Pathway of biogenesis of apolipoprotein E-containing HDL in vivo with the participation of ABCA1 and LCAT

Biochemical Journal

Volumn 403, Issue 2, 2007, Pages 359-367

  Kypreos, Kyriakos E ^a   Zannis, Vassilis I ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenovirus mediated gene transfer; Apolipoprotein E (apoE); ATP binding cassette transporter A1 (ABCA1); High density lipoprotein (HDL); Lecithin:cholesterol acyltransferase (LCAT)

Indexed keywords

DISEASES; ENZYME KINETICS; GENE TRANSFER; PARTICLE SIZE;

ADENOVIRUS MEDIATED GENE TRANSFER; APOLIPOPROTEIN E (APOE); ATP BINDING CASSETTE TRANSPORTER A1 (ABCA1); HIGH DENSITY LIPOPROTEIN (HDL); LECITHIN CHOLESTEROL ACYLTRANSFERASE (LCAT);

PROTEINS;

ABC TRANSPORTER A1; ADENOVIRUS VECTOR; ALANINE; APOLIPOPROTEIN A1; APOLIPOPROTEIN E4; HIGH DENSITY LIPOPROTEIN; LIPID; LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN; ABC TRANSPORTER; APOLIPOPROTEIN E; APOLIPOPROTEIN E RICH HDL; APOLIPOPROTEIN E-RICH HDL; MESSENGER RNA; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADENOVIRUS; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FAST PROTEIN LIQUID CHROMATOGRAPHY; FEMALE; GENE TRANSFER; HYPERCHOLESTEROLEMIA; LIPID ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; VIRUS INFECTION; ANIMAL; BIOSYNTHESIS; BLOOD; GENETICS; HUMAN; HYDROPHOBICITY; METABOLISM; MOUSE MUTANT;

ADENOVIRIDAE; MUS;

ADENOVIRIDAE; ALANINE; ANIMALS; APOLIPOPROTEIN A-I; APOLIPOPROTEINS E; ATP-BINDING CASSETTE TRANSPORTERS; HUMANS; HYDROPHOBICITY; LIPOPROTEINS, HDL; METABOLIC NETWORKS AND PATHWAYS; MICE; MICE, KNOCKOUT; PHOSPHATIDYLCHOLINE-STEROL O-ACYLTRANSFERASE; RECOMBINANT PROTEINS; RNA, MESSENGER;

EID: 34247170098     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061048     Document Type: Article

References (44)

1. Zannis, V. I., Kypreos, K. E., Chroni, A., Kardassis, D. and Zanni, E. E. (2004) Lipoproteins and atherogenesis. In Molecular Mechanisms of Atherosclerosis (Loscalzo, J., ed.), pp. 111-174, Taylor & Francis, New York
2. Zannis, V. I., Zanni, E. E., Makrides, S. C., Kardassis, D. and Aleshkov, S. (1998) Role of apolipoprotein E in Alzheimer's disease. In NATO ASI Series, Life Sciences (Catravas, J. D., ed.), pp. 179-209, Plenum Press, New York
3. Plump, A. S., Smith, J. D., Hayek, T., Aalto-Setala, K., Walsh, A., Verstuyft, J. G., Rubin, E. M. and Breslow, J. L. (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71, 343-353
4. Schaefer, E. J., Gregg, R. E., Ghiselli, G., Forte, T. M., Ordovas, J. M., Zech, L. A. and Brewer, Jr, H. B. (1986) Familial apolipoprotein E deficiency. J. Clin. Invest. 78, 1206-1219
5. Linton, M. F. and Fazio, S. (1999) Macrophages, lipoprotein metabolism, and atherosclerosis: insights from murine bone marrow transplantation studies. Curr. Opin. Lipidol. 10, 97-105
6. Hasty, A. H., Linton, M. F., Brandt, S. J., Babaev, V. R., Gleaves, L. A. and Fazio, S. (1999) Retroviral gene therapy in ApoE-deficient mice: ApoE expression in the artery wall reduces early foam cell lesion formation. Circulation 99, 2571-2576
7. Thorngate, F. E., Rudel, L. L., Walzem, R. L. and Williams, D. L. (2000) Low levels of extrahepatic nonmacrophage ApoE inhibit atherosclerosis without correcting hypercholesterolemia in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 1939-1945
8. Raffai, R. L., Loeb, S. M. and Weisgraber, K. H. (2005) Apolipoprotein E promotes the regression of atherosclerosis independently of lowering plasma cholesterol levels. Arterioscler. Thromb. Vasc. Biol. 25, 436-441
9. Tsukamoto, K., Tangirala, R. K., Chun, S., Usher, D., Pure, E. and Rader, D. J. (2000) Hepatic expression of apolipoprotein E inhibits progression of atherosclerosis without reducing cholesterol levels in LDL receptor-deficient mice. Mol. Ther. 1, 189-194
10. Huang, Y., von Eckardstein, A., Wu, S., Maeda, N. and Assmann, G. (1994) A plasma lipoprotein containing only apolipoprotein E and with γ mobility on electrophoresis releases cholesterol from cells. Proc. Natl. Acad. Sci. U.S.A. 91, 1834-1838
11. Shimano, H., Ohsuga, J., Shimada, M., Namba, Y., Gotoda, T., Harada, K., Katsuki, M., Yazaki, Y. and Yamada, N. (1995) Inhibition of diet-induced atheroma formation in transgenic mice expressing apolipoprotein E in the arterial wall. J. Clin. Invest. 95, 469-476
12. Tsukamoto, K., Tangirala, R., Chun, S. H., Pure, E. and Rader, D. J. (1999) Rapid regression of atherosclerosis induced by liver-directed gene transfer of ApoE in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 19, 2162-2170
13. Kypreos, K. E. and Zannis, V. I. (2006) LDL receptor deficiency or apoE mutations prevent remnant clearance and induce hypertriglyceridemia in mice. J. Lipid Res. 47, 521-529
14. Kypreos, K. E., Van Dijk, K. W., van Der, Z. A., Havekes, L. M. and Zannis, V. I. (2001) Domains of apolipoprotein E contributing to triglyceride and cholesterol homeostasis in vivo: carboxyl-terminal region 203-299 promotes hepatic very low density lipoprotein-triglyceride secretion. J. Biol. Chem. 276, 19778-19786
15. Havel, R. J., Kotite, L., Vigne, J. L., Kane, J. P., Tun, P., Phillips, N. and Chen, G. C. (1980) Radioimmunoassay of human arginine-rich apolipoprotein, apoprotein E: concentration in blood plasma and lipoproteins as affected by apoprotein E-3 deficiency. J. Clin. Invest. 66, 1351-1362
16. Zannis, V. I., Chroni, A., Kypreos, K. E., Kan, H. Y., Cesar, T. B., Zanni, E. E. and Kardassis, D. (2004) Probing the pathways of chylomicron and HDL metabolism using adenovirus-mediated gene transfer. Curr. Opin. Lipidol. 15, 151-166
17. Kypreos, K. E., Van Dijk, K. W., Havekes, L. M. and Zannis, V. I. (2005) Generation of a recombinant apolipoprotein E variant with improved biological functions: hydrophobic residues (Leu-261, Trp-264, Phe-265, Leu-268, Val-269) of apoE can account for the apoE-induced hypertriglyceridemia. J. Biol. Chem. 280, 6276-6284
18. Nolte, R. T. and Atkinson, D. (1992) Conformational analysis of apolipoprotein A-I and E-3 based on primary sequence and circular dichroism. Biophys. J. 63, 1221-1239
19. Steinmetz, A., Kaffarnik, H. and Utermann, G. (1985) Activation of phosphatidylcholine-sterol acyltransferase by human apolipoprotein E isoforms. Eur. J. Biochem. 152, 747-751
20. Chroni, A., Nieland, T. J., Kypreos, K. E., Krieger, M. and Zannis, V. I. (2005) SR-BI mediates cholesterol efflux via its interactions with lipid-bound ApoE: structural mutations in SR-BI diminish cholesterol efflux. Biochemistry 44, 13132-13143
21. Chroni, A., Liu, T., Gorshkova, I., Kan, H. Y., Uehara, Y., von Eckardstein, A. and Zannis, V. I. (2003) The central helices of apoA-I can promote ATP-binding cassette transporter A1 (ABCA1)-mediated lipid efflux: amino acid residues 220-231 of the wild-type apoA-I are required for lipid efflux in vitro and high density lipoprotein formation in vivo. J. Biol. Chem. 278, 6719-6730
22. Williamson, R., Lee, D., Hagaman, J. and Maeda, N. (1992) Marked reduction of high density lipoprotein cholesterol in mice genetically modified to lack apolipoprotein A-I. Proc. Natl. Acad. Sci. U.S.A. 89, 7134-7138
23. McNeish, J., Aiello, R. J., Guyot, D., Turi, T., Gabel, C., Aldinger, C., Hoppe, K. L., Roach, M. L., Royer, L. J., de Wet, J. et al. (2000) High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc. Natl. Acad. Sci. U.S.A. 97, 4245-4250
24. Zhang, S. H., Reddick, R. L., Piedrahita, J. A. and Maeda, N. (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258, 468-471
25. Chroni, A., Duka, A., Kan, H. Y., Liu, T. and Zannis, V. I. (2005) Point mutations in apolipoprotein a-I mimic the phenotype observed in patients with classical lecithin: cholesterol acyltransferase deficiency. Biochemistry 44, 14353-14366
26. Chroni, A., Kan, H. Y., Shkodrani, A., Liu, T. and Zannis, V. I. (2005) Deletions of helices 2 and 3 of human ApoA-I are associated with severe dyslipidemia following adenovirus-mediated gene transfer in ApoA-I-deficient mice. Biochemistry 44, 4108-4117
27. Kypreos, K. E., Li, X., Van Dijk, K. W., Havekes, L. M. and Zannis, V. I. (2003) Molecular mechanisms of type III hyperlipoproteinemia: the contribution of the carboxy-terminal domain of ApoE can account for the dyslipidemia that is associated with the E2/E2 phenotype. Biochemistry 42, 9841-9853
28. Mitchell, C. D., King, W. C., Applegate, K. R., Forte, T., Glomset, J. A., Norum, K. R. and Gjone, E. (1980) Characterization of apolipoprotein E-rich high density lipoproteins in familial lecithin:cholesterol acyltransferase deficiency. J. Lipid Res. 21, 625-634
29. Assmann, G., von Eckardstein, A. and Brewer, H. B. (2001) Familial analphalipoproteinemia: Tangier disease. In The Metabolic and Molecular Basis of Inherited Disease (Scriver, C. R., Beaudet, A. L., Sly, W. S. and Valle, D., eds.), pp. 2937-2960, McGraw-Hill, New York
30. Hamilton, R. L., Williams, M. C., Fielding, C. J. and Havel, R. J. (1976) Discoidal bilayer structure of nascent high density lipoproteins from perfused rat liver. J. Clin. Invest. 58, 667-680
31. Gong, E. L., Nichols, A. V., Weisgraber, K. H., Forte, T. M., Shore, V. G. and Blanche, P. J. (1989) Discoidal complexes containing apolipoprotein E and their transformation by lecithin-cholesterol acyltransferase. Biochim. Biophys. Acta 1006, 317-328
32. Wahrle, S. E., Jiang, H., Parsadanian, M., Legleiter, J., Han, X., Fryer, J. D., Kowalewski, T. and Holtzman, D. M. (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J. Biol. Chem. 279, 40987-40993
33. Krimbou, L., Denis, M., Haidar, B., Carrier, M., Marcil, M. and Genest, Jr, J. (2004) Molecular interactions between apoE and ABCA1: impact on apoE lipidation. J. Lipid Res. 45, 839-848
34. Koldamova, R., Staufenbiel, M. and Lefterov, I. (2005) Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J. Biol. Chem. 280, 43224-43235
35. Hirsch-Reinshagen, V., Maia, L. F., Burgess, B. L., Blain, J. F., Naus, K. E., McIsaac, S. A., Parkinson, P. F., Chan, J. Y., Tansley, G. H., Hayden, M. R. et al. (2005) The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J. Biol. Chem. 280, 43243-43256
36. Zhao, Y., Thorngate, F. E., Weisgraber, K. H., Williams, D. L. and Parks, J. S. (2005) Apolipoprotein E is the major physiological activator of lecithin-cholesterol acyltransferase (LCAT) on apolipoprotein B lipoproteins. Biochemistry 44, 1013-1025
37. Liu, T., Krieger, M., Kan, H. Y. and Zannis, V. I. (2002) The effects of mutations in helices 4 and 6 of apoA-I on scavenger receptor class B type I (SR-BI)-mediated cholesterol efflux suggest that formation of a productive complex between reconstituted high density lipoprotein and SR-BI is required for efficient lipid transport. J. Biol. Chem. 277, 21576-21584
38. Rader, D. J. (2002) High-density lipoproteins and atherosclerosis. Am. J. Cardiol. 90, 62i-70i
39. Navab, M., Hama, S. Y., Cooke, C. J., Anantharamaiah, G. M., Chaddha, M., Jin, L., Subbanagounder, G., Faull, K. F., Reddy, S. T., Miller, N. E. and Fogelman, A. M. (2000) Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: step 1. J. Lipid Res. 41, 1481-1494
40. Yuhanna, I. S., Zhu, Y., Cox, B. E., Hahner, L. D., Osborne-Lawrence, S., Lu, P., Marcel, Y. L., Anderson, R. G., Mendelsohn, M. E., Hobbs, H. H. and Shaul, P. W. (2001) High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 7, 853-857
41. Li, H., Reddick, R. L. and Maeda, N. (1993) Lack of apoA-I is not associated with increased susceptibility to atherosclerosis in mice. Arterioscler. Thromb. 13, 1814-1821
42. Hughes, S. D., Verstuyft, J. and Rubin, E. M. (1997) HDL deficiency in genetically engineered mice requires elevated LDL to accelerate atherogenesis. Arterioscler. Thromb. Vasc. Biol. 17, 1725-1729
43. Trigatti, B., Rayburn, H., Vinals, M., Braun, A., Miettinen, H., Penman, M., Hertz, M., Schrenzel, M., Amigo, L., Rigotti, A. and Krieger, M. (1999) Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc. Natl. Acad. Sci. U.S.A. 96, 9322-9327
44. Braun, A., Trigatti, B. L., Post, M. J., Sato, K., Simons, M., Edelberg, J. M., Rosenberg, R. D., Schrenzel, M. and Krieger, M. (2002) Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ. Res. 90, 270-276