345:136-150.
45. Tietge, U.J.F., et al. 1999. Hepatic overexpression of microsomal triglyceride transfer protein (MTP) results in increased in vivo secretion of VLDL triglycerides and apolipoprotein B. J. Lipid Res. 40:2134-2139.
46. Raabe, M., et al. 1998. Knockout of the abetalipoproteinemia gene in mice: reduced lipoprotein secretion in heterozygotes and embryonic lethality in homozygotes. Proc. Natl. Acad. Sci. USA. 95:8686-8691.
47. Goldstein, J.L., Basu, S.K., Brunschede, G.Y., and Brown, M.S. 1976. Release of low density lipoprotein from its cell surface receptor by sulfated glycosaminoglycans. Cell. 7:85-95.
48. Powell-Braxton, L., et al. 1998. A mouse model of human familial hypercholesterolemia: markedly elevated low density lipoprotein cholesterol levels and severe atherosclerosis on a low-fat chow diet. Nat. Med. 4:934-938.
49. Valiant, M.M., et al. 1998. Lipoprotein clearance mechanisms in LDL receptor-deficient "Apo-B48-only" and "Apo-B100-only" mice. J. Clin. Invest. 102:1559-1568.
50. Ishibashi, S., Herz, J., Maeda, N., Goldstein, J.L., and Brown, M.S. 1994.The two-receptor model of lipoprotein clearance: tests of the hypothesis in "knockout" mice lacking the low density lipoprotein receptor, apolipoprotein E. or both proteins. Proc. Natl. Acad. Sci. USA. 91:4431-4435.
51. Patsch, W., Tamai, T., and Schonfeld, G. 1983. Effect of fatty acids on lipid and apoprotein secretion and association in hepatocyte cultures. J. Clin. Invest. 72:371-378.
52. Sorci-Thomas, M., Wilson, M.D., Johnson, F.L., Williams, D.L., and Rudel, L.L. 1989. Studies on the expression of genes encoding apolipoproteins B100 and B48 and the low density lipoprotein receptor in nonhuman primates. Comparison of dietary fat and cholesterol. J. Biol. Chem. 264:9039-9045.
53. Pullinger, C.R., et al. 1989. The apolipoprotein B gene is constitutively expressed in HepG2 cells: regulation of secretion by oleic acid, albumin, and insulin, and measurement of the mRNA half-life. J. Lipid Res. 30:1065-1077.
54. Moberly, J.B., Cole, T.G., Alpers, D.H., and Schonfeld, G. 1990. Oleic acid stimulation of apolipoprotein B secretion from HepG2 and Caco-2 cells occurs post-transcriprionally. Biochim. Biophys. Acta. 1042:70-80.
55. White, A.L., Guerra, B., Wang, J., and Lanford, R.E. 1999. Presecretory degradation of apolipoprotein[a] is mediated by the proteasome pathway. J. Lipid Res. 40:275-286.
56. Benoist, F., and Grand-Perret, T. 1997. Co-translational degradation of apolipoprotein B100 by the proteasome is prevented by microsomal triglyceride transfer protein. J. Biol. Chem. 272:20435-20442.
57. Davis, R.A., Boogaerts, J.R., Borchardt, R.A., Malone-McNeal, M., and Archambault-Schexnayder, J. 1985. Intrahepatic assembly of very low density lipoproteins. Varied synthetic response of individual apolipoproteins to fasting. J. Biol. Chem. 260:14137-14144.
58. Attie, A.D., Pittman, R.C., and Steinberg, D. 1980. Metabolism of native and of lactosylated human low density lipoprotein: evidence for two pathways for catabolism of exogenous proteins in rat hepatocytes. Proc. Natl. Acad. Sci. USA. 77:5923-5927.
59. Wang, C.N., Hobman, T.C., and Brindley, D.N. 1995. Degradation of apolipoprotein B in cultured rat hepatocytes occurs in a post-endoplasmic reticulum compartment. J. Biol. Chem. 270:24924-24931.
60. Welty, F.K., Seman, L., and Yen, F.T. 1995. Purification of the apolipoprotein B-67-containing low density lipoprotein particle and its affinity for the low density lipoprorein receptor. J. Lipid Res. 36:2622-2629.
61. Borén, J., et al. 1998. Identification of the low density lipoprotein receptor-binding sire in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J. Clin. Invest. 101:1084-1093.
62. Weisgraber, K.H., and Rall, S.C. 1987. Human apolipoprotein B-100 heparin-binding sites. J. Biol. Chem. 262:11097-11103.
63. Borén, J., et al, 1998. Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J. Clin. Invest. 101:2658-2664.
64. Goldberg, I.J. et al. 1998. The NH2-terminal region of apolipoprotein B is sufficient for lipoprotein association with glycosaminoglycans. J. Biol. Chem. 273:35355-35361.
65. Alexander, C.A., Hamilton, R.L., and Havel, R.J. 1976. Subcellular localization of B apoprotein of plasma lipoproteins in rat livers. J. Cell Biol. 69:241-263.
66. Cartwright, I.J., Hebbachi, A., and Higgins, J.A. 1993. Transit and sorting of apolipoprotein B within the endoplasmic reticulum and Golgi compartments of isolated hepatocytes from normal and orotic acid-fed rats. J. Biol. Chem. 268:20937-20952.
67. Aridor, M., and Balch, W.E. 1999. Integration of endoplasmic reticulum signaling in health and disease. Nat. Med. 5:745-751.
68. Bu, G., and Schwartz, A.L. 1998. RAP, a novel type of ER chaperone. Trends Cell Biol. 8:272-276.
69. Bu, G., and Rennke, S. 1996. Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J. Biol. Chem. 271:22218-22224.
70. Zhen, L., Baumann, H., Novak, E.K., and Swank, R.T. 1993. The signal for retention of the egasyn-glucuronidase complex within the endoplasmic reticulum. Arch. Biochem. Biophys. 304:402-414.
71. Zhen, L., Rusiniak, M.E. and Swank, R.T. 1995. The beta-glucuronidase propeptide contains a serpin-related octamer necessary for complex formation with egasyn esterase and for retention within the endoplasmic reticulum. J. Biol. Chem. 270:11912-11920.
72. Geleziunas, R., Bour, S., and Wainberg, M.A. 1994. Cell surface down-modulation of CD4 after infection by HIV-1. FASEB J. 8:593-600.
73. Chuck, S.L., and Lingappa, V.R. 1992. Pause transfer: a topogenic sequence in apolipoprotein B mediates stopping and restarting of translocation. Cell. 68:9-21.
74. Mitchell, D.M., et al. 1998. Apoprotein B100 has a prolonged interaction with the translocon during which its lipidation and translocation change from dependence on the microsomal triglyceride transfer protein to independence. Proc. Natl. Acad. Sci. USA. 95:14733-14738.
75. Davis, R.A., et al. 1989. Intrahepatic assembly of very low density lipoproteins: immunologic characterization of apolipoprotein B in lipoproteins and hepatic membrane fractions and its intracellular distribution. J. Lipid Res. 30:1185-1196.
76. Wu, X., et al. 1997. A two-site model for apoB degradation in HepG2 cells. J. Biol. Chem. 272:11575-11580.
77. Yamamoto, T., Bishop, R.W., Brown, M.S., Goldstein, J.L., and Russell, D.W. 1986. Deletion in cysteine-rich region of LDL receptor impedes transport to cell surface in WHHL rabbit. Science. 232:1230-1237.
78. Hornick, C.A., Kita, T., Hamilton, R.L., Kane, J.P., and Havel, R.J. 1983. Secretion of lipoproteins from the liver of normal and Watanabe heritable hyperlipidemic rabbits. Proc. Natl. Acad. Sci. USA. 80:6096-6100.
79. Tanaka, M., Otani, H., Yokode, M., and Kita, T. 1995. Regulation of apolipoprotein B secretion in hepatocytes from Watanabe heritable hyperlipidemic rabbit, an animal model of familial hypercholesterolemia. Atherosclerosis. 114:73-82.
80. Ginsberg, H.N., Le, N.A., Short, M.P., Ramakrishnan, R., and Desnick, R.J. 1987. Suppression of apolipoprotein B production during treatment of cholesteryl ester storage disease with lovastatin. Implications for regulation of apolipoprotein B synthesis. J. Clin. Invest. 80:1692-1697.
81. Vega, G.L., Krauss, R.M., and Grundy, S.M. 1990. Pravastatin therapy in primary moderate hypercholesterolaemia: changes in metabolism of apolipoprotein B-containmg lipoproteins. J. Intern. Med. 227:81-94.
82. Mohammadi, A., et al. 1998. Effects of Atorvastatin on the intracellular stability and secretion of apolipoprotein B in HepG2 cells. Arterioscl. Thromb. Vasc. Biol. 18:783-793.
83. Bisgaier, C.L., et al. 1997. Attenuation of plasma low density lipoprotein cholesterol by select 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors in mice devoid of low density lipoprotein receptors. J. Lipid Res. 38:2502-2515.
84. Carew, T.E., Schwenke, D.C., and Steinberg, D. 1987. Antiatherogenic effect of probucol unrelated to its hypocholesterlemic effect: evidence that antioxidants in vivo can selectively inhibit low density lipoprorein degradation in macrophage-rich fatty streaks and slow the progression of atherosclerosis in the Watanabe heritable hyperlipidemic rabbit. Proc. Natl. Acad. Sci. USA. 84:7725-7729.
85. Marais, A.D., et al. 1997. Decreased production of low density lipoprotein by atorvastatin after apheresis in homozygous familial hypercholesterolemia. J. Lipid Res. 38:2071-2078.
86. Kuipers, F., et al. 1997. Impaired secretion of very low density lipoprotein-triglycerides by apolipoprotein E-deficient mouse hepatocytes. J. Clin. Invest. 100:2913-2922.
87. Huang, Y., et al. 1998. Overexpression and accumulation of apolipoprotein E as a cause of hypertriglyceridemia. J. Biol. Chem. 273:26388-26393.
88. Zhao, Y., and Mazzone, T. 1999. LDL receptor binds newly synthesized apoE in macrophages. A precursor pool for apoE secretion. J. Lipid Res. 40:1029-1035.
89. Schmitt, M., and Grand-Perret, T. 1999. Regulated turnover of a cell surface-associated pool of newly synthesized apolipoprotein E in HepG2 cells. J. Lipid Res. 40:39-49.