Abstract
To elucidate further the binding of high-density-lipoprotein subfraction 3 (HDL3) to cells, the involvement of glycosylphosphatidylinositol-anchored proteins (GPI-proteins) was studied. Treatment of cultured cells, such as fibroblasts or SK-MES-1 cells, with a phosphatidylinositol-specific phospholipase C (PI-PLC) significantly decreases specific HDL3 binding. Moreover, PI-PLC treatment of cultured cells or cellular plasma membrane fractions results in releasing proteins. These proteins have a soluble form and can also bind HDL3, as revealed by ligand blotting experiments with HDL3. In order to obtain enriched GPI-proteins, we used a detergent-free purification method to prepare a caveolar membrane fraction. In the caveolar fraction, we obtained, by ligand blotting experiments, the enrichment of two HDL3-binding proteins with molecular masses of 120 and 80 kDa. These proteins were also revealed in a plasma membrane preparation with two other proteins, with molecular masses of 150 and 104 kDa, and were sensitive to PI-PLC treatment. Electron microscopy also showed the binding of Au-labelled HDL3 inside the caveolar membrane invaginations. In SK-MES-1 cells, HDL3 are internalized into a particular structure, resulting in the accumulation and concentration of such specific membrane domains. To sum up, a demonstration has been made of the implication of GPI-proteins as well as caveolae in the binding of HDL3 to cells.
Full Text
The Full Text of this article is available as a PDF (577.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Acton S., Rigotti A., Landschulz K. T., Xu S., Hobbs H. H., Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996 Jan 26;271(5248):518–520. doi: 10.1126/science.271.5248.518. [DOI] [PubMed] [Google Scholar]
- Anderson R. G., Kamen B. A., Rothberg K. G., Lacey S. W. Potocytosis: sequestration and transport of small molecules by caveolae. Science. 1992 Jan 24;255(5043):410–411. doi: 10.1126/science.1310359. [DOI] [PubMed] [Google Scholar]
- Anderson R. G. Plasmalemmal caveolae and GPI-anchored membrane proteins. Curr Opin Cell Biol. 1993 Aug;5(4):647–652. doi: 10.1016/0955-0674(93)90135-d. [DOI] [PubMed] [Google Scholar]
- BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
- Barbaras R., Puchois P., Fruchart J. C., Pradines-Figueres A., Ailhaud G. Purification of an apolipoprotein A binding protein from mouse adipose cells. Biochem J. 1990 Aug 1;269(3):767–773. doi: 10.1042/bj2690767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Betard C., Vu-Dac N., Mezdour H., Nestruck A. C., Leroy A., Fruchart J. C. Standardization of an enzymometric assay for apolipoprotein A-I by using mixtures of monoclonal antibodies). J Clin Chem Clin Biochem. 1987 Dec;25(12):893–899. doi: 10.1515/cclm.1987.25.12.893. [DOI] [PubMed] [Google Scholar]
- Bilheimer D. W., Eisenberg S., Levy R. I. The metabolism of very low density lipoprotein proteins. I. Preliminary in vitro and in vivo observations. Biochim Biophys Acta. 1972 Feb 21;260(2):212–221. doi: 10.1016/0005-2760(72)90034-3. [DOI] [PubMed] [Google Scholar]
- Bond H. M., Morrone G., Venuta S., Howell K. E. Characterization and purification of proteins which bind high-density lipoprotein. A putative cell-surface receptor. Biochem J. 1991 Nov 1;279(Pt 3):633–641. doi: 10.1042/bj2790633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davitz M. A., Low M. G., Nussenzweig V. Release of decay-accelerating factor (DAF) from the cell membrane by phosphatidylinositol-specific phospholipase C (PIPLC). Selective modification of a complement regulatory protein. J Exp Med. 1986 May 1;163(5):1150–1161. doi: 10.1084/jem.163.5.1150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferreri K., Menon K. M. Characterization and isolation of a high-density-lipoprotein-binding protein from bovine corpus luteum plasma membrane. Biochem J. 1992 Nov 1;287(Pt 3):841–848. doi: 10.1042/bj2870841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fielding P. E., Fielding C. J. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry. 1995 Nov 7;34(44):14288–14292. doi: 10.1021/bi00044a004. [DOI] [PubMed] [Google Scholar]
- Fujiki Y., Hubbard A. L., Fowler S., Lazarow P. B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol. 1982 Apr;93(1):97–102. doi: 10.1083/jcb.93.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham D. L., Oram J. F. Identification and characterization of a high density lipoprotein-binding protein in cell membranes by ligand blotting. J Biol Chem. 1987 Jun 5;262(16):7439–7442. [PubMed] [Google Scholar]
- HAVEL R. J., EDER H. A., BRAGDON J. H. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest. 1955 Sep;34(9):1345–1353. doi: 10.1172/JCI103182. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Handley D. A., Arbeeny C. M., Eder H. A., Chien S. Hepatic binding and internalization of low density lipoprotein-gold conjugates in rats treated with 17 alpha-ethinylestradiol. J Cell Biol. 1981 Sep;90(3):778–787. doi: 10.1083/jcb.90.3.778. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hidaka H., Fidge N. H. Affinity purification of the hepatic high-density lipoprotein receptor identifies two acidic glycoproteins and enables further characterization of their binding properties. Biochem J. 1992 May 15;284(Pt 1):161–167. doi: 10.1042/bj2840161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hokland B., Mendez A. J., Oram J. F. Cellular localization and characterization of proteins that bind high density lipoprotein. J Lipid Res. 1992 Sep;33(9):1335–1342. [PubMed] [Google Scholar]
- Kilgour E. A role for inositol-glycan mediators and G-proteins in insulin action. Cell Signal. 1993 Mar;5(2):97–105. doi: 10.1016/0898-6568(93)90062-q. [DOI] [PubMed] [Google Scholar]
- Kurzchalia T. V., Parton R. G. And still they are moving.... dynamic properties of caveolae. FEBS Lett. 1996 Jun 24;389(1):52–54. doi: 10.1016/0014-5793(96)00585-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Li S., Okamoto T., Chun M., Sargiacomo M., Casanova J. E., Hansen S. H., Nishimoto I., Lisanti M. P. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem. 1995 Jun 30;270(26):15693–15701. doi: 10.1074/jbc.270.26.15693. [DOI] [PubMed] [Google Scholar]
- Low M. G. The glycosyl-phosphatidylinositol anchor of membrane proteins. Biochim Biophys Acta. 1989 Dec 6;988(3):427–454. doi: 10.1016/0304-4157(89)90014-2. [DOI] [PubMed] [Google Scholar]
- Mayor S., Rothberg K. G., Maxfield F. R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 1994 Jun 24;264(5167):1948–1951. doi: 10.1126/science.7516582. [DOI] [PubMed] [Google Scholar]
- McKnight G. L., Reasoner J., Gilbert T., Sundquist K. O., Hokland B., McKernan P. A., Champagne J., Johnson C. J., Bailey M. C., Holly R. Cloning and expression of a cellular high density lipoprotein-binding protein that is up-regulated by cholesterol loading of cells. J Biol Chem. 1992 Jun 15;267(17):12131–12141. [PubMed] [Google Scholar]
- Mendez A. J., Oram J. F., Bierman E. L. Protein kinase C as a mediator of high density lipoprotein receptor-dependent efflux of intracellular cholesterol. J Biol Chem. 1991 Jun 5;266(16):10104–10111. [PubMed] [Google Scholar]
- Nazih-Sanderson F., Pinchon G., Nion S., Fruchart J. C., Delbart C. HDL3-signalling in HepG2 cells involves glycosyl-phosphatidylinositol-anchored proteins. Biochim Biophys Acta. 1997 May 17;1346(1):45–60. doi: 10.1016/s0005-2760(97)00017-9. [DOI] [PubMed] [Google Scholar]
- Parton R. G. Caveolae and caveolins. Curr Opin Cell Biol. 1996 Aug;8(4):542–548. doi: 10.1016/s0955-0674(96)80033-0. [DOI] [PubMed] [Google Scholar]
- Powis G., Seewald M. J., Gratas C., Melder D., Riebow J., Modest E. J. Selective inhibition of phosphatidylinositol phospholipase C by cytotoxic ether lipid analogues. Cancer Res. 1992 May 15;52(10):2835–2840. [PubMed] [Google Scholar]
- Rogler G., Trümbach B., Klima B., Lackner K. J., Schmitz G. HDL-mediated efflux of intracellular cholesterol is impaired in fibroblasts from Tangier disease patients. Arterioscler Thromb Vasc Biol. 1995 May;15(5):683–690. doi: 10.1161/01.atv.15.5.683. [DOI] [PubMed] [Google Scholar]
- Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. doi: 10.1016/0092-8674(92)90143-z. [DOI] [PubMed] [Google Scholar]
- Rothberg K. G., Ying Y. S., Kamen B. A., Anderson R. G. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J Cell Biol. 1990 Dec;111(6 Pt 2):2931–2938. doi: 10.1083/jcb.111.6.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnitzer J. E., Oh P., Pinney E., Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol. 1994 Dec;127(5):1217–1232. doi: 10.1083/jcb.127.5.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smart E. J., Ying Y. S., Mineo C., Anderson R. G. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10104–10108. doi: 10.1073/pnas.92.22.10104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang L. H., Rothberg K. G., Anderson R. G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol. 1993 Dec;123(5):1107–1117. doi: 10.1083/jcb.123.5.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de la Llera Moya M., Atger V., Paul J. L., Fournier N., Moatti N., Giral P., Friday K. E., Rothblat G. A cell culture system for screening human serum for ability to promote cellular cholesterol efflux. Relations between serum components and efflux, esterification, and transfer. Arterioscler Thromb. 1994 Jul;14(7):1056–1065. doi: 10.1161/01.atv.14.7.1056. [DOI] [PubMed] [Google Scholar]