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Interactions of Lipoproteins with Proteoglycans

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Proteoglycan Protocols

Part of the book series: Methods in Molecular Biology™ ((MIMB,volume 171))

Abstract

Significant physiological and pathophysiological processes involve interactions of specific lipoproteins with specific proteoglycans. So far, these interactions fall into two large groups. The first is interactions with heparan sulfate proteoglycans (HSPGs), primarily on the cell surface that lead to cellular uptake of the lipoproteins. These pathways are of interest because they involve endocytic machinery, intracellular itineraries, and regulation that are generally distinct from classic, coated pit-mediated endocytosis (1). Moreover, many important nonlipoprotein ligands, such as infectious agents, growth factors, platelet secretory products, and proteins implicated in Alzheimer’s disease, bind to the same HSPGs, and lipoproteins are a convenient model ligand to study HSPG-mediated catabolism. The second group of lipoprotein- proteoglycan interactions involves chondroitin sulfate proteoglycans (CSPGs), primarily in the extracellular matrix, leading to retention of cholesterol-rich lipoproteins. Many lines of evidence now support the concept that retention of lipoproteins within the arterial wall is the key initial step in provoking atherosclerosis, the major killer in Western countries (2,3t).

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References

  1. Williams, K. J. and Fuki, I. V. (1997) Cell-surface heparan sulfate proteoglycans: dynamic molecules mediating ligand catabolism. Curr. Opin. Lipidol. 8, 252–261.

    Article  Google Scholar 

  2. Williams, K. J. and Tabas, I. (1995) The response-to-retention hypothesis of early atherogenesis. Arterioscler. Thromb. Vasc. Biol. 15, 551–561.

    PubMed  CAS  Google Scholar 

  3. Williams, K. J. and Tabas, I. (1998) The response-to-retention hypothesis of atherogenesis reinforced. Curr. Opin. Lipidol. 9, 471–474.

    Article  PubMed  CAS  Google Scholar 

  4. Tabas, I., Li, Y., Brocia, R. W., Xu, S. W., Swenson, T. L., and Williams, K. J. (1993) Lipoprotein lipase and sphingomyelinase synergistically enhance the association of atherogenic lipoproteins with smooth muscle cells and extracellular matrix. A possible mechanism for low density lipoprotein and lipoprotein(a) retention and macrophage foam cell formation. J. Biol. Chem. 268, 20419–20432.

    PubMed  CAS  Google Scholar 

  5. Hurt-Camejo, E., Olsson, U., Wiklund, O., Bondjers, G., and Camejo, G. (1997) Cellular consequences of the association of apoB lipoproteins with proteoglycans. Potential contribution to atherogenesis. Arterioscler. Thromb. Vasc. Biol. 17, 1011–1017.

    PubMed  CAS  Google Scholar 

  6. Pentikäinen, M. O., Lehtonen, E. M., and Kovanen, P. T. (1996) Aggregation and fusion of modified low density lipoprotein. J. Lip id Res. 37, 2638–2649.

    Google Scholar 

  7. Pentikäinen, M. O., örni, K., Lassila, R., and Kovanen, P. T. (1997) The proteoglycan decorin links low density lipoproteins with collagen type I. J. Biol. Chem. 272, 7633–7638.

    Article  PubMed  Google Scholar 

  8. O’Brien, K.D., Olin, K.L., Alpers, C.E., Chiu, W., Ferguson, M., Hudkins, K., Wight, T. N., and Chait, A. (1998) Comparison of apolipoprotein and proteoglycan deposits in human coronary atherosclerotic plaques: colocalization of biglycan with apolipoproteins. Circulation 98, 519–527.

    PubMed  Google Scholar 

  9. Borén, J., Olin, K. L., Lee, I., Chait, A., Wight, T., and Innerarity, T. L. (1998) Identification of the principal proteoglycan-binding site in LDL. A single point mutation in apoB100 severely affects proteoglycan interaction without affecting LDL receptor binding. J. Clin. Invest. 101, 2658–2664.

    Article  PubMed  Google Scholar 

  10. Borén, J., Olin, K., O’Brien, K. D., Arnold, K. S., Ludwig, E. H., Wight, T. N., Chait, A., and Innerarity, T. L. (1998) Engineering non-atherogenic low density lipoproteins: direct evidence for the “Response-to-Retention” hypothesis of atherosclerosis. Circulation 98(suppl.), I–314 (abstract).

    Google Scholar 

  11. Borén, J., Gustafsson, M., Skålén, K., Flood, C., Innerarity, T.L. (2000) Role of extracellular retention of low density lipoproteins in atherosclerosis. Cur. Opin. Lipidol. 11: 451–456.

    Article  Google Scholar 

  12. Mazany, K. D., Peng, T., Watson, C. E., Tabas, I., and Williams, K. J. (1998) Human chondroitin 6-sulfotransferase: cloning, gene structure, and chromosomal localization. Biochim. Biophys. Acta 1407, 92–97.

    PubMed  CAS  Google Scholar 

  13. Fukuta, M., Kobayashi, Y., Uchimura, K., Kimata, K., and Habuchi, O. (1998) Molecular cloning and expression of human chondroitin 6-sulfotransferase. Biochim. Biophys. Acta 1399, 57–61.

    PubMed  CAS  Google Scholar 

  14. San Antonio, J. D. and Lander, A. D. (2001). Affinity coelectrophoresis of proteoglycanprotein complexes, in Proteoglycan Protocols (R.V. Iozzo, ed.), Humana Press, Totowa, NJ, pp. 401–414.

    Chapter  Google Scholar 

  15. Shen, B. W., Scanu, A. M., and Kezdy, F. J. (1977) Structure of human serum lipoproteins inferred from compositional analysis. Proc. Natl. Acad. Sci. (USA) 74, 837–841.

    Article  CAS  Google Scholar 

  16. Al-Haideri, M., Goldberg, I. J., Galeano, N.F., Gleeson, A., Vogel, T., Gorecki, M., Sturley, S. L., and Deckelbaum, R. J. (1997) Heparan sulfate proteoglycan-mediated uptake of apolipoprotein E-triglyceride-rich lipoprotein particles: a major pathway at physiological particle concentrations. Biochemistry 36, 12766–12772.

    Article  PubMed  CAS  Google Scholar 

  17. Kesaniemi, Y. A., Witztum, J. L., and Steinbrecher, U. P. (1983) Receptor-mediated catabolism of low density lipoprotein in man. Quantitation using glucosylated low density lipoprotein. J. itClin. Invest. 71, 950–959.

    Article  CAS  Google Scholar 

  18. Goldstein, J. L. and Brown, M. S. (1977) Atherosclerosis: the low-density lipoprotein receptor hypothesis. Metabolism 26, 1257–1275.

    Article  PubMed  CAS  Google Scholar 

  19. Havel, R. J., Eder, H. A., and Bragdon, J. H. (1955) The distribution and chemical composition of ultracentrifually separated lipoproteins in human serum. J. Clin. Invest. 34, 1345–1353.

    Article  PubMed  CAS  Google Scholar 

  20. Goldstein, J. L., Basu, S. K., and Brown, M. S. (1983) Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Meth. Enzymol. 98, 241–260.

    Article  PubMed  CAS  Google Scholar 

  21. McFarlane, A. S. (1958) Efficient trace-labelling of proteins with iodine. Nature 182, 53.

    Article  PubMed  CAS  Google Scholar 

  22. Bilheimer, D. W., Eisenberg, S., and Levy, R. I. (1972) The metabolism of very low density lipoprotein proteins. I. Preliminary in vitro and in vivo observations. Biochim. Biophys. Acta 260, 212–221.

    PubMed  CAS  Google Scholar 

  23. Innerarity, T. L., Pitas, R. E., and Mahley, R. W. (1986) Lipoprotein-receptor interactions. Meth. Enzymol. 129, 542–565.

    Article  PubMed  CAS  Google Scholar 

  24. Pitas, R.E., Innerarity, T. L., Weinstein, J. N., and Mahley, R. W. (1981) Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1, 177–185.

    PubMed  CAS  Google Scholar 

  25. Teupser, D., Thiery, J., Walli, A. K., and Seidel, D. (1996) Determination of LDL-and scavenger-receptor activity in adherent and non-adherent cultured cells with a new singlestep fluorometric assay. Biochim. Biophys. Acta 1303, 193–198.

    PubMed  Google Scholar 

  26. Scherberg, N. H., Seo, H., and Hynes, R. (1978) Incorporation of radioiodotyroisines into proteins formed during cell-free translation. J. itBiol. Chem. 253, 1773–1779.

    CAS  Google Scholar 

  27. Bierman, E. L., Stein, O., and Stein, Y. (1974) Lipoprotein uptake and metabolism by rat aortic smooth muscle cells in tissue culture. Circ. Res. 35,136–150.

    PubMed  CAS  Google Scholar 

  28. Fuki, I. V., Kuhn, K. M., Lomazov, I. R., Rothman, V. L., Tuszynski, G. P., Iozzo, R. V., Swenson, T. L., Fisher, E. A., and Williams, K. J. (1997) The syndecan family of proteoglycans: novel receptors mediating internalization of atherogenic lipoproteins in vitro. J. Clin. Invest. 100, 1611–1622.

    Article  CAS  Google Scholar 

  29. Chen, T. R., Drabkowski, D., Hay, R. J., Macy, M., and Peterson, W., Jr. (1987) WiDr is a derivative of another colon adenocarcinoma cell line, HT-29. Cancer Genet. Cytogenet. 27, 125–134.

    Article  PubMed  CAS  Google Scholar 

  30. Iozzo, R. V. (1984) Biosynthesis of heparan sulfate proteoglycan by human colon carcinoma cells and its localization at the cell surface. J. Cell Biol. 99, 403–417.

    Article  PubMed  CAS  Google Scholar 

  31. Iozzo, R. V. (1987) Turnover of heparan sulfate proteoglycan in human colon carcinoma cells. A quantitative biochemical and autoradiographic study. J. Biol. Chem. 262,1888–1900.

    PubMed  CAS  Google Scholar 

  32. Fuki, I. V., Iozzo, R. V., and Williams, K. J. (1996) Perlecan heparan sulfate proteoglycan (HSPG): a novel, distinct receptor for atherogenic lipoproteins. Circulation 94(suppl. I), 698–699 (abstract).

    Google Scholar 

  33. Fuki, I. V., Iozzo, R. V., and Williams, K. J. (2000). Perlecan heparan sulfate proteoglycan: a novel receptor that mediates a distinct pathway for ligand catabolism. J. Biol. Chem. 275, 25742–25750.

    Article  PubMed  CAS  Google Scholar 

  34. Liu, W., Litwack, E. D., Stanley, M. J., Langford, J. K., Lander, A. D., and Sanderson, R. D. (1998) Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. . Biol. Chem. 273, 22825–22832.

    Article  CAS  Google Scholar 

  35. Williams, K. J., Fless, G. M., Petrie, K. A., Snyder, M. L., Brocia, R. W., and Swenson, T. L. (1992) Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins. Roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J. Biol. Chem. 267, 13284–13292.

    PubMed  CAS  Google Scholar 

  36. Socorro, L., Green, C. C., and Jackson, R. L. (1985) Preparation of a homogeneous and stable form of bovine milk lipoprotein lipase. Prep. Biochem. 15, 133–143.

    Article  PubMed  CAS  Google Scholar 

  37. Saxena, U., Witte, L. D., and Goldberg, I. J. (1989) Release of endothelial cell lipoprotein lipase by plasma lipoproteins and free fatty acids. J. Biol. Chem. 264, 4349–4355.

    PubMed  CAS  Google Scholar 

  38. Rumsey, S. C., Obunike, J. C., Arad, Y., Deckelbaum, R. J., and Goldberg, I. J. (1992) Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J. Clin. Invest. 90, 1504–1512.

    Article  PubMed  CAS  Google Scholar 

  39. Ji, Z. S., Fazio, S., Lee, Y. L., and Mahley, R. W. (1994) Secretion-capture role for apolipoprotein E in remnant lipoprotein metabolism involving cell surface heparan sulfate proteoglycans. J. Biol. Chem. 269, 2764–2772.

    PubMed  CAS  Google Scholar 

  40. Ji, Z. S., Lauer, S. J., Fazio, S., Bensadoun, A., Taylor, J. M., and Mahley, R. W. (1994) Enhanced binding and uptake of remnant lipoproteins by hepatic lipase-secreting hepatoma cells in culture. J. Biol. Chem. 269, 13429–13436.

    PubMed  CAS  Google Scholar 

  41. Eisenberg, S., Sehayek, E., Olivecrona, T., and Vlodavsky, I. (1992) Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J. Clin. Invest. 90, 2013–2021.

    Article  PubMed  CAS  Google Scholar 

  42. Mulder, M., Lombardi, P., Jansen, H., van Berkel, T. J., Frants, R. R., and Havekes, L. M. (1993) Low density lipoprotein receptor internalizes low density and very low density lipoproteins that are bound to heparan sulfate proteoglycans via lipoprotein lipase. J. Biol. Chem. 268, 9369–9375.

    PubMed  CAS  Google Scholar 

  43. Esko, J. D. (1991) Genetic analysis of proteoglycan structure, function and metabolism. Curr. Opin. Cell Biol. 3, 805–816.

    Article  PubMed  CAS  Google Scholar 

  44. Higazi, A. A-R., Nassar, T., Ganz, T., Rader, D.J. Udassin, R., Bdeir, K., et al. (2000) The α-defensins stimulate proteoglycan-dependent catabolism of low-density lipoprotein by vascular cells: a new class of inflammatory apolipoprotein and a possible contributor to atherogenesis. Blood 96:1393–1398.

    PubMed  CAS  Google Scholar 

  45. Humphries, D. E. and Silbert, J. E. (1988) Chlorate: a reversible inhibitor of proteoglycan sulfation. Biochem. Biophys. Res. Commun. 154, 365–371.

    Article  PubMed  CAS  Google Scholar 

  46. Sehayek, E., Olivecrona, T., Bengtsson-Olivecrona, G., Vlodavsky, I., Levkovitz, H, Avner, R, and Eisenberg, S. (1995) Binding to heparan sulfate is a major event during catabolism of lipoprotein lipase by HepG2 and other cell cultures. Atherosclerosis 114, 1–8.

    Article  PubMed  CAS  Google Scholar 

  47. Seo, T. and St.Clair, R. W. (1997) Heparan sulfate proteoglycans mediate internalization and degradation of β-VLDL and promote cholesterol accumulation by pigeon macrophages. J. LipidRes. 38, 765–779.

    CAS  Google Scholar 

  48. Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., and Pericak-Vance, M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 261, 921–923.

    Article  PubMed  CAS  Google Scholar 

  49. Ji, Z. S., Pitas, R. E., and Mahley, R. W. (1998) Differential cellular accumulation/retention of apolipoprotein E mediated by cell surface heparan sulfate proteoglycans. Apolipoproteins E3 and E2 greater than E4. J. Biol. Chem. 273, 13,452–13,460.

    Article  PubMed  CAS  Google Scholar 

  50. Pitas, R. E., Ji, Z.-S., Fuki, I. V., Williams, K. J., and Mahley, R. W. (1998) ApoE isoforms and neurite outgrowth: possible role of heparan sulfate proteoglycans. Neurobiol. Aging 19(4S), S222 (abstract).

    Google Scholar 

  51. Lund-Katz, S., Ibdah, J. A., Letizia, J. Y., Thomas, M. T., and Phillips, M. C. (1988) A 13C NMR characterization of lysine residues in apolipoprotein B and their role in binding to the low density lipoprotein receptor. J. Biol. Chem. 263, 13,831–13,838.

    PubMed  CAS  Google Scholar 

  52. Goldberg, I. J., Wagner, W. D., Pang, L., Paka, L., Curtiss, L. K., DeLozier, J. A., Shelness, G. S., Young, C. S. H., and Pillarisetti, S. (1998) The NH2-terminal region of apolipoprotein B is sufficient for lipoprotein association with glycosaminoglycans. J. Biol. Chem. 273, 35,355–35,361.

    Article  PubMed  CAS  Google Scholar 

  53. Burgess, J. W., Gould, D. R., and Marcel, Y. L. (1998) The HepG2 extracellular matrix contains separate heparinase-and lipid-releasable pools of ApoE. Implications for hepatic lipoprotein metabolism. J. Biol. Chem. 273, 5645–5654.

    Article  PubMed  CAS  Google Scholar 

  54. Koo, C., Wernette-Hammond, M. E., and Innerarity, T. L. (1986) Uptake of canine β-very low density lipoproteins by mouse peritoneal macrophages in mediated by a low density lipoprotein receptor. J. Biol. Chem. 261, 11194–11201.

    PubMed  CAS  Google Scholar 

  55. Beisiegel, U., Schneider, W. J., Goldstein, J. L., Anderson, R. G. W., and Brown, M. S. (1981) Monoclonal antibodies to the low density lipoprotein receptor as probes for study of receptor-mediated endocytosis and the genetics of familial hypercholesterolemia. J. Biol. Chem. 256, 11,923–11,931.

    PubMed  CAS  Google Scholar 

  56. van Driel, I. R., Brown, M. S., and Goldstein, J. L. (1989) Stoichiometric binding of low density lipoprotein (LDL) and monoclonal antibodies to LDL receptors in a solid phase assay. J. Biol. Chem. 264, 9533–9538.

    PubMed  Google Scholar 

  57. Vijayagopal, P., Figueroa, J. E., Guo, Q., Fontenot, J. D., and Tao, Z. (1996) Marked alteration of proteoglycan metabolism in cholesterol-enriched human arterial smooth muscle cells. Biochem. J. 315, 995–1000.

    PubMed  CAS  Google Scholar 

  58. Tabas, I., Weiland, D. A., and Tall, A. R. (1986) Inhibition of acylcoenzyme A:cholesterol acyl transferase in J774 macrophages enhances down-regulation of the low density lipoprotein receptor and 3-hydroxy-3-methylglutaryl-coenzyme A reductase and prevents low density lipoprotein-induced cholesterol accumulation. J. Biol. Chem. 261, 3147–3155.

    PubMed  CAS  Google Scholar 

  59. Dueland, S., Trawick, J. D., Nenseter, M. S., MacPhee, A. A., and Davis, R. A. (1992) Expression of 7 α-hydroxylase in non-hepatic cells results in liver phenotypic resistance of the low density lipoprotein receptor to cholesterol repression. J. Biol. Chem. 267, 22,695–22,698.

    PubMed  CAS  Google Scholar 

  60. Sege, R. D., Kozarsky, K. F., and Krieger, M. (1986) Characterization of a family of gamma-ray-induced CHO mutants demonstrates that the ldlA locus is diploid and encodes the low-density lipoprotein receptor. Mol. Cell Biol. 6, 3268–3277.

    PubMed  CAS  Google Scholar 

  61. Ishibashi, S., Brown, M. S., Goldstein, J. L., Gerard, R. D., Hammer, R. E., and Herz, J. (1993) Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92, 883–893.

    Article  PubMed  CAS  Google Scholar 

  62. Williams, S. E., Ashcom, J. D., Argraves, W. S., and Strickland, D. K. (1992) A novel mechanism for controlling the activity of α2 macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J. Biol. Chem. 267, 9035–9040.

    PubMed  CAS  Google Scholar 

  63. Strickland, D. K., Ashcom, J. D., Williams, S., Battey, F., Behre, E., McTigue, K., Battey, J. F., and Argraves, W. S. (1991) Primary structure of α2 macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266, 13364–13369.

    CAS  Google Scholar 

  64. Ji, Z-S. and Mahley, R. W. (1994) Lactoferrin binding to heparan sulfate proteoglycans and the LDL receptor-related protein. Further evidence supporting the importance of direct binding of remnant lipoproteins to HSPG. Arterioscler. Thromb. 14, 2025–2032.

    PubMed  CAS  Google Scholar 

  65. Vassiliou, G. and Stanley, K. K. (1994) Exogenous receptor-associated protein binds to two distinct sites on human fibroblasts but does not bind to the glycosaminoglycan residues of heparan sulfate proteoglycans. J. Biol. Chem. 269, 15,172-15,178.

    Google Scholar 

  66. Lyon, M., Deakin, J. A., and Gallagher, J. T. (1994) Liver heparan sulfate structure. A novel molecular design. J. Biol. Chem. 269, 11,208–11,215.

    PubMed  CAS  Google Scholar 

  67. Willnow, T. E. and Herz, J. (1994) Genetic deficiency in low density lipoprotein receptorrelated protein confers cellular resistance to Pseudomonas exotoxin A. Evidence that this protein is required for uptake and degradation of multiple ligands. J. Cell Sci. 107, 719–726.

    PubMed  CAS  Google Scholar 

  68. FitzGerald, D. J., Fryling, C. M., Zdanovsky, A., Saelinger, C. B., Kounnas, M., Winkles, J. A., Strickland, D., and Leppla, S. (1995) Pseudomonas exotoxin-mediated selection yields cells with altered expression of low-density lipoprotein receptor-related protein. J. Cell Biol. 129,1533–1541.

    Article  PubMed  CAS  Google Scholar 

  69. Sehayek, E., Wang, X. X., Vlodavsky, I., Avner, R., Levkovitz, H., Olivecrona, T., Olivecrona, G., Willnow, T. E., Herz, J., and Eisenberg, S. (1996) Heparan sulfate-dependent and low density lipoprotein receptor-related protein-dependent catabolic pathways for lipoprotein lipase in mouse embryonic fibroblasts. Isr. J. Med. Sci. 32, 449–454.

    PubMed  CAS  Google Scholar 

  70. Rohlmann, A., Gotthardt, M., Hammer, R. E., and Herz, J. (1998) Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J. Clin. Invest. 101, 689–695.

    Article  PubMed  CAS  Google Scholar 

  71. Chappell, D. A., Fry, G. L., Waknitz, M. A., Iverius, P-H., Williams, S. E., and Strickland, D. K. (1992) The low density lipoprotein receptor-related protein/α2 macroglobulin receptor binds and mediates catabolism of bovine lipoprotein lipase. J. Biol. Chem. 267, 25,764–25,767.

    PubMed  CAS  Google Scholar 

  72. Mahley, R. W., Ji, Z. S., Brecht, W. J., Miranda, R. D., and He, D. (1994) Role of heparan sulfate proteoglycans and the LDL receptor-related protein in remnant lipoprotein metabolism. Ann. N.Y. Acad. Sci. 737, 39–52.

    Article  PubMed  CAS  Google Scholar 

  73. Beisiegel, U. (1995) Receptors for triglyceride-rich lipoproteins and their role in lipopro-tein metabolism. Curr. Opin. Lipidol. 6, 117–122.

    Article  PubMed  CAS  Google Scholar 

  74. Brown, M. S. and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34–47.

    Article  PubMed  CAS  Google Scholar 

  75. Weigel, P. H. and Oka, J. A. (1982) Endocytosis and degradation mediated by the asialoglycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 257, 1201–1207.

    PubMed  CAS  Google Scholar 

  76. Akiyama, T., Ishida, J., Nakagawa, S., Ogawara, H., Watanabe, S., Itoh, N., Shibuya, M., and Fukami, Y. (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262, 5592–5595.

    PubMed  CAS  Google Scholar 

  77. Sampath, P. and Pollard, T.D. (1991) Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 19(30), 1973–1980.

    Article  Google Scholar 

  78. Luton, F., Buferne, M., Davoust, J., Schmitt-Verhulst, A.M., and Boyer, C. (1994) Evidence for protein tyrosine kinase involvement in ligand-induced TCR/CD3 internaliza-tion and surface redistribution. J. Immunol. 153, 63–72.

    PubMed  CAS  Google Scholar 

  79. Khoo, J. C., Miller, E., McLoughlin, P., and Steinberg, D. (1988) Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis 8, 348–358.

    PubMed  CAS  Google Scholar 

  80. Yanagishita, M. (1992) Glycosylphosphatidylinositol-anchored and core protein-intercalated heparan sulfate proteoglycans in rat ovarian granulosa cells have distinct secretory, endocytotic, and intracellular degradative pathways. J. Biol. Chem. 267, 9505–9511.

    PubMed  CAS  Google Scholar 

  81. Fuki, I. V. and Williams, K. J. (1998) Direct internalization of atherogenic lipoproteins by syndecan heparan sulfate proteoglycans is a multi-step process independent of coated pits. Circulation 98(suppl.), I–109 (abstract).

    Google Scholar 

  82. Fuki, I. V., Meyer, M. E., and Williams, K. J. (1999). Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 351, 607–612.

    Article  Google Scholar 

  83. Fuki, I. V., Mazany, K. D., and Williams, K. J. (1999) Molecular determinants of syndecan-mediated endocytosis, a novel, multi-step pathway independent of coated pits. Circulation 100(suppl.), I–706 (abstract).

    Google Scholar 

  84. Williams, K. J., Petrie, K. A., Brocia, R. W., and Swenson, T. L. (1991) Lipoprotein lipase modulates net secretory output of apolipoprotein B in vitro. A possible pathophysiologic explanation for familial combined hyperlipidemia. J. Clin. Invest. 88, 1300–1306.

    Article  PubMed  CAS  Google Scholar 

  85. Markwell, M. A. K., Haas, S. M., Bieber, L. L., and Tolbert, N. E. (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87, 206–210.

    Article  PubMed  CAS  Google Scholar 

  86. Davis, W., Harrison, P. T., Hutchinson, M. J., and Allen, J. M. (1995) Two distinct regions of Fcγ RI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO J. 14, 432–441.

    PubMed  CAS  Google Scholar 

  87. Jentoft, N. and Dearborn, D. G. (1983) Protein labeling by reductive alkylation. Methods Enzymol. 91, 570–579.

    Article  PubMed  CAS  Google Scholar 

  88. Rapraeger, A., Jalkanen, M., and Bernfield, M. (1986) Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J. Cell Biol. 103, 2683–2696.

    Article  PubMed  CAS  Google Scholar 

  89. Miettinen, H. M. and Jalkanen, M. (1994) The cytoplasmic domain of syndecan-1 is not required for association with TritonX-100-insoluble material. J. CellSci. 107,1571–1581.

    CAS  Google Scholar 

  90. Carey, D. J., Bendt, K. M., and Stahl, R. C. (1996) The cytoplasmic domain of syndecan1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J. Biol. Chem. 271, 15,253–15,260.

    Article  PubMed  CAS  Google Scholar 

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  1. The Dorrance H. Hamilton Research Laboratories, Division of Endocrinology, Diabetes, and Metabolic Diseases, Department of Medicine, Jefferson Medical College of Thomas Jefferson University, Philadelphia, PA

    Kevin Jon Williams

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  1. Department of Pathology, Anatomy, and Cell Biology, Thomas Jefferson University, Philadelphia, PA

    Renato V. Iozzo MD

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Williams, K.J. (2001). Interactions of Lipoproteins with Proteoglycans. In: Iozzo, R.V. (eds) Proteoglycan Protocols. Methods in Molecular Biology™, vol 171. Humana Press. https://doi.org/10.1385/1-59259-209-0:457

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  • DOI: https://doi.org/10.1385/1-59259-209-0:457

  • Publisher Name: Humana Press

  • Print ISBN: 978-0-89603-759-5

  • Online ISBN: 978-1-59259-209-8

  • eBook Packages: Springer Protocols

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