The syndecan family of proteoglycans: Novel receptors mediating internalization of atherogenic lipoproteins in vitro

Journal of Clinical Investigation

Volumn 100, Issue 6, 1997, Pages 1611-1622

  Fuki, Ilia V ^a   Kuhn, Kenneth M ^a,f   Lomazov, Igor R ^a   Rothman, Vicky L ^b   Tuszynski, George P ^b   Iozzo, Renato V ^c   Swenson, Theresa L ^d,g   Fisher, Edward A ^e   Williams, Kevin Jon ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f STANFORD UNIVERSITY   (United States)

^g Diagnescent Technologies Inc   (United States)

Author keywords

Atherosclerosis; Endocytosis; Heparan sulfate proteoglycans; Lipoprotein lipase; Receptor

Indexed keywords

LIPOPROTEIN; PROTEOGLYCAN; SYNDECAN;

ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; CELL MEMBRANE TRANSPORT; CHO CELL; CONTROLLED STUDY; ENDOCYTOSIS; INTERNALIZATION; LIPID TRANSPORT; LIPOPROTEIN METABOLISM; NONHUMAN; PRIORITY JOURNAL;

EID: 0030803636     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119685     Document Type: Article

References (117)

1. Williams, K.J., T.L. Swenson, R.W. Brocia, V.L. Rothman, G.P. Tuszynski, and E.A. Fisher. 1993. Involvement of the syndecan family of heparan sulfate proteoglycans (HSPGs) in cellular uptake of complexes of lipoprotein lipase (LpL) with lipoproteins. Circulation. 88:1-365. (Abstr.)
2. Fuki, I.V., K.M. Kuhn, I.R. Lomazov, E.A. Fisher, and K.J. Williams. 1995. The cytoplasmic and transmembrane domains of syndecan, a cell-surface binding site for lipoproteins, direct the internalization of bound ligands. Circulation. 92:1-3. (Abstr.)
3. Kita, T., J.L. Goldstein, M.S. Brown, Y. Watanabe, C.A. Hornick, and R.J. Havel. 1982. Hepatic uptake of chylomicron remnants in WHHL rabbits: a mechanism genetically distinct from the low density lipoprotein receptor. Proc. Natl Acad. Sci. USA. 79:3623-3627.
4. Rubinsztein, D.C., J.C. Cohen, G.M. Berger, D.R. van der Westhuyzen, G.A. Coetzee, and W. Gevers. 1990. Chylomicron remnant clearance from the plasma is normal in familial hypercholesterolemic homozygotes with defined receptor defects. J. Clin. Invest. 86:1306-1312.
5. Ishibashi, S., J. Herz, N. Maeda, J.L. Goldstein, and M.S. Brown. 1994. 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. USA. 91:4431-4435.
6. Beisiegel, U., A. Krapp, W. Weber, and G. Olivecrona. 1994. The role of alpha 2M receptor/LRP in chylomicron remnant metabolism. Ann. N.Y. Acad. Sci. 737:53-69.
7. Williams, K.J., and I. Tabas. 1995. The response-to-retention hypothesis of early atherogenesis. Arterioscler. Thromb. Vasc. Biol. 15:551-561.
8. Goldstein, J.L., and M.S. Brown. 1977. Atherosclerosis: the low-density lipoprotein receptor hypothesis. Metabolism. 26:1257-1275.
9. Kesaniemi, Y.A., J.L. Witztum, and U.P. Steinbrecher. 1983. Receptor-mediated catabolism of low density lipoprotein in man. Quantitation using glucosylated low density lipoprotein. J. Clin. Invest. 71:950-959.
10. Williams, K.J., G.M. Fless, K.A. Petrie, M.L. Snyder, R.W. Brocia, and T.L. Swenson. 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.
11. Ji, Z.S., W.J. Brecht, R.D. Miranda, M.M. Hussain, T.L. Innerarity, and R.W. Mahley. 1993. Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells. J. Biol. Chem. 268:10160-10167.
12. Camejo, G., E. Hurt-Camejo, U. Olsson, and G. Bondjers. 1993. Proteoglycans and lipoproteins in atherosclerosis. Curr. Opin. Lipidol. 4:385-391.
13. Tabas, I., Y. Li, R.W. Brocia, S.W. Xu, T.L. Swenson, and K.J. Williams. 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.
14. Robinson, D.S. 1987. Lipoprotein lipase - past, present, and future. In Lipoprotein Lipase. J. Borensztajn, editor. Evener, Chicago. 1-13.
15. Mahley, R.W., and T.L. Innerarity. 1977. Interaction of canine and swine lipoproteins with the low density lipoprotein receptor of fibroblasts as correlated with heparin/manganese precipitability. J. Biol. Chem. 252:3980-3986.
16. Oswald, B., F. Shelburne, B. Landis, A. Linker, and S. Quarfordt. 1986. The relevance of glycosaminoglycan sulfates to apo E induced lipid uptake by hepatocyte monolayers. Biochem. Biophys. Res. Commun. 141:158-164.
17. LaRosa, J.C., R.I. Levy, H.G. Windmueller, and D.S. Fredrickson. 1972. Comparison of the triglyceride lipase of liver, adipose tissue, and postheparin plasma. J. Lipid Res. 13:356-363.
18. Davis, R.C., H. Wong, J. Nikazy, K. Wang, O. Han, and M.C. Schotz. 1992. Chimeras of hepatic lipase and lipoprotein lipase. Domain localization of enzyme-specific properties. J. Biol. Chem. 267:21499-21504.
19. Robinson, D.S. 1963. The clearing factor lipase and its action in the transport of fatty acids between the blood and the tissues. Adv. Lipid Res. 1: 133-182.
20. Felts, J.M., H. Itakura, and R.T. Crane. 1975. The mechanims of assimilation of consitutents of chylomicrons, very low density lipoproteins and remnants - a new theory. Biochem Biophys. Res. Commun. 66:1467-1475.
21. Oswald, B., and S. Quarfordt. 1987. Effect of apoE on triglyceride emulsion interaction with hepatocyte and hepatoma G2 cells. J. Lipid Res. 28: 798-809.
22. Williams, K.J., G.M. Fless, K. Petrie, M.L. Snyder, R.W. Brocia, and T.L. Swenson. 1991. Lipoprotein lipase enhances cellular catabolism of lipoprotein(a). Circulation. 84:11-566. (Abstr.)
23. Vilaró, S., I. Ramírez, G. Bengtsson-Olivecrona, T. Olivecrona, and M. Llobera. 1988. Lipoprotein lipase in liver. Release by heparin and immunocytochemical localization. Biochim. Biophys. Acta. 959:106-117.
24. Corey, J.E., and D.B. Zilversmit. 1977. Effect of cholesterol feeding on arterial lipolytic activity in the rabbit. Atherosclerosis. 27:201-212.
25. Ylä-Herttuala, S., B.A. Lipton, M.E. Rosenfeld, I.J. Goldberg, D. Steinberg, and J.L. Witztum. 1991. Macrophages and smooth muscle cells express lipoprotein lipase in human and rabbit atherosclerotic lesions. Proc. Natl. Acad. Sci. USA. 88:10143-10147.
26. Rumsey, S.C., J.C. Obunike, Y. Arad, R.J. Deckelbaum, and I.J. Goldberg. 1992. Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J. Clin. Invest. 90:1504-1512.
27. Eisenberg, S., E. Sehayek, T. Olivecrona, and I. Vlodavsky. 1992. Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J. Clin. Invest. 90:2013-2021.
28. Mulder, M., P. Lombardi, H. Jansen, T.J.C. van Berkel, R.R. Frants, and L.M. Havekes. 1992. Heparan sulphate proteoglycans are involved in the lipoprotein lipase-mediated enhancement of the cellular binding of very low density and low density lipoproteins. Biochem. Biophys. Res. Commun. 185:582-587.
29. Ji, Z.S., S. Fazio, and R.W. Mahley. 1994. Variable heparan sulfate proteoglycan binding of apolipoprotein E variants may modulate the expression of type III hyperlipoproteinemia. J. Biol. Chem. 269:13421-13428.
30. Mann, W.A., N. Meyer, W. Weber, S. Meyer, H. Greten, and U. Beisiegel. 1995. 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. 36:517-525.
31. Ji, Z.S., S.J. Lauer, S. Fazio, A. Bensadoun, J.M. Taylor, and R.W. Mahley. 1994. Enhanced binding and uptake of remnant lipoproteins by hepatic lipase-secreting hepatoma cells in culture. J. Biol. Chem. 269:13429-13436.
32. Shafi, S., S.E. Brady, A. Bensadoun, and R.J. Havel. 1994. Role of hepatic lipase in the uptake and processing of chylomicron remnants in rat liver. J. Lipid Res. 35:709-720.
33. de Faria, E., L.G. Fong, M. Komaromy, and A.D. Cooper. 1996. Relative roles of the LDL receptor, the LDL receptor-like protein, and hepatic lipase in chylomicron remnant removal by the liver. J. Lipid Res. 37:197-209.
34. Mahley, R.W., Z.S. Ji, W.J. Brecht, R.D. Miranda, and D. He. 1994. Role of heparan sulfate proteoglycans and the LDL receptor-related protein in remnant lipoprotein metabolism. Ann. N.Y. Acad. Sci. 737:39-52.
35. Beisiegel, U. 1995. Receptors for triglyceride-rich lipoproteins and their role in lipoprotein metabolism. Curr. Opin. Lipidol. 6:117-122.
36. Willnow, T.E., J.L. Goldstein, K. Orth, M.S. Brown, and J. Herz. 1992. 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. 267:26172-26180.
37. Beisiegel, U., W. Weber, G. Ihrke, J. Herz, and K.K., Stanley. 1989. The LDL-receplor-related protein, LRP, is an apolipoprotein E-binding protein. Nature (Lond.). 341:162-164.
38. Nykjaer, A., G. Bengtsson-Olivecrona, A. Lookene, S.K. Moestrup, CM. Petersen, W. Weber, U. Beisiegel, and J. Gliemann. 1993. 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. 268:15048-15055.
39. 2-macroglobulin receptor in vitro. A process facilitated by cell-surface proteoglycans. J. Biol. Chem. 268:14168-14175.
40. Mokuno, H., S. Brady, L. Kotite, J. Herz, and R.J. Havel. 1994. 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. 269:13238-13243.
41. Willnow, T.E., Z. Sheng, S. Ishibashi, and J. Herz. 1994. Inhibition of hepatic chylomicron remnant uptake by gene transfer of a receptor antagonist. Science (Wash. DC). 264:1471-1474.
42. Hussain, M.M., F.R. Maxfield, J. Mas-Oliva, I. Tabas, Z.S. Ji, T.L. Innerarity, and R.W. Mahley. 1991. Clearance of chylomicron remnants by the low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266:13936-13940.
43. Choi, S.Y., and A.D. Cooper. 1993. A comparison of the roles of the low density lipoprotein (LDL) receptor and the LDL receptor-related protein/alpha 2-macroglobulin receptor in chylomicron remnant removal in the mouse in vivo. J. Biol. Chem. 268:15804-15811.
44. 2-macroglobulin in adipocytes. J. Biol. Chem. 268:974-981.
45. Chappell, D.A., I. Inoue, G.L. Fry, M.W. Pladet, S.L. Bowen, P.H. Iverius, J.M. Lalouel, and D.K. Strickland. 1994. Cellular catabolism of normal very low density lipoproteins via the low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor is induced by the C-terminal domain of lipoprotein lipase. J. Biol. Chem. 269:18001-18006.
46. Willnow, T.E., S.A. Armstrong, R.E. Hammer, and J. Herz. 1995. Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo. Proc. Natl. Acad. Sci. USA. 92: 4537-4541.
47. Sehayek, E., X.X. Wang, I. Vlodavsky, R. Avner, H. Levkovitz, T. Olivecrona, G. Olivecrona, T.E. Willnow, J. Herz, and S. Eisenberg. 1996. Heparan sulfate-dependent and low density lipoprotein receptor-related protein-dependent catabolic pathways for lipoprotein lipase in mouse embryonic fihroblasts. Isr. J. Med. Sci. 32:449-454.
48. Strickland, D.K., J.D. Ashcom, S. Williams, F. Battey, E. Behre, K. McTigue, J.F. Battey, and W.S. Argraves. 1991. Primary structure of alpha 2-macroglohulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266:13364-13369.
49. Ji, Z.-S., and R.W. Mahley. 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.
50. Vassiliou, G., and K.K. Stanley. 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. 269:15172-15178.
51. Obunike, J.C., I.J. Edwards, S.C. Rumsey, L.K. Curtiss, W.D. Wagner, R.J. Deckelbaum, and I.J. Goldberg. 1994. Cellular differences in lipoprotein lipase-mediated uptake of low density lipoproteins. J. Biol. Chem. 269:13129-13135.
52. Seo, T., and R.W. St. Clair. 1995. Role of cell surface proteoglycans in βVLDL metabolism by pigeon macrophages. Circulation. 92:I-3. (Abstr.)
53. Mortimer, B.C., D.J. Beveridge, I.J. Martins, and T.G. Redgrave. 1995. Intracellular localization and metabolism of chylomicron remnants in the livers of low density lipoprotein receptor-deficient mice and apo E-deficient mice. Evidence for slow metabolism via an alternative apo E-dependent pathway. J. Biol. Chem. 270:28767-28776.
54. Ziere, G.J., J.K. Kruijt, M.K. Bijsterbosch, and T.J. van Berkel. 1996. Recognition of lactoferrin and aminopeptidase M-modified lactoferrin by the liver: involvement of proteoglycans and the remnant receptor. Biochem. J. 313: 289-295.
55. 2MR/LRP) in white Carneau pigeon peritoneal macrophages: its role in lipoprotein metabolism. Biochim. Biophys. Acta. 1344:171-188.
56. 2-macroglobulin in the rat. J. Lipid Res. 34:309-315.
57. Ji, Z.S., D.A. Sanan, and R.W. Mahley. 1995. Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: in vivo role of heparan sulfate proteoglycans. J. Lipid Res. 36:583-592.
58. Windler, E., J. Greeve, H. Robenek, F. Rinninger, H. Greten, and S. Jäckle. 1996. Differences in the mechanisms of uptake and endocytosis of small and large chylomicron remnants by rat liver. Hepatology. 24:344-351.
59. Reiland, J., and A.C. Rapraeger. 1993. Heparan sulfate proteoglycan and FGF receptor target basic FGF to different intracellular destinations. J. Cell Sci. 105:1085-1093.
60. Kounnas, M.Z., D.A. Chappell, H. Wong, W.S. Argraves, and D.K. Strickland. 1995. The cellular internalization and degradation of hepatic lipase is mediated by low density lipoprotein receptor-related protein and requires cell surface proteoglycans. J. Biol. Chem. 270:9307-9312.
61. Berryman, D.E., and A. Bensadoun. 1995. 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. 270:24525-24531.
62. Gleizes, P.E., J. Noaillac-Depeyre, F. Amalric, and N. Gas. 1995. Basic fibroblast growth factor (FGF-2) internalization through the heparan sulfate proteoglycans-mediated pathway: an ultrastructural approach. Eur. J. Cell Biol. 66:47-59.
63. Mali, M., P. Jaakkola, A.-M. Arvilommi, and M. Jalkanen. 1990. Sequence of human syndecan indicates a novel gene family of integral membrane proteoglycans. J. Biol. Chem. 265:6884-6889.
64. Bernfield, M., R. Kokenyesi, M. Kato, M.T. Hinkes, J. Spring, R.L. Gallo, and E.J. Lose. 1992. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8:365-393.
65. David, G. 1993. Integral membrane heparan sulfate proteoglycans. FASEB (Fed. Am. Soc. Exp. Biol.) J. 7:1023-1030.
66. Hayashi, K., M. Hayashi, M. Jalkanen, J.H. Firestone, R.L. Trestad, and M. Bernfield. 1987. Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissue. A light and electron microscopic study. J. Histochem. Cytochem. 35:1079-1088.
67. Roskams, T., H. Moshage, R. De Vos, D. Guido, P. Yap, and V. Desmel. 1995. Heparan sulfate proteoglycan expression in normal human liver. Hepatology. 21:950-958.
68. Kojima, T., N.W. Shworak, and R.D. Rosenberg. 1992. Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J. Biol. Chem. 267:4870-4877.
69. Cizmeci-Smkh, G., R.C. Stahl, L.J. Showalter, and D.J. Carey. 1993. Differential expression of transmembrane proteoglycans in vascular smooth muscle cells. J. Biol. Chem. 268:18740-18747.
70. Yeaman, C., and A.C. Rapraeger. 1993. Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J. Cell Biol. 122: 941-950.
71. Weiner, O.H., M. Zoremba, and A.M. Gressner. 1996. Gene expression of syndecans and betaglycan in isolated rat liver cells. Cell Tissue Res. 285:11-16.
72. Spring, J., S.E. Paine-Saunders, R.O. Hynes, and M. Bernfield. 1994. Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. Proc. Natl. Acad. Sci. USA. 91:3334-3338.
73. Socorro, L., C.C. Green, and R.L. Jackson. 1985. Preparation of a homogeneous and stable form of bovine milk lipoprotein lipase. Prep. Biochem. 15:133-143.
74. Williams, K.J., K.A. Petrie, R.W. Brocia, and T.L. Swenson. 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.
75. Tuszynski, G.P., S. Srivastava, H.I. Switalska, J.C. Holt, C.S. Cierniewski, and S. Niewiarowski. 1985. The interaction of human platelet thrombospondin with fibrinogen. Thrombospondin purification and specificity of interaction. J. Biol. Chem. 260:12240-12245.
76. Williams, S.E., J.D. Ashcom, W.S. Argraves, and D.K. Strickland. 1992. A novel mechanism for controlling the activity of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J. Biol. Chem. 267:9035-9040.
77. Goldstein, J.L., S.K. Basu, and M.S. Brown. 1983. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98: 241-260.
78. 13C NMR characterization of lysine residues in apolipoprotein B and their role in binding to the low density lipoprotein receptor. J. Biol. Chem. 263: 13831-13838.
79. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, New York. vols. 1-3.
80. Leppa, S., M. Mali, H.M. Miettinen, and M. Jalkanen. 1992. Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc. Natl. Acad. Sci. USA. 89:932-936.
81. Pierce, A., M. Lyon, I.N. Hampson, G.J. Cowling, and J.T. Gallagher. 1992. Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J. Biol. Chem. 267:3894-3900.
82. Kozak, M. 1981. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res. 9:5233-5262.
83. Allen, J.M., and B. Seed. 1989. Isolation and expression of functional high-affinity Fc receptor complementary DNAs. Science (Wash. DC). 243:378-381.
84. Asundi, V.K., and D.J. Carey. 1995. 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. 270:26404-26410.
85. Carey, D.J., R.C. Stahl, B. Tucker, K.A. Bendt, and G. Cizmeci-Smith. 1994. Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp. Cell Res. 214:12-21.
86. Akiyama, T., J. Ishida, S. Nakagawa, H. Ogawara, S. Watanabe, N. Itoh, M. Shibuya, and Y. Fukami. 1987. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262:5592-5595.
87. Lehrich, R.W., and J.N. Forrest, Jr. 1995. Tyrosine phosphorylation is a novel pathway for regulation of chloride secretion in shark rectal gland. Am. J. Physiol. 269:F594-F600.
88. Markwell, M.A.K., S.M. Haas, L.L. Bieber, and N.E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochim. 87:206-210.
89. Davis, W., P.T. Harrison, M.J. Hutchinson, and J.M. Allen. 1995. Two distinct regions of Fc gamma RI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO (Eur. Mol. Biol. Organ.) J. 14:432-441.
90. 2-macroglobulin receptor binds and mediates catabolism of bovine lipoprotein lipase. J. Biol. Chem. 267:25764-25767.
91. Glantz, S.A. 1992. Primer of Biostatistics. McGraw-Hill. Inc., New York. 32-109.
92. Sun, X., D.F. Mosher, and A. Rapraeger. 1989. Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J. Biol. Chem. 264:2885-2889.
93. Corless, C.L., A. Mendoza, T. Collins, and J. Lawler. 1992. Colocalization of thrombospondin and syndecan during murine development. Dev. Dyn. 193:346-358.
94. Sun, X., P.R. Kaesberg, J. Choay, J. Harenberg, W.B. Ershler, and D.F. Mosher. 1992. Effects of sized heparin oligosaccharide on the interactions of Chinese hamster ovary cell with thrombospondin. Semin. Thromb. Hemost. 18: 243-251.
95. Booth, W.J., P.A. Castaldi, and M.C. Berndt. 1985. Platelet thrombospondin haemagglutinin activity is due to aggregate formation. Thromb. Res. 39:29-42.
96. van de Winkel, J.G. and P.J. Capel. 1993. Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications. Immunol. Today. 14:215-221.
97. Kruskal, B.A., K. Sastry, A.B. Warner, C.E. Mathieu, and R.A. Ezekowitz. 1992. Phagocytic chimeric receptors require both transmembrane and cytoplasmic domains from the mannose receptor. J. Exp. Med. 176:1673-1680.
98. Tabas, I., J.N. Myers, T.L. Innerarity, X.X. Xu, K. Arnold, J. Boyles, and F.R. Maxfield. 1991. The influence of particle size and multiple apoprotein E-receptor interactions on the endocytic targeting of β-VLDL in mouse peritoneal macrophages. J. Cell Biol. 115:1547-1560.
99. Weigel, P.H., and J.A. Oka. 1982. Endocytosis and degradation mediated by the asialoglycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 257:1201-1207.
100. Brown, M.S., and J.L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science (Wash. DC). 232:34-47.
101. Warshawsky, L. and A.L. Schwartz. 1996. The 39-kDa protein regulates LRP activity in cultured endothelial and smooth muscle cells. Eur. J. Cell Biol. 69:156-165.
102. Rapraeger, A., M. Jalkanen, and M. Bernfield. 1986. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J. Cell Biol. 103:2683-2696.
103. Reiland, J., V.L. Ott, C.S. Lebakken, C. Yeaman, J. McCarthy, and A.C. Rapraeger. 1996. Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of syndecan-1. Biochem. J. 319:39-47.
104. Luton, F., M. Buferne, J. Davoust, A.M. Schmitt-Verhulst, and C. Boyer. 1994. Evidence for protein tyrosine kinase involvement in ligand-induced TCR/CD3 internalization and surface redistribution. J. Immunol. 153:63-72.
105. Kokenyesi, R., and M. Bernfield. 1994. Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1. J. Biol. Chem. 269:12304-12309.
106. Lyon, M., J.A. Deakin, and J.T. Gallagher. 1994. Liver heparan sulfate structure. A novel molecular design. J. Biol. Chem. 269:11208-11215.
107. Fransson, L.-Å., I. Carlstedt, L. Coster, and A. Malmström. 1983. Proteoheparan sulfate from human skin fibroblasts. Evidence for self-interaction via the heparan sulfate side chains. J. Biol. Chem. 258:14342-14345.
108. Nader, H.B., T.M. Ferreira, L. Toma, S.F. Chavante, C.P. Dietrich, B. Casu, and G. Torri. 1988. Maintenance of heparan sulfate structure throughout evolution: chemical and enzymic degradation, and 13C-n.m.r.-spectral evidence. Carbohydr. Res. 184:292-300.
109. Fuki, I., K. Kuhn, I. Lomazov, V. Rothman, G. Tuszynski, R. Iozzo, T. Swenson, E. Fisher, and K.J. Williams. 1996. Perlecan and syndecan proteoglycans: two new classes of lipoprotein receptors. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:A1140. (Abstr.)
110. Hayashi, K., J.A. Madri, and P.D. Yurchenco. 1992. 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. 119:945-959.
111. Herz, J., S.Q. Qiu, A. Oesterle, H.V. DeSilva, S. Shafi, and R.J. Havel. 1995. Initial hepatic removal of chylomicron remnants is unaffected but endocytosis is delayed in mice lacking the low density lipoprotein receptor. Proc. Natl. Acad. Sci. USA. 92:4611-1615.
112. Rapraeger, A.C., A. Krufka, and B.B. Olwin. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science (Wash. DC). 252:1705-1708.
113. Yayon, A., M. Klagsbrun, J.D. Esko, P. Leder, and D.M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64:841-848.
114. 2-macroglobulin receptor mediates the cellular internalization and degradation of thrombospondin. A process facilitated by cell-surface proteoglycans. J. Biol. Chem. 270:9543-9549.
115. Deckert, M., M. Ticchioni, and A. Bernard. 1996. Endocytosis of GPI-anchored proteins in human lymphocytes: role of glycolipid-based domains, actin cytoskeleton, and protein kinases. J. Cell Biol. 133:791-799.
116. Parton, R.G., B. Joggerst, and K. Simons. 1994. Regulated internalization of caveolae. J. Cell Biol. 127:1199-1215.
117. Williams, K.J., and I.V. Fuki. 1997. Cell-surface heparan sulfate proteoglycans: dynamic molecules mediating ligand catabolism. Curr. Opin. Lipidol. 8:252-261.