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. 1992 May 15;284(Pt 1):145–151. doi: 10.1042/bj2840145

The role of apoproteins AI and AII in binding of high-density lipoprotein3 to membranes derived from bovine aortic endothelial cells.

P K Vadiveloo 1, N H Fidge 1
PMCID: PMC1132709  PMID: 1599393

Abstract

Although binding of high-density lipoproteins (HDL) to a variety of cells in culture has been widely reported, the mechanism of this binding has yet to be fully elucidated. The aim of the current studies was to explore the roles of apoproteins (apo) AI and AII in HDL3 binding to membranes derived from bovine aortic endothelial cells. Binding studies showed that HDL3 (which contains both apo AI and apo AII) and AII-HDL3 (which contain only apo AII) bound to membranes with similar affinity (44 +/- 6 and 41 +/- 9 micrograms/ml respectively) and capacity (673 +/- 97 and 969 +/- 101 ng bound/mg of membrane protein respectively). In contrast with these results, HDL3 [AI w/o AII] (which contain apo AI, but not apo AII) bound to the membranes with a significantly higher capacity (2228 +/- 206 ng bound/mg of membrane protein) and lower affinity (65 +/- 3 micrograms/ml) as compared with HDL3 or AII-HDL3. Therefore, although both apo AI and apo AII appear capable of facilitating HDL3 binding, the mechanisms involved probably differ. A model which fits the data postulates that a common receptor exists which binds both apo AI and apo AII, and that a particle containing AII can occupy up to four receptors (partly owing to each AII molecule containing two binding domains), whereas an HDL3 [AI w/o AII] particle can occupy only one.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atmeh R. F., Shepherd J., Packard C. J. Subpopulations of apolipoprotein A-I in human high-density lipoproteins. Their metabolic properties and response to drug therapy. Biochim Biophys Acta. 1983 Apr 13;751(2):175–188. doi: 10.1016/0005-2760(83)90172-8. [DOI] [PubMed] [Google Scholar]
  2. Barbaras R., Grimaldi P., Negrel R., Ailhaud G. Characterization of high-density lipoprotein binding and cholesterol efflux in cultured mouse adipose cells. Biochim Biophys Acta. 1986 Sep 19;888(2):143–156. doi: 10.1016/0167-4889(86)90015-7. [DOI] [PubMed] [Google Scholar]
  3. Barbaras R., Grimaldi P., Négrel R., Ailhaud G. Binding of lipoproteins and regulation of cholesterol synthesis in cultured mouse adipose cells. Biochim Biophys Acta. 1985 Jun 30;845(3):492–501. doi: 10.1016/0167-4889(85)90215-0. [DOI] [PubMed] [Google Scholar]
  4. Barbaras R., Puchois P., Fruchart J. C., Ailhaud G. Cholesterol efflux from cultured adipose cells is mediated by LpAI particles but not by LpAI:AII particles. Biochem Biophys Res Commun. 1987 Jan 15;142(1):63–69. doi: 10.1016/0006-291x(87)90451-7. [DOI] [PubMed] [Google Scholar]
  5. Barbaras R., Puchois P., Grimaldi P., Barkia A., Fruchart J. C., Ailhaud G. Relationship in adipose cells between the presence of receptor sites for high density lipoproteins and the promotion of reverse cholesterol transport. Biochem Biophys Res Commun. 1987 Dec 16;149(2):545–554. doi: 10.1016/0006-291x(87)90402-5. [DOI] [PubMed] [Google Scholar]
  6. Basu S. K., Goldstein J. L., Brown M. S. Characterization of the low density lipoprotein receptor in membranes prepared from human fibroblasts. J Biol Chem. 1978 Jun 10;253(11):3852–3856. [PubMed] [Google Scholar]
  7. Biesbroeck R., Oram J. F., Albers J. J., Bierman E. L. Specific high-affinity binding of high density lipoproteins to cultured human skin fibroblasts and arterial smooth muscle cells. J Clin Invest. 1983 Mar;71(3):525–539. doi: 10.1172/JCI110797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blanche P. J., Nichols A. V., Forte T. M., Gong E. L. Characterization of complexes of egg yolk phosphatidylcholine and apolipoprotein A-II prepared in the absence and presence of sodium cholate. Biochim Biophys Acta. 1988 Feb 4;958(2):143–152. doi: 10.1016/0005-2760(88)90171-3. [DOI] [PubMed] [Google Scholar]
  9. Brewer H. B., Jr, Lux S. E., Ronan R., John K. M. Amino acid sequence of human apoLp-Gln-II (apoA-II), an apolipoprotein isolated from the high-density lipoprotein complex. Proc Natl Acad Sci U S A. 1972 May;69(5):1304–1308. doi: 10.1073/pnas.69.5.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brouillette C. G., Jones J. L., Ng T. C., Kercret H., Chung B. H., Segrest J. P. Structural studies of apolipoprotein A-I/phosphatidylcholine recombinants by high-field proton NMR, nondenaturing gradient gel electrophoresis, and electron microscopy. Biochemistry. 1984 Jan 17;23(2):359–367. doi: 10.1021/bi00297a027. [DOI] [PubMed] [Google Scholar]
  11. Chen Y. D., Kraemer F. B., Reaven G. M. Identification of specific high density lipoprotein-binding sites in rat testis and regulation of binding by human chorionic gonadotropin. J Biol Chem. 1980 Oct 10;255(19):9162–9167. [PubMed] [Google Scholar]
  12. Fidge N. H., Nestel P. J. Identification of apolipoproteins involved in the interaction of human high density lipoprotein3 with receptors on cultured cells. J Biol Chem. 1985 Mar 25;260(6):3570–3575. [PubMed] [Google Scholar]
  13. Fidge N. H., Nestel P. J., Suzuki N. Comparison of binding and degradation of high density lipoprotein by intestinal mucosal cells, fibroblasts and adrenal cortical cells in culture. Biochim Biophys Acta. 1983 Aug 29;753(1):14–21. doi: 10.1016/0005-2760(83)90092-9. [DOI] [PubMed] [Google Scholar]
  14. Fidge N., Leonard-Kanevsky M., Nestel P. The hormonal stimulation of high-density lipoprotein binding, internalization and degradation by cultured rat adrenal cortical cells. Biochim Biophys Acta. 1984 Apr 18;793(2):180–186. doi: 10.1016/0005-2760(84)90319-9. [DOI] [PubMed] [Google Scholar]
  15. Fong B. S., Rodrigues P. O., Salter A. M., Yip B. P., Despres J. P., Angel A., Gregg R. E. Characterization of high density lipoprotein binding to human adipocyte plasma membranes. J Clin Invest. 1985 Jun;75(6):1804–1812. doi: 10.1172/JCI111893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fong B. S., Salter A. M., Jimenez J., Angel A. The role of apolipoprotein A-I and apolipoprotein A-II in high-density lipoprotein binding to human adipocyte plasma membranes. Biochim Biophys Acta. 1987 Jul 31;920(2):105–113. doi: 10.1016/0005-2760(87)90249-9. [DOI] [PubMed] [Google Scholar]
  17. Havekes L., Schouten D., van Hinsbergh V., de Wit E. Characterisation of the binding of apolipoprotein E-free high density lipoprotein to cultured human endothelial cells. Biochem Biophys Res Commun. 1984 Jul 31;122(2):785–790. doi: 10.1016/s0006-291x(84)80102-3. [DOI] [PubMed] [Google Scholar]
  18. Hoeg J. M., Demosky S. J., Jr, Edge S. B., Gregg R. E., Osborne J. C., Jr, Brewer H. B., Jr Characterization of a human hepatic receptor for high density lipoproteins. Arteriosclerosis. 1985 May-Jun;5(3):228–237. doi: 10.1161/01.atv.5.3.228. [DOI] [PubMed] [Google Scholar]
  19. Hopkins G. J., Barter P. J. Capacity of lipoproteins to act as substrates for lecithin:cholesterol acyltransferase. Enhancement by pre-incubation with an artificial triacylglycerol emulsion. Biochim Biophys Acta. 1984 Jun 6;794(1):31–40. doi: 10.1016/0005-2760(84)90294-7. [DOI] [PubMed] [Google Scholar]
  20. Hopkins P. N., Williams R. R. A survey of 246 suggested coronary risk factors. Atherosclerosis. 1981 Aug-Sep;40(1):1–52. doi: 10.1016/0021-9150(81)90122-2. [DOI] [PubMed] [Google Scholar]
  21. Hwang J., Menon K. M. Binding of apolipoprotein A-I and A-II after recombination with phospholipid vesicles to the high density lipoprotein receptor of luteinized rat ovary. J Biol Chem. 1985 May 10;260(9):5660–5668. [PubMed] [Google Scholar]
  22. Jackson R. L., Holdsworth G. Isolation and properties of human apolipoproteins C-I, C-II, and C-III. Methods Enzymol. 1986;128:288–297. doi: 10.1016/0076-6879(86)28074-x. [DOI] [PubMed] [Google Scholar]
  23. James R. W., Proudfoot A., Pometta D. Immunoaffinity fractionation of high-density lipoprotein subclasses 2 and 3 using anti-apolipoprotein A-I and A-II immunosorbent gels. Biochim Biophys Acta. 1989 Apr 26;1002(3):292–301. doi: 10.1016/0005-2760(89)90343-3. [DOI] [PubMed] [Google Scholar]
  24. Jonas A., Kézdy K. E., Wald J. H. Defined apolipoprotein A-I conformations in reconstituted high density lipoprotein discs. J Biol Chem. 1989 Mar 25;264(9):4818–4824. [PubMed] [Google Scholar]
  25. Jonas A., Zorich N. L., Kézdy K. E., Trick W. E. Reaction of discoidal complexes of apolipoprotein A-I and various phosphatidylcholines with lecithin cholesterol acyltransferase. Interfacial effects. J Biol Chem. 1987 Mar 25;262(9):3969–3974. [PubMed] [Google Scholar]
  26. Jürgens G., Xu Q. B., Huber L. A., Böck G., Howanietz H., Wick G., Traill K. N. Promotion of lymphocyte growth by high density lipoproteins (HDL). Physiological significance of the HDL binding site. J Biol Chem. 1989 May 25;264(15):8549–8556. [PubMed] [Google Scholar]
  27. Kagami A., Fidge N., Suzuki N., Nestel P. Characteristics of the binding of high-density lipoprotein3 by intact cells and membrane preparations of rat intestinal mucosa. Biochim Biophys Acta. 1984 Sep 12;795(2):179–190. doi: 10.1016/0005-2760(84)90064-x. [DOI] [PubMed] [Google Scholar]
  28. Kilsdonk E. P., Van Gent T., Van Tol A. Characterization of human high-density lipoprotein subclasses LP A-I and LP A-I/A-II and binding to HepG2 cells. Biochim Biophys Acta. 1990 Aug 6;1045(3):205–212. doi: 10.1016/0005-2760(90)90121-d. [DOI] [PubMed] [Google Scholar]
  29. Koschinsky T., Carew T. E., Steinberg D. A comparative study of surface binding of human low density and high density lipoproteins to human fibroblasts: regulation by sterols and susceptibility to proteolytic digestion. J Lipid Res. 1977 Jul;18(4):451–458. [PubMed] [Google Scholar]
  30. Kunitake S. T., La Sala K. J., Kane J. P. Apolipoprotein A-I-containing lipoproteins with pre-beta electrophoretic mobility. J Lipid Res. 1985 May;26(5):549–555. [PubMed] [Google Scholar]
  31. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  32. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  33. Lagocki P. A., Scanu A. M. In vitro modulation of the apolipoprotein composition of high density lipoprotein. Displacement of apolipoprotein A-I from high density lipoprotein by apolipoprotein A-II. J Biol Chem. 1980 Apr 25;255(8):3701–3706. [PubMed] [Google Scholar]
  34. McPherson G. A. Analysis of radioligand binding experiments. A collection of computer programs for the IBM PC. J Pharmacol Methods. 1985 Nov;14(3):213–228. doi: 10.1016/0160-5402(85)90034-8. [DOI] [PubMed] [Google Scholar]
  35. Mendel C. M., Kunitake S. T., Kane J. P. Discrimination between subclasses of human high-density lipoproteins by the HDL binding sites of bovine liver. Biochim Biophys Acta. 1986 Jan 3;875(1):59–68. doi: 10.1016/0005-2760(86)90011-1. [DOI] [PubMed] [Google Scholar]
  36. Munson P. J., Rodbard D. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem. 1980 Sep 1;107(1):220–239. doi: 10.1016/0003-2697(80)90515-1. [DOI] [PubMed] [Google Scholar]
  37. Nichols A. V., Gong E. L., Blanche P. J., Forte T. M. Characterization of discoidal complexes of phosphatidylcholine, apolipoprotein A-I and cholesterol by gradient gel electrophoresis. Biochim Biophys Acta. 1983 Feb 7;750(2):353–364. doi: 10.1016/0005-2760(83)90040-1. [DOI] [PubMed] [Google Scholar]
  38. Oppenheimer M. J., Oram J. F., Bierman E. L. Downregulation of high density lipoprotein receptor activity of cultured fibroblasts by platelet-derived growth factor. Arteriosclerosis. 1987 Jul-Aug;7(4):325–332. doi: 10.1161/01.atv.7.4.325. [DOI] [PubMed] [Google Scholar]
  39. Pitas R. E., Innerarity T. L., Arnold K. S., Mahley R. W. Rate and equilibrium constants for binding of apo-E HDLc (a cholesterol-induced lipoprotein) and low density lipoproteins to human fibroblasts: evidence for multiple receptor binding of apo-E HDLc. Proc Natl Acad Sci U S A. 1979 May;76(5):2311–2315. doi: 10.1073/pnas.76.5.2311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Pitas R. E., Innerarity T. L., Mahley R. W. Cell surface receptor binding of phospholipid . protein complexes containing different ratios of receptor-active and -inactive E apoprotein. J Biol Chem. 1980 Jun 10;255(11):5454–5460. [PubMed] [Google Scholar]
  41. Puchois P., Kandoussi A., Fievet P., Fourrier J. L., Bertrand M., Koren E., Fruchart J. C. Apolipoprotein A-I containing lipoproteins in coronary artery disease. Atherosclerosis. 1987 Nov;68(1-2):35–40. doi: 10.1016/0021-9150(87)90091-8. [DOI] [PubMed] [Google Scholar]
  42. Rifici V. A., Eder H. A. A hepatocyte receptor for high-density lipoproteins specific for apolipoprotein A-I. J Biol Chem. 1984 Nov 25;259(22):13814–13818. [PubMed] [Google Scholar]
  43. Rodbard D., Ruder H. J., Vaitukaitis J., Jacobs H. S. Mathematical analysis of kinetics of radioligand assays: improved sensitivity obtained by delayed addition of labeled ligand. J Clin Endocrinol Metab. 1971 Aug;33(2):343–355. doi: 10.1210/jcem-33-2-343. [DOI] [PubMed] [Google Scholar]
  44. Scanu A. M., Lim C. T., Edelstein C. On the subunit structure of the protein of human serum high density lipoprotein. II. A study of Sephadex fraction IV. J Biol Chem. 1972 Sep 25;247(18):5850–5855. [PubMed] [Google Scholar]
  45. Schmitz G., Niemann R., Brennhausen B., Krause R., Assmann G. Regulation of high density lipoprotein receptors in cultured macrophages: role of acyl-CoA:cholesterol acyltransferase. EMBO J. 1985 Nov;4(11):2773–2779. doi: 10.1002/j.1460-2075.1985.tb04003.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Silberman S. R., Bernini F., Sparrow J. T., Gotto A. M., Jr, Smith L. C. Monoclonal antibodies as probes of high-density lipoprotein structure: identification and localization of a lipid-dependent epitope. Biochemistry. 1987 Sep 8;26(18):5833–5843. doi: 10.1021/bi00392a038. [DOI] [PubMed] [Google Scholar]
  47. Slotte J. P., Oram J. F., Bierman E. L. Binding of high density lipoproteins to cell receptors promotes translocation of cholesterol from intracellular membranes to the cell surface. J Biol Chem. 1987 Sep 25;262(27):12904–12907. [PubMed] [Google Scholar]
  48. Steinmetz A., Barbaras R., Ghalim N., Clavey V., Fruchart J. C., Ailhaud G. Human apolipoprotein A-IV binds to apolipoprotein A-I/A-II receptor sites and promotes cholesterol efflux from adipose cells. J Biol Chem. 1990 May 15;265(14):7859–7863. [PubMed] [Google Scholar]
  49. Sviridov D. D., Misharin A. Y., Safonova I. G., Bushmakina N. G., Repin V. S., Smirnov V. N. Binding of partially reassembled high-density lipoprotein to isolated human small intestine epithelial cells. Effect of lipid composition. Biochim Biophys Acta. 1988 Nov 4;963(1):119–125. doi: 10.1016/0005-2760(88)90344-x. [DOI] [PubMed] [Google Scholar]
  50. Vadiveloo P. K., Fidge N. H. Studies on the interaction between apolipoprotein A-II-enriched HDL3 and cultured bovine aortic endothelial (BAE) cells. Biochim Biophys Acta. 1990 Jul 16;1045(2):135–141. doi: 10.1016/0005-2760(90)90142-k. [DOI] [PubMed] [Google Scholar]
  51. van Tornout P., Caster H., Lievens M. J., Rosseneu M., Assmann G. In vitro interaction of human HDL with human apolipoprotein A-II. Synthesis of apolipoprotein A-II-rich HDL. Biochim Biophys Acta. 1981 Mar 23;663(3):630–636. doi: 10.1016/0005-2760(81)90073-4. [DOI] [PubMed] [Google Scholar]

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