Cell-surface heparan sulfate proteoglycans: Dynamic molecules mediating ligand catabolism

Current Opinion in Lipidology

Volumn 8, Issue 5, 1997, Pages 253-262

  Williams, Kevin Jon ^a   Fuki, Ilia V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; GLYCOSAMINOGLYCAN; LIGAND; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE ANTIGEN; PERLECAN; PROTEIN; PROTEOHEPARAN SULFATE; SYNDECAN;

ARTERY WALL; CATABOLISM; CELL MEMBRANE; CELL SURFACE; CYTOPLASM; EVOLUTION; INTERNALIZATION; LIVER; PATHOPHYSIOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; REVIEW;

EID: 0030775796     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-199710000-00003     Document Type: Review

References (116)

1. Avery OT, MacLeod CM, McCarty M: Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a deoxyribonucleic acid fraction isolated from pneumococcus Type III. J Exp Med 1944, 79:137-157.
2. Stryer L: Biochemistry 3rd edn. New York: WH Freeman and Company; 1988.
3. Rigotti A, Acton SL, Krieger M: The class B scavenger receptors SR-Bl and CD36 are receptors for anionic phospholipids. J Biol Chem 1995, 270:16221-16224.
4. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ: Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 1992, 8:365-393.
5. Spicer AP, Olson JS, McDonald JA: Molecular cloning and characterization of a cDNA encoding the third putative mammalian hyaluronan synthase. J Biol Chem 1997, 272:8957-8961.
6. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD et al.: Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 1996, 273:1058-1073.
7. 13C-n.m.r.-spectral evidence. Carbohydr Res 1988, 184:292-300.
8. Spring J, Paine-Saunders SE, Hynes RO, Bernfield M: Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. Proc Natl Acad Sci U S A 1994, 91:3334-3338.
9. Esko JD: Genetic analysis of proteoglycan structure, function and metabolism. Curr Opin Cell Biol 1991, 3:805-816.
10. Parthasarathy N, Goldberg IJ, Sivaram P, Mulloy B, Flory DM, Wagner WD: Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase. J Biol Chem 1994, 269:22391-22396.
11. Williams KJ: Atherosclerosis: cell biology and lipoproteins. Curr Opin Lipidol 1996, 7:U202-U208.
12. David G: Integral membrane heparan sulfate proteoglycans. FASEB J 1993, 7:1023-1030.
13. Salmivirta M, Jalkanen M: Syndecan family of cell surface proteoglycans: developmentally regulated receptors for extracellular effector molecules. Experientia 1995, 51:863-872.
14. Iozzo RV, Murdoch AD. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J 1996, 10:598-614.
15. Iozzo RV: Turnover of heparan sulfate proteoglycan in human colon carcinoma cells. A quantitative biochemical and autoradiographic study. J Biol Chem 1987, 262:1888-1900.
16. Yanagishita M: 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 1992, 267:9505-9511.
17. 1/2 for liver HSPGs was 16 h. Turnover rates in different tissues varied widely.
18. Robinson DS: The clearing factor lipase and its action in the transport of fatty acids between the blood and the tissues. Adv Lipid Res 1963, 1:133-182.
19. Williams KJ, Fless GM, Petrie K, Snyder ML, Brocia RW, Swenson TL: Lipoprotein lipase enhances cellular catabolism of lipoprotein (a) [Abstract]. Circulation 1991, 84(suppl II): 566.
20. Williams KJ, Fless GM, Petrie KA, Snyder ML, Brocia RW, Swenson TL: 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 1992, 267:13284-13292.
21. Eisenberg S, Sehayek E, Olivecrona T, Vlodavsky I: Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J Clin Invest 1992, 90:2013-2021.
22. Mulder M, Lombardi P, Jansen H, van Berkel TJ, Frants RR, Havekes LM: 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 1993, 268:9369-9375.
23. Rumsey SC, Obunike JC, Arad Y, Deckelbaum RJ, Goldberg IJ: Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J Clin Invest 1992, 90:1504-1512.
24. Ji ZS, Brecht WJ, Miranda RD, Hussain MM, Innerarity TL, Mahley RW: Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells. J Biol Chem 1993, 268:10160-10167.
25. Ji ZS, Lauer SJ, Fazio S, Bensadoun A, Taylor JM, Mahley RW: Enhanced binding and uptake of remnant lipoproteins by hepatic lipase-secreting hepatoma cells in culture. J Biol Chem 1994, 269:13429-13436.
26. van Barlingen HH, de Jong H, Erkelens DW, de Bruin TW: Lipoprotein lipase-enhanced binding of human triglyceride-rich lipoproteins to heparan sulfate: modulation by apolipoprotein E and apolipoprotein C. J Lipid Res 1996, 37:754-763.
27. Aalto-Setälä K, Weinstock PH, Bisgaier CL, Wu L, Smith JD, Breslow JL: Further characterization of the metabolic properties of triglyceride-rich lipoproteins from human and mouse apoC-III transgenic mice. J Lipid Res 1996, 37:1802-1811.
28. Shachter NS, Ebara T, Ramakrishnan R, Steiner G, Breslow JL, Ginsberg HN, Smith JD: Combined hyperlipidemia in transgenic mice overexpressing human apolipoprotein Cl. J Clin Invest 1996, 98:846-655.
29. Mahley RW, Ji ZS, Brecht WJ, Miranda RD, He D: Role of heparan sulfate proteoglycans and the LDL receptor-related protein in remnant lipoprotein metabolism. Ann NY Acad Sci 1994, 737:39-52.
30. Beisiegel U: Receptors for triglyceride-rich lipoproteins and their role in lipoprotein metabolism. Curr Opin Lipidol 1995, 6:117-122.
31. Rapraeger AC, Krufka A, Olwin BB: Requirement of heparan sulfate for bFGF-medlated fibroblast growth and myoblast differentiation. Science 1991, 252:1705-1708.
32. Aviezer D, Hecht D, Safran M, Eisinger M, David G, Yayon A: Perlecan, basai lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell 1994, 79:1005-1013.
33. Reiland J, Rapraeger AC: Heparan sulfate proteoglycan and FGF receptor target basic FGF to different intracellular destinations. J Cell Sci 1993, 105:1085-1093.
34. Quarto N, Amalric F: Heparan sulfate proteoglycans as transducers of FGF-2 signalling. J Cell Sci 1994, 107:3201-3212.
35. Gleizes PE, Noaillac-Depeyre J, Amalric F, Gas N: Basic fibroblast growth factor (FGF-2) internalization through the heparan sulfate proteoglycans-mediated pathway: an ultrastructural approach. Eur J Cell Biol 1995, 66:47-59.
36. 125I-labeled LPL. At least 60% of LPL internalization by wild-type cells was found to proceed through an HSPG-dependent, LRP-independent pathway. In addition, the authors concluded that the heparan sulfate- and LRP-dependent pathways are independent of each other.
37. 2-macroglobulin. Surface-bound LpL-enriched lipoproteins colocalized with LpL. Internalization of LpL-enriched lipoproteins was comparatively slow, into small, widely distributed vesicles that gradually reached the lysosomes, whereas internalization via LRP or LDL receptors was rapid, and led to rapid delivery to central, lysosome-like vesicles.
38. Willnow TE, Goldstein JL, Orth K, Brown MS, Herz J: Low density lipoprotein receptor-related protein and gp330 bind similar ligands, including plasminogen activator-inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance. J Biol Chem 1992, 267:26172-26180.
39. Berryman DE, Bensadoun A: Heparan sulfate proteoglycans are primarily responsible for the maintenance of enzyme activity, binding, and degradation of lipoprotein lipase in Chinese hamster ovary cells. J Biol Chem 1995, 270:24525-24531.
40. Obunike JC, Edwards IJ, Rumsey SC, Curtiss LK, Wagner WD, Deckelbaum RJ, Goldberg IJ: Cellular differences in lipoprotein lipase-mediated uptake of low density lipoproteins. J Biol Chem 1994, 269:13129-13135.
41. Seo T, Wang HC, Feldman SR, St. Clair RW: Characterization of alpha 2-macroglobulin receptor low density lipoprotein receptor-related protein (alpha 2MR/LRP) in White Carneau pigeon peritoneal macrophages: its role in lipoprotein metabolism. Biochim Biophys Acta 1997, 1344:171-188.
42. Ziere GJ, Kruijt JK, Bijsterbosch MK, van Berkel TJ: Recognition of lactoferrin and aminopeptidase M-modified lactoferrin by the liver: involvement of proteoglycans and the remnant receptor. Biochem J 1996, 313:289-295.
43. Fuki IV, Kuhn KM, Lomazov IR, Rothman VL, Tuszynski GP, Iozzo RV, Swenson TL, Fisher EA, Williams KJ: The syndecan family of proteoglycans: novel receptors mediating internalization of atherogenic lipoproteins. J Clin Invest 1997 (in press). This study demonstrated that specific cell-surface HSPGs belonging to the syndecan family can directly mediate internalization and efficient delivery of ligands to lysosomes. Several key features of this pathway are distinct from coated-pit endocytosis.
44. Seo T, St. Clair RW: Heparan sulfate proteoglycans mediate internalization and degradation of beta-VLDL and promote cholesterol accumulation by pigeon macrophages. J Lipid Res 1997, 38:765-779.
45. Nykjaer A, Bengtsson-Olivecrona G, Lookene A, Moestrup SK, Petersen CM, Weber W, Beisiegel U, Gliemann J: The alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein binds lipoprotein lipase and beta-migrating very low density lipoprotein associated with the lipase. J Biol Chem 1993, 268:15048-15055.
46. Willnow TE, Sheng Z, Ishibashi S, Herz J: Inhibition of hepatic chylomicron remnant uptake by gene transfer of a receptor antagonist. Science 1994, 264:1471-1474.
47. Mokuno H, Brady S, Kotite L, Herz J, Havel RJ: Effect of the 39-kDa receptor-associated protein on the hepatic uptake and endocytosis of chylomicron remnants and low density lipoproteins in the rat. J Biol Chem 1994, 269:13238-13243.
48. Strickland DK, Ashcom JD, Williams S, Battey F, Behre E, McTigue K, Battey JF, Argraves WS: Primary structure of alpha 2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J Biol Chem 1991, 266:13364-13369.
49. Cardin AD, Weintraub HR: Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 1989, 9:21-32.
50. Ji Z-S, Mahley RW: 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 1994, 14:2025-2032.
51. Vassiliou G, Stanley KK: 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 1994, 269:15172-15178.
52. Kato M, Wang H, Bernfield M, Gallagher JT, Turnbull JE: Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains. J Biol Chem 1994, 269:18881-18890.
53. Sanderson RD, Turnbull JE, Gallagher JT, Lander AD: Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J Biol Chem 1994, 269:13100-13106.
54. Lyon M, Deakin JA, Gallagher JT: Liver heparan sulfate structure. A novel molecular design. J Biol Chem 1994, 269:11208-11215.
55. Williams KJ, Swenson TL, Brocia RW, Rothman VL, Tuszynski GP, Fisher EA: Involvement of the syndecan family of heparan sulfate proteoglycans (HSPGs) in cellular uptake of complexes of lipoprotein lipase (LpL) with lipoproteins [Abstract]. Circulation 1993, 88(suppl):1-365.
56. Fuki IV, Kuhn KM, Lomazov IR, Fisher EA, Williams KJ: The cytoplasmic and transmembrane domains of syndecan, a cell-surface binding site for lipoproteins, direct the internalization of bound ligands [Abstract]. Circulation 1995, 92(suppl I):3.
57. Fuki I, Kuhn K, Lomazov I, Rothman V, Tuszynski G, Iozzo R, Swenson T, Fisher E, Williams KJ: Perlecan and syndecan proteoglycans: two new classes of lipoprotein receptors [Abstract]. FASEB J 1996, 10:A1140.
58. Fuki IV, Iozzo RV, Williams KJ: Perlecan heparan sulfate proteoglycan (HSPG): a novel, distinct receptor for atherogenic lipoproteins [Abstract]. Circulation 1996 94(suppl I):698-699.
59. Davidson WS, Rodrigueza WV, Lund-Katz S, Johnson WJ, Rothblat GH, Phillips MC: Effects of acceptor particle size on the efflux of cellular free cholesterol. J Biol Chem 1995, 270:17106-17113.
60. Rodrigueza WV, Williams KJ, Rothblat GH, Phillips MC: Remodeling and shuttling: mechanisms for the synergistic effects between different acceptor particles in the mobilization of cellular cholesterol. Arterioscler Thromb Vasc Biol 1997, 17:383-393.
61. Williams KJ, Tabas I: The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol 1995, 15:551-561.
62. Itano N, Oguri K, Nagayasu Y, Kusano Y, Nakanishi H, David G: Phosphorylation of a membrane-intercalated proteoglycan, syndecan-2, expressed in a stroma-inducing clone from a mouse Lewis lung carcinoma. Biochem J 1996, 315:925-930.
63. Prasthofer T, Ek B, Ekman P, Owens R, Hook M, Johansson S: Protein kinase C phosphorylates two of the four known syndecan cytoplasmic domains in vitro. Biochem Mol Biol Int 1995, 36:793-802.
64. Reiland J, Ott VL, Lebakken CS, Yeaman C, McCarthy J, Rapraeger AC: Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of syndecan-1. Biochem J 1996, 319:39-47.
65. Carey DJ, Stahl RC, Tucker B, Bendt KA, Cizmeci-Smith G: Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp Cell Res 1994, 214:12-21
66. Carey DJ, Bendt KM, Stahl RC: The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain rescues. J Biol Chem 1996, 271:15253-15260. Using truncations and point mutations of the syndecan-1 core protein, the authors determined that the microfilament association depends on a specific region within the cytoplasmic tail and the detergent insolubility depends on the transmembrane domain.
67. Miettinen HM, Jalkanen M: The cytoplasmic domain of syndecan-1 is not required for association with Triton X-100-insoluble material. J Cell Sci 1994, 107:1571-1581.
68. Rapraeger A, Jalkanen M, Bernfield M: Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol 1986, 1032683-2596
69. Kato M, Saunders S, Nguyen H, Bernfield M: Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol Biol Cell 1995, 6:559-576.
70. Fransson LA, Carlstedt I, Coster L, Malmstrom A: Proteoheparan sulfate from human skin fibroblasts. Evidence for self-interaction via the heparan sulfate side chains. J Biol Chem 1983, 258:14342-14345.
71. Asundi VK, Carey DJ: Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J Biol Chem 1995, 270:26404-26410.
72. Sun X, Kaesberg PR, Choay J, Harenberg J, Ershler WB, Mosher DF: Effects of sized heparin oligosaccharide on the interactions of Chinese hamster ovary cell with thrombospondin. Semin Thromb Hemost 1992, 18:243-251.
73. Fuki IV, Bagasra O, Williams KJ: Syndecan heparan sulfate proteoglycans internalize lipoproteins via a pathway involving caveolae [Abstract]. Atherosclerosis (in press).
74. Sargiacomo M, Sudol M, Tang Z, Lisanti MP: Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 1993, 122:789-807.
75. Gleizes PE, Noaillacdepeyre J, Dupont MA, Gas N: Basic fibroblast growth factor (FGF-2) is addressed to caveolae after binding to the plasma membrane of BHK cells. Eur J Cell Biol 1996, 71:144-153.
76. Martinho RG, Castel S, Ureǹa J, Fernández-Borja M, Makiya R, Olivecrona G, Reina M, Alonsa A, Vilaró S: Ligand binding to heparan sulfate proteoglycans induces their aggregation and distribution along actin cytoskeleton. Mol Biol Cell 1996, 7:1771-1788.
77. Iozzo RV, Cohen IR, Grassel S, Murdoch AD: The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem J 1994, 302:625-639.
78. Bork P, Patthy L: The SEA module: a new extracellular domain associated with O-glycosylation. Protein Sci 1995, 4:1421-1425.
79. Hayashi K, Madri JA, Yurchenco PD: Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins: an adhesion modulated by glycosaminoglycan. J Cell Biol 1992, 119:945-959.
80. Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA: The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J Biol Chem 1996, 271:10079-10086.
81. Ishibashi S, Herz J, Maeda N, Goldstein JL, Brown MS: The two-receptor model of lipoprotein clearance: tests of the hypothesis in 'knockout' mice lacking the low density lipoprotein receptor, apolipoprotein E, or both proteins. Proc Natl Acad Sci U S A 1994, 91:4431-4435.
82. Mortimer BC, Beveridge DJ, Martins IJ, Redgrave TG: Intracellular localization and metabolism of chylomicron remnants in the livers of low density lipoprotein receptor-deficient mice and apoE-deficient mice. Evidence for slow metabolism via an alternative apoE-dependent pathway. J Biol Chem 1995, 270:28767-28776.
83. Goldstein JL, Brown MS: Atherosclerosis: the low-density lipoprotein receptor hypothesis. Metabolism 1977, 26:1257-1275.
84. Kesaniemi YA, Witztum JL, Steinbrecher UP: Receptor-mediated catabolism of low density lipoprotein in man. Quantitation using glucosylated low density lipoprotein. J Clin Invest 1983, 71:950-959.
85. Vilella E, Joven J, Fernández M, Vilaró S, Brunzell JD, Olivecrona T, Bengtsson-Olivecrona G: Lipoprotein lipase in human plasma is mainly inactive and associated with cholesterol-rich lipoproteins. J Lipid Res 1993, 34:1555-1564.
86. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trestad RL, Bernfield M: Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissue. A light and electron microscopic study. J Histochem Cytochem 1987, 35:1079-1088.
87. Roskams T, Moshage H, De Vos R, Guido D, Yap P, Desmet V: Heparan sulfate proteoglycan expression in normal human liver. Hepatology 1995, 21:950-958.
88. Gallai M, Sebestyen A, Nagy P, Kovalszky I, Onody T, Thorgeirsson SS: Proteoglycan gene expression in rat liver after partial hepatectomy. Biochem Biophys Res Commun 1996, 228:690-694.
89. Kojima T, Shworak NW, Rosenberg RD: Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J Biol Chem 1992, 267:4870-4877.
90. Kainulainen V, Nelimarkka L, Jarvelainen H, Laato M, Jalkanen M, Elenius K: Suppression of syndecan-1 expression in endothelial cells by tumor necrosis factor-alpha. J Biol Chem 1996, 271:18759-18766.
91. Yeaman C, Rapraeger AC: Membrane-anchored proteoglycans of mouse macrophages: P388D1 cells express a syndecan-4-like heparan sulfate proteoglycan and a distinct chondroitin sulfate form. J Cell Physiol 1993, 157:413-425.
92. Weiner OH, Zoremba M, Gressner AM: Gene expression of syndecans and betaglycan in isolated rat liver cells. Cell Tissue Res 1996, 285:11-16.
93. Yeaman C, Rapraeger AC: Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol 1993, 122:941-950.
94. Kovalszky H, Gallai M, Armbrust T, Ramadori G: Syndecan-1 gene expression in isolated rat liver cells (hepatocytes, Kupffer cells, endothelial and lto cells). Biochem Biophys Res Commun 1994, 204:944-949.
95. Cizmeci-Smith G, Stahl RC, Showalter LJ, Carey DJ: Differential expression of transmembrane proteoglycans in vascular smooth muscle cells. J Biol Chem 1993, 268:18740-18747.
96. Cizmeci-Smith G, Langan E, Youkey J, Showalter LJ, Carey DJ: Syndecan-4 is a primary-response gene induced by basic fibroblast growth factor and arterial injury in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1997, 17:172-180.
97. Vihinen T, Maatta A, Jaakkola P, Auvinen P, Jalkanen M: Functional characterization of mouse syndecan-1 promoter. J Biol Chem 1996, 271:12532-12541.
98. Cook DM, Hinkes MT, Bernfield M, Rauscher FJ: Transcriptional activation of the syndecan-1 promoter by the Wilms' tumor protein WT1. Oncogene 1996, 13:1789-1799.
99. Iozzo RV, Pillarisetti J, Sharma B, Murdoch AD, Danielson KG, Uitto J, Mauviel A: Structural and functional characterization of the human perlecan gene promoter - transcriptional activation by transforming growth factor-beta via a nuclear factor 1-binding element. J Biol Chem 1997, 272:5219-5228.
100. Ji ZS, Fazio S, Mahley RW: Variable heparan sulfate proteoglycan binding of apolipoprotein E variants may modulate the expression of type III hyperlipoproteinemia. J Biol Chem 1994, 269:13421-13428.
101. Mann WA, Meyer N, Weber W, Meyer S, Greten H, Beisiegel U: Apolipoprotein E isoforms and rare mutations: parallel reduction in binding to cells and to heparin reflects severity of associated type III hyperlipoproteinemia. J Lipid Res 1995, 36:517-525.
102. Ji ZS, Sanan DA, Mahley RW: Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: in vivo role of heparan sulfate proteoglycans. J Lipid Res 1995, 36:583-592.
103. Windler E, Greeve J, Robenek H, Rinninger F, Greten H, Jäckle S: Differences in the mechanisms of uptake and endocytosis of small and large chylomicron remnants by rat liver. Hepatology 1996, 24:344-351. The authors found that small fasting chylomicron remnants were cleared by hepatic LDL receptors, whereas uptake of large post-prandial chylomicron remnants proceeded through an LDL receptor-independent pathway that was significantly impaired by infusion of heparin or heparinase. Large remnants were cleared from plasma much faster than the small particles, but were more slowly internalized by hepatocytes. Upon internalization, both types of particles appeared in the compartment of uncoupling of receptors and ligands and in multivesicular bodies.
104. Herz J, Qiu SQ, Oesterle A, DeSilva HV, Shafi S, Havel RJ: Initial hepatic removal of chylomicron remnants is unaffected but endocytosis is delayed in mice lacking the low density lipoprotein receptor. Proc Natl Acad Sci U S A 1995, 92:4611-4615.
105. Ishibashi S, Perrey S, Chen Z, Osuga J, Shimada M, Ohashi K, Harada K, Yazaki Y, Yamada N: Role of the low density lipoprotein (LDL) receptor pathway in the metabolism of chylomicron remnants. A quantitative study in knockout mice lacking the LDL receptor, apolipoprotein E, or both. J Biol Chem 1996, 271: 22422-22427.
106. de Faria E, Fong LG, Komaromy M, Cooper D: Relative roles of the LDL receptor, the LDL receptor-like protein, and hepatic lipase in chylomicron remnant removal by the liver. J Lipid Res 1996, 37:197-209.
107. Tabas I: The stimulation of the cholesterol esterification pathway by atherogenic lipoproteins in macrophages. Curr Opin Lipidol 1995, 6:260-268.
108. Fielding PE, Fielding CJ: Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae. Biochemistry 1996, 35:14932-14938.
109. Smart EJ, Ying YS, Donzell WC, Anderson RGW: A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 1996, 271:29427-29435.
110. Sinnis P, Willnow TE, Briones MRS, Herz J, Nussenzweig V: Remnant lipoproteins inhibit malaria sporozoite invasion of hepatocytes. J Exp Med 1996, 184:945-954.
111. Shakibaei M, Frevert U: Dual interaction of the malaria circumsporozoite protein with the low density lipoprotein receptor-related protein (LRP) and heparan sulfate proteoglycans. J Exp Med 1996, 184:1699-1711.
112. van Putten JP, Paul SM: Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J 1995, 14:2144-2154.
113. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA: Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
114. Snow AD, Kinsella MG, Parks E, Sekiguchi RT, Miller JD, Kimata K, Wight TN: Differential binding of vascular cell-derived proteoglycans (perlecan, biglycan, decorin, and versican) to the beta-amyloid protein of Alzheimer's disease. Arch Biochem Biophys 1995, 320:84-95.
115. Tumova S, Bame KJ: The interaction between basic fibroblast growth factor and heparan sulfate can prevent the in vitro degradation of the glycosaminoglycan by Chinese hamster ovary cell heparanases. J Biol Chem 1997, 272:9078-9085.
116. Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, Crowther RA: Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycan. Nature 1996, 383:550-553.