Apolipoproteins A-I, A-II and E are independently distributed among intracellular and newly secreted HDL of human hepatoma cells

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 12, 2009, Pages 1125-1132

  Gillard, Baiba K ^a   Lin, Hu Yu Alice ^a   Massey, John B ^a   Pownall, Henry J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

apo A I; apo A II; apo E; HDL formation; HepG2; Huh7

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN E; HETERODIMER; HIGH DENSITY LIPOPROTEIN; HOMODIMER; MONOMER; VERY LOW DENSITY LIPOPROTEIN; APOA1 PROTEIN, HUMAN; APOA2 PROTEIN, HUMAN; DRUG DERIVATIVE; SEPHAROSE; THIOPROPYL SEPHAROSE; THIOPROPYL-SEPHAROSE;

ARTICLE; CATALYSIS; CELL LYSATE; CELL STRAIN HEPG2; CHOLESTEROL TRANSPORT; DIMERIZATION; FRACTIONATION; GEL PERMEATION CHROMATOGRAPHY; HEPATOMA CELL; HUMAN; HUMAN CELL; LIPOPHILICITY; LIPOPROTEIN SECRETION; MODEL; PRIORITY JOURNAL; BIOLOGICAL MODEL; GEL CHROMATOGRAPHY; INTRACELLULAR SPACE; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SECRETION; TIME; ULTRACENTRIFUGATION;

APOLIPOPROTEIN A-I; APOLIPOPROTEIN A-II; APOLIPOPROTEINS E; CARCINOMA, HEPATOCELLULAR; CHROMATOGRAPHY, GEL; HEP G2 CELLS; HUMANS; INTRACELLULAR SPACE; LIPOPROTEINS, HDL; LIVER NEOPLASMS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SEPHAROSE; TIME FACTORS; ULTRACENTRIFUGATION;

EID: 73949137392     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.07.004     Document Type: Article

References (70)

1. Rader D.J. Molecular regulation of HDL metabolism and function: implications for novel therapies. J. Clin. Invest 116 (2006) 3090-3100
2. Curtiss L.K., Valenta D.T., Hime N.J., and Rye K.A. What is so special about apolipoprotein AI in reverse cholesterol transport?. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 12-19
3. Datta G., Epand R.F., Epand R.M., Chaddha M., Kirksey M.A., Garber D.W., Lund-Katz S., Phillips M.C., Hama S., Navab M., Fogelman A.M., Palgunachari M.N., Segrest J.P., and Anantharamaiah G.M. Aromatic residue position on the nonpolar face of class a amphipathic helical peptides determines biological activity. J. Biol. Chem. 279 (2004) 26509-26517
4. Navab M., Anantharamaiah G.M., and Fogelman A.M. The role of high-density lipoprotein in inflammation. Trends Cardiovasc. Med. 15 (2005) 158-161
5. Havel R.J., Goldstein J.L., and Brown M.S. Lipoproteins and Lipid Transport (1980) 393-494
6. Cheung M.C., and Albers J.J. Characterization of lipoprotein particles isolated by immunoaffinity chromatography. Particles containing A-I and A-II and particles containing A-I but no A-II. J. Biol. Chem. 259 (1984) 12201-12209
7. Clay M.A., Pyle D.H., Rye K.A., and Barter P.J. Formation of spherical, reconstituted high density lipoproteins containing both apolipoproteins A-I and A-II is mediated by lecithin:cholesterol acyltransferase. J. Biol. Chem. 275 (2000) 9019-9025
8. Ikewaki K., Zech L.A., Kindt M., Brewer H.B., and Rader D.J. Apolipoprotein A-II production rate is a major factor regulating the distribution of apolipoprotein A-I among HDL subclasses LpA-I and LpA-I:A-II in normolipidemic humans. Arterioscler. Thromb. Vasc. Biol. 15 (1995) 306-312
9. Edelstein C., Halari M., and Scanu A.M. On the mechanism of the displacement of apolipoprotein A-I by apolipoprotein A-II from the high density lipoprotein surface. Effect of concentration and molecular forms of apolipoprotein A-II. J. Biol. Chem. 257 (1982) 7189-7195
10. Hime N.J., Drew K.J., Wee K., Barter P.J., and Rye K.A. Formation of high density lipoproteins containing both apolipoprotein A-I and A-II in the rabbit. J. Lipid Res. 47 (2006) 115-122
11. Castro G.R., and Fielding C.J. Evidence for the distribution of apolipoprotein E between lipoprotein classes in human normocholesterolemic plasma and for the origin of unassociated apolipoprotein E (Lp-E). J. Lipid Res. 25 (1984) 58-67
12. McCall M.R., Forte T.M., and Shore V.G. Heterogeneity of nascent high density lipoproteins secreted by the hepatoma-derived cell line, Hep G2. J. Lipid Res. 29 (1988) 1127-1137
13. Asztalos B.F., Schaefer E.J., Horvath K.V., Yamashita S., Miller M., Franceschini G., and Calabresi L. Role of LCAT in HDL remodeling: investigation of LCAT deficiency states. J. Lipid Res. 48 (2007) 592-599
14. McKeone B.J., Massey J.B., Knapp R.D., and Pownall H.J. Apolipoproteins C-I, C-II, and C-III: kinetics of association with model membranes and intermembrane transfer. Biochemistry 27 (1988) 4500-4505
15. Guha M., Gao X., Jayaraman S., and Gursky O. Correlation of structural stability with functional remodeling of high-density lipoproteins: the importance of being disordered. Biochemistry 47 (2008) 11393-11397
16. Tangirala R.K., Tsukamoto K., Chun S.H., Usher D., Pure E., and Rader D.J. Regression of atherosclerosis induced by liver-directed gene transfer of apolipoprotein A-I in mice. Circulation 100 (1999) 1816-1822
17. Temel R.E., Walzem R.L., Banka C.L., and Williams D.L. Apolipoprotein A-I is necessary for the in vivo formation of high density lipoprotein competent for scavenger receptor BI-mediated cholesteryl ester-selective uptake. J. Biol. Chem. 277 (2002) 26565-26572
18. Marcel Y.L., and Kiss R.S. Structure-function relationships of apolipoprotein A-I: a flexible protein with dynamic lipid associations. Curr. Opin. Lipidol. 14 (2003) 151-157
19. Blanco-Vaca F., Escola-Gil J.C., Martin-Campos J.M., and Julve J. Role of apoA-II in lipid metabolism and atherosclerosis: advances in the study of an enigmatic protein. J. Lipid Res. 42 (2001) 1727-1739
20. Kalopissis A.D., Pastier D., and Chambaz J. Apolipoprotein A-II: beyond genetic associations with lipid disorders and insulin resistance. Curr. Opin. Lipidol. 14 (2003) 165-172
21. Birjmohun R.S., Dallinga-Thie G.M., Kuivenhoven J.A., Stroes E.S., Otvos J.D., Wareham N.J., Luben R., Kastelein J.J., Khaw K.T., and Boekholdt S.M. Apolipoprotein A-II is inversely associated with risk of future coronary artery disease. Circulation 116 (2007) 2029-2035
22. Blanco-Vaca F., Via D.P., Yang C.Y., Massey J.B., and Pownall H.J. Characterization of disulfide-linked heterodimers containing apolipoprotein D in human plasma lipoproteins. J. Lipid Res. 33 (1992) 1785-1796
23. Connelly P.W., Maguire G.F., Vezina C., Hegele R.A., and Little J.A. Identification of disulfide-linked apolipoprotein species in human lipoproteins. J. Lipid Res. 34 (1993) 1717-1727
24. Lund-Katz S., Murley Y.M., Yon E., Gillotte K.L., and Davidson W.S. Comparison of the structural and functional effects of monomeric and dimeric human apolipoprotein A-II in high density lipoprotein particles. Lipids 31 (1996) 1107-1113
25. Gillard B.K., Chen Y.S., Gaubatz J.W., Massey J.B., and Pownall H.J. Plasma factors required for human apolipoprotein A-II dimerization. Biochemistry 44 (2005) 471-479
26. Mahley R.W., and Huang Y. Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr. Opin. Lipidol. 10 (1999) 207-217
27. Mahley R.W., Huang Y., and Weisgraber K.H. Putting cholesterol in its place: apoE and reverse cholesterol transport. J. Clin. Invest 116 (2006) 1226-1229
28. Weisgraber K.H., and Mahley R.W. Apoprotein (E-A-II) complex of human plasma lipoproteins. I. Characterization of this mixed disulfide and its identification in a high density lipoprotein subfraction. J. Biol. Chem. 253 (1978) 6281-6288
29. Weisgraber K.H., and Shinto L.H. Identification of the disulfide-linked homodimer of apolipoprotein E3 in plasma. Impact on receptor binding activity. J. Biol. Chem. 266 (1991) 12029-12034
30. Thrift R.N., Forte T.M., Cahoon B.E., and Shore V.G. Characterization of lipoproteins produced by the human liver cell line, Hep G2, under defined conditions. J. Lipid Res. 27 (1986) 236-250
31. Chisholm J.W., Burleson E.R., Shelness G.S., and Parks J.S. ApoA-I secretion from HepG2 cells: evidence for the secretion of both lipid-poor apoA-I and intracellularly assembled nascent HDL. J. Lipid Res. 43 (2002) 36-44
32. Maric J., Kiss R.S., Franklin V., and Marcel Y.L. Intracellular lipidation of newly synthesized apolipoprotein A-I in primary murine hepatocytes. J. Biol. Chem. 280 (2005) 39942-39949
33. Chau P., Nakamura Y., Fielding C.J., and Fielding P.E. Mechanism of prebeta-HDL formation and activation. Biochemistry 45 (2006) 3981-3987
34. Tsujita M., Wu C.A., Abe-Dohmae S., Usui S., Okazaki M., and Yokoyama S. On the hepatic mechanism of HDL assembly by the ABCA1/apoA-I pathway. J. Lipid Res. 46 (2005) 154-162
35. Hara S., McCall M.R., and Forte T.M. Re-uptake of nascent low-density lipoproteins by HepG2 cells. Biochim. Biophys. Acta 1168 (1993) 199-204
36. Heeren J., Grewal T., Laatsch A., Rottke D., Rinninger F., Enrich C., and Beisiegel U. Recycling of apoprotein E is associated with cholesterol efflux and high density lipoprotein internalization. J. Biol. Chem. 278 (2003) 14370-14378
37. Heeren J., Beisiegel U., and Grewal T. Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 442-448
38. Erickson S.K., and Fielding P.E. Parameters of cholesterol metabolism in the human hepatoma cell line, Hep-G2. J. Lipid Res. 27 (1986) 875-883
39. McCall M.R., Nichols A.V., Morton R.E., Blanche P.J., Shore V.G., Hara S., and Forte T.M. Transformation of HepG2 nascent lipoproteins by LCAT: modulation by HepG2 d > 1.235 g/ml fraction. J. Lipid Res. 34 (1993) 37-48
40. Hara S., McCall M.R., and Forte T.M. Re-uptake of nascent low-density lipoproteins by HepG2 cells. Biochim. Biophys. Acta 1168 (1993) 199-204
41. Pownall H.J. Remodeling of human plasma lipoproteins by detergent perturbation. Biochemistry 44 (2005) 9714-9722
42. Pownall H.J., Hosken B.D., Gillard B.K., Higgins C.L., Lin H.Y., and Massey J.B. Speciation of human plasma high-density lipoprotein (HDL): HDL stability and apolipoprotein A-I partitioning. Biochemistry 46 (2007) 7449-7459
43. Yvan-Charvet L., Pagler T.A., Wang N., Senokuchi T., Brundert M., Li H., Rinninger F., and Tall A.R. SR-BI inhibits ABCG1-stimulated net cholesterol efflux from cells to plasma HDL. J. Lipid Res. 49 (2008) 107-114
44. Kunitake S.T., and Kane J.P. Factors affecting the integrity of high density lipoproteins in the ultracentrifuge. J. Lipid Res. 23 (1982) 936-940
45. Borghini I., James R.W., Blatter M.C., and Pometta D. Distribution of apolipoprotein E between free and A-II complexed forms in very-low-and high-density lipoproteins: functional implications. Biochim. Biophys. Acta 1083 (1991) 139-146
46. Remaley A.T., Wong A.W., Schumacher U.K., Meng M.S., Brewer Jr. H.B., and Hoeg J.M. O-linked glycosylation modifies the association of apolipoprotein A-II to high density lipoproteins. J. Biol. Chem. 268 (1993) 6785-6790
47. Bradley W.A., and Gianturco S.H. ApoE is necessary and sufficient for the binding of large triglyceride-rich lipoproteins to the LDL receptor; apoB is unnecessary. J. Lipid Res. 27 (1986) 40-48
48. Gusarova V., Seo J., Sullivan M.L., Watkins S.C., Brodsky J.L., and 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. 282 (2007) 19453-19462
49. Nakabayashi H., Taketa K., Yamane T., Miyazaki M., Miyano K., and Sato J. Phenotypical stability of a human hepatoma cell line, HuH-7, in long-term culture with chemically defined medium. Gann 75 (1984) 151-158
50. Nakabayashi H., Taketa K., Miyano K., Yamane T., and Sato J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42 (1982) 3858-3863
51. Higashi Y., Itabe H., Fukase H., Mori M., Fujimoto Y., and Takano T. Transmembrane lipid transfer is crucial for providing neutral lipids during very low density lipoprotein assembly in endoplasmic reticulum. J. Biol. Chem. 278 (2003) 21450-21458
52. Higashi Y., Itabe H., Fukase H., Mori M., Fujimoto Y., Sato R., Imanaka T., and Takano T. Distribution of microsomal triglyceride transfer protein within sub-endoplasmic reticulum regions in human hepatoma cells. Biochim. Biophys. Acta 1581 (2002) 127-136
53. McCall M.R., Forte T.M., and Shore V.G. Heterogeneity of nascent high density lipoproteins secreted by the hepatoma-derived cell line, Hep G2, J. Lipid Res. 29 (1988) 1127-1137
54. McCall M.R., Nichols A.V., Blanche P.J., Shore V.G., and Forte T.M. Lecithin:cholesterol acyltransferase-induced transformation of HepG2 lipoproteins. J. Lipid Res. 30 (1989) 1579-1589
55. McCall M.R., Nichols A.V., Morton R.E., Blanche P.J., Shore V.G., Hara S., and Forte T.M. Transformation of HepG2 nascent lipoproteins by LCAT: modulation by HepG2 d > 1.235 g/ml fraction. J. Lipid Res. 34 (1993) 37-48
56. Kaser S., Foger B., Ebenbichler C.F., Kirchmair R., Gander R., Ritsch A., Sandhofer A., and Patsch J.R. Influence of leptin and insulin on lipid transfer proteins in human hepatoma cell line, HepG2. Int. J. Obes. Relat Metab Disord. 25 (2001) 1633-1639
57. Swenson T.L., Simmons J.S., Hesler C.B., Bisgaier C., and Tall A.R. Cholesteryl ester transfer protein is secreted by Hep G2 cells and contains asparagine-linked carbohydrate and sialic acid. J. Biol. Chem. 262 (1987) 16271-16274
58. Siggins S., Jauhiainen M., Olkkonen V.M., Tenhunen J., and Ehnholm C. PLTP secreted by HepG2 cells resembles the high-activity PLTP form in human plasma. J. Lipid Res. 44 (2003) 1698-1704
59. Jonas A., Sweeny S.A., and Herbert P.N. Discoidal complexes of A and C apolipoproteins with lipids and their reactions with lecithin: cholesterol acyltransferase. J. Biol. Chem. 259 (1984) 6369-6375
60. Nichols A.V., Blanche P.J., Gong E.L., Shore V.G., and Forte T.M. Molecular pathways in the transformation of model discoidal lipoprotein complexes induced by lecithin:cholesterol acyltransferase. Biochim. Biophys. Acta 834 (1985) 285-300
61. Forte T.M., Bielicki J.K., Goth-Goldstein R., Selmek J., and McCall M.R. Recruitment of cell phospholipids and cholesterol by apolipoproteins A-II and A-I: formation of nascent apolipoprotein-specific HDL that differ in size, phospholipid composition, and reactivity with LCAT. J. Lipid Res. 36 (1995) 148-157
62. Koo C., Innerarity T.L., and Mahley R.W. Obligatory role of cholesterol and apolipoprotein E in the formation of large cholesterol-enriched and receptor-active high density lipoproteins. J. Biol. Chem. 260 (1985) 11934-11943
63. Gordon V., Innerarity T.L., and Mahley R.W. Formation of cholesterol-and apoprotein E-enriched high density lipoproteins in vitro. J. Biol. Chem. 258 (1983) 6202-6212
64. Pownall H.J., Hickson D., and Gotto Jr. A.M. Thermodynamics of lipid-protein association. The free energy of association of lecithin with reduced and carboxymethylated apolipoprotein A-II from human plasma high density lipoprotein. J. Biol. Chem. 256 (1981) 9849-9854
65. Oram J.F., and Heinecke J.W. ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev. 85 (2005) 1343-1372
66. Wang N., and Tall A.R. Regulation and mechanisms of ATP-binding cassette transporter A1-mediated cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1178-1184
67. Rader D.J., Schaefer J.R., Lohse P., Ikewaki K., Thomas F., Harris W.A., Zech L.A., Dujovne C.A., and Brewer Jr. H.B. Increased production of apolipoprotein A-I associated with elevated plasma levels of high-density lipoproteins, apolipoprotein A-I, and lipoprotein A-I in a patient with familial hyperalphalipoproteinemia. Metabolism 42 (1993) 1429-1434
68. Ikewaki K., Zech L.A., Brewer Jr. H.B., and Rader D.J. ApoA-II kinetics in humans using endogenous labeling with stable isotopes: slower turnover of apoA-II compared with the exogenous radiotracer method. J. Lipid Res. 37 (1996) 399-407
69. Pownall H.J. Detergent-mediated phospholipidation of plasma lipoproteins increases HDL cholesterophilicity and cholesterol efflux via SR-BI. Biochemistry 45 (2006) 11514-11522
70. Mowri H.O., Patsch J.R., Gotto Jr. A.M., and Patsch W. Apolipoprotein A-II influences the substrate properties of human HDL2 and HDL3 for hepatic lipase. Arterioscler. Thromb. Vasc. Biol. 16 (1996) 755-762