Intracellular processing of endocytosed triglyceride-rich lipoproteins comprises both recycling and degradation

Journal of Cell Science

Volumn 112, Issue 3, 1999, Pages 349-359

  Heeren, Jörg ^a   Weber, Wilfried ^a   Beisiegel, Ulrike ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Apoprotein E; Intracellular processing; Lipoprotein lipase; Recycling; Triglyceride rich lipoprotein

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN C; APOLIPOPROTEIN E; LIPOPROTEIN; LIPOPROTEIN LIPASE; LOW DENSITY LIPOPROTEIN; TRANSFERRIN; TRIACYLGLYCEROL;

ARTICLE; ENDOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING;

APOPROTEINS; CELL LINE; ELECTROPHORESIS, GEL, PULSED-FIELD; ENDOCYTOSIS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; KINETICS; LIPOPROTEIN LIPASE; LIPOPROTEINS; LIPOPROTEINS, LDL; MODELS, BIOLOGICAL; TRIGLYCERIDES;

EID: 0033037582     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Aulinskas, T. H., van der Westhuyzen, D. R., Bierman, E. L., Gevers, W. and Coetzee, G. A. (1981). Retro-endocytosis of low density lipoprotein by cultured bovine aortic smooth muscle cells. Biochim. Biophys. Acta 664, 255-265.
2. Aulinskas, T. H., Oram, J. F., Bierman, E. L., Coetzee, G. A., Gevers, W. and van der Westhuyzen, D. R. (1985). Retro-endocytosis of low density lipoprotein by cultured human skin fibroblasts. Arteriosclerosis 5, 45-54.
3. Barter, P. (1993). High-density lipoproteins and reverse cholesterol transport. Curr. Opin. Lipidol. 211-217.
4. Beisiegel, U. (1992) Apolipoproteins as ligands tor lipoprotein receptors. In Structure and Function of Apolipoproteins (ed. M. Rosseneu), pp. 269-294. CRC Press, Boca Raton, USA.
5. Beisiegel, U., Weber, W., Ihrke, G., Herz, J. and Stanley, K. K. (1989). The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341, 162-164.
6. Beisiegel, U., Weber, W. and Bengtsson-Olivecrona, G. (1991). Lipoprotein lipase enhances the binding of chylomicrons to low density lipoprotein receptor-related protein. Proc. Nat. Acad. Sci. USA 88, 8342-8346.
7. Beisiegel, U. (1995). Receptors for triglyceride-rich lipoproteins and their role in lipoprotein metabolism. Curr. Opin. Lipidol. 6, 117-122.
8. Bradley, W. A. and Gianturco, S. H. (1986). ApoE is necessary and sufficient for the binding of large triglyceride-rich lipoproteins to the LDL receptor; apoB is unnecessary. J. Lipid Res. 27, 40-48.
9. Brown, M. S., Anderson, R. G. and Goldstein, J. L. (1983). Recycling receptors: the round-trip itinerary of migrant membrane proteins. Cell 32, 663-667.
10. Brunzell, J. D. (1989) Familial lipoprotein lipase deficiency and other causes of the Chylomicronemia Syndrome. In The Metabolic Basis of Inherited Disease (ed. C. R. Scriver, A. L. Beaudet, W. S. Sly and D. Valle), pp. 1165-1180. McGraw-Hill Information Services Company, USA.
11. Carlsson, S. R., Roth, J., Piller, F. and Fukuda, M. (1988). Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan. J. Biol. Chem. 263, 18911-18919.
12. 125I-epidermal growth factor and ferritin-low density lipoprotein in coated pits: a quantitative electron microscopic study in normal and mutant human fibroblasts. J. Cell Biol. 95, 73-77.
13. 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/alpha 2-macroglobulin receptor binds and mediates catabolism of bovine milk lipoprotein lipase. J. Biol. Chem. 267, 25764-25767.
14. Ciechanover, A., Schwartz, A. L., Dautry-Varsat, A. and Lodish, H. F. (1983). Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J. Biol. Chem. 258, 9681-9689.
15. Cooper, A. D. (1998). Hepatic uptake of chylomicron remnants. J. Lipid Res. 38, 2173-2192.
16. Dautry-Varsat, A., Ciechanover, A. and Lodish, H. F. (1983). pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Nat. Acad. Sci. USA 80, 2258-2262.
17. Davis, C. G., Goldstein, J. L., Suedhof, T. C., Anderson, R. G., Russell, D. W. and Brown, M. S. (1987). Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature 326, 760-765.
18. Felts, J. M., Itakura, H. and Crane, R. T. (1975). The mechanism of assimilation of constituents of chylomicrons, very low density lipoproteins and remnants - a new theory. Biochem. Biophys. Res. Commun. 66, 1467-1475.
19. Forte, T. M., McCall, M. R., Knowles, B. B. and Shore, V. G. (1989). Isolation and characterization of lipoproteins produced by human hepatoma-derived cell lines other than HepG2. J. Lipid Res. 30, 817-829.
20. Fraker, P. J. and Speck, J. C. J. (1978). Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a, 6a-diphrenylglycoluril. Biochem. Biophys. Res. Commun. 80, 849-857.
21. Futter, C. E., Pearse, A., Hewlett, L. J. and Hopkins, C. R. (1996). Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132, 1011-1023.
22. Ghosh, R. N., Gelman, D. L. and Maxfield, F. R. (1994). Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy. J. Cell Sci. 107, 2177-2189.
23. Goldberg, I. J., Kandel, J. J., Blum, C. B. and Ginsberg, H. N. (1986). Association of plasma lipoproteins with postheparin lipase activities. J. Clin. Invest. 78, 1523-1528.
24. Goldstein, J. L. and Brown, M. S. (1974). Binding and degradation of low density lipoproteins by cultured human fibroblasts. Comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J. Biol. Chem. 249, 5153-5162.
25. 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.
26. Goldstein, J. L., Brown, M. S., Anderson, R. G., Russell, D. W. and Schneider, W. J. (1985). Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell 1, 1-39.
27. Griffin, B. A. and Packard, C. J. (1994). Metabolism of VLDL and LDL subclasses. Curr. Opin. Lipidol. 5, 200-206.
28. Havel, R. J. (1984). The formation of LDL: mechanisms and regulation. J. Lipid Res. 25, 1570-1576.
29. Havel, R. J. (1995). Chylomicron remnants: hepatic receptors and metabolism. Curr. Opin. Lipidol. 6, 312-316.
30. Hui, D. Y., Innerarity, T. L., Milne, R. W., Marcel, V. L. and Mahley, R. W. (1984). Binding of chylomicron remnants and beta-very low density lipoproteins to hepatic and extrahepatic lipoprotein receptors. A process independent of apolipoprotein B48. J. Biol. Chem. 259, 15060-15068.
31. Jensen, T. G., Roses, A. D. and Jorgensen, A. L. (1994). Apolipoprotein E uptake and degradation via chloroquine sensitive pathway in cultivated monkey cells overexpressing low density lipoprotein receptor. Neurosci. Lett. 180, 193-196.
32. Jones, A. L., Hradek, G. T., Hornick, C., Renaud, G., Windler, E. E. and Havel, R. J. (1984). Uptake and processing of remnants of chylomicrons and very low density lipoproteins by rat liver. J. Lipid Res. 25, 1151-1158.
33. Kambouris, A. M., Roach, P. D., Calvert, G. D. and Nestel, P. J. (1990). Retroendocytosis of high density lipoproteins by the human hepatoma cell line, HepG2. Arteriosclerosis 10, 582-590.
34. Klausner, R. D., Ashwell, G., van Renswoude, J., Harford, J. B. and Bridges, K. R. (1983). Binding of apotransferrin to K562 cells: explanation of the transferrin cycle. Proc. Nat. Acad. Sci. USA 80, 2263-2266.
35. Kowal, R. C., Herz, J., Goldstein, J. L., Esser, V. and Brown, M. S. (1989). Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc. Nat. Acad. Sci. USA 86, 5810-5814.
36. Liu, M. S., Ma, Y., Hayden, M. and Brunzell, J. D. (1992). Mapping of the epitope on lipoprotein lipase recognized by a monoclonal antibody (5D2) which inhibits lipase activity. Biochim. Biophys. Acta 110-115.
37. Lombardi, P., Mulder, M., van der Boom, H., Frants, R. R. and Havekes, L. M. (1993). Inefficient degradation of triglyceride-rich lipoprotein by HepG2 cells is due to a retarded transport to the lysosomal compartment. J. Biol. Chem. 268, 26113-26119.
38. Lookene, A., Skottova, N. and Olivecrona, G. (1994). Interactions of lipoprotein lipase with the active-site inhibitor tetrahydrolipstatin (Orlistat). Eur. J. Biochem. 222, 395-403.
39. Mahley, R. W. and Hussain, M. M. (1991). Chylomicron and chylomicron remnant catabolism. Curr. Opin. Lipidol. 170-176.
40. Mann, W. A., Meyer, N., Weber, W., Rinninger, F., Greten, H. and Beisiegel, U. (1995). Apolipoprotein E and lipoprotein lipase co-ordinately enhance binding and uptake of chylomicrons by human hepatocytes. Eur. J. Clin. Invest. 25, 880-882.
41. Marsh, E. W., Leopold, P. L., Jones, N. L. and Maxfield, F. R. (1995). Oligomerized transferrin receptors are selectively retained by a lumenal sorting signal in a long-lived endocytic recycling compartment. J. Cell Biol. 129, 1509-1522.
42. Mayor, S., Presley, J. F. and Maxfield, F. R. (1993). Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121, 1257-1269.
43. McFarlane, A. S. (1958). Efficient trace labeling of proteins with iodine. Nature 57.
44. Mortimer, B. C., Beveridge, D. J., Martins, I. J. and Redgrave, T. G. (1995). 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. 270, 28767-28776.
45. Myers, J. N., Tabas, I., Jones, N. L. and Maxfield, F. R. (1993). Beta-very low density lipoprotein is sequestered in surface-connected tubules in mouse peritoneal macrophages. J. Cell Biol. 123, 396-402.
46. Nykjaer, A., Bengtsson-Olivecrona, G., Lookene, A., Moestrup, S. K., Petersen, C. M., Weber, W., Beisiegel, U. and Gliemann, J. (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.
47. Olivecrona, T. and Bengtsson-Olivecrona, G. (1993). Lipoprotein lipase and hepatic lipase. Curr. Opin. Lipidol. 190-196.
48. Pastan, I. H. and Willingham, M. C. (1981). Journey to the center of the cell: role of the receptosome. Science 214, 504-509.
49. Pitas, R. E., Innerarity, T. L., Weinstein, J. N. and Mahley, R. W. (1981). Acetoacetylated lipoproteins used to distinguish fibroblasls from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1, 177-185.
50. 125l-labeled lipoproteins by skin fibroblasts, smooth muscle cells, and peritoneal macrophages in culture. Am. J. Pathol. 121, 200-211.
51. Skerka, C., Hellwage, J., Weber, W., Tilkorn, A., Buck, F., Marti, T., Kampen, E., Beisiegel, U. and Zipfel, P. F. (1997). The human factor H-related protein 4 (FHR-4). A novel short consensus repeat-containing protein is associated with human triglyceride-rich lipoproteins. J. Biol. Chem. 272, 5627-5634.
52. Stoorvogel, W., Geuze, H. J., Griffith, J. M. and Strous, G. J. (1988). The pathways of endocylosed transferrin and secretory protein are connected in the trans-Golgi reticulum. J. Biol. Chem. 106, 1821-1829.
53. Stoorvogel, W., Geuze, H. J. and Strous, G. J. (1987). Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J. Biol. Chem. 104, 1261-1268.
54. Stoorvogel, W., Strous, G. J., Geuze, H. J., Oorschot, V. and Schwartz, A. L. (1991). Late endosomes derive from early endosomes by maturation. Cell 65, 417-427.
55. Tabas, I., Lim, S., Xu, X. X. and Maxfield, F. R. (1990). Endocytosed beta-VLDL and LDL are delivered to different intracellular vesicles in mouse peritoneal macrophages. J. Cell Biol. 111, 929-940.
56. Tabas, I., Myers, J. N., Innerarity, T. L., Xu, X. X., Arnold, K., Boyles, J. and Maxfield, F. R. (1991). The influence of particle size and multiple apoprotein E-receptor interactions on the endocytic targeting of beta-VLDL in mouse peritoneal macrophages. J. Cell Biol. 115, 1547-1560.
57. Wileman, T., Harding, C. and Stahl, P. (1985). Receptor-mediated endocytosis. Biochem. J. 232, 1-14.
58. Willnow, T. E., Sheng, Z., Ishibashi, S. and Herz, J. (1994). Inhibition of hepatic chylomicron remnant uptake by gene transfer of a receptor antagonist. Science 264, 1471-1474.
59. Yamashiro, D. J., Tycko, B., Fluss, S. R., Maxfield, F. R., Willingham, M. C., Hanover, J. A., Dickson, R. B. and Pastan, I. (1984). Segregation of transferrin to a mildly acidic (pH 6. 5) para-Golgi compartment in the recycling pathway. Cell 81, 175-179.
60. Zambon, A., Schmidt, I., Beisiegel, U. and Brunzell, J. D. (1996). Dimeric lipoprotein lipase is bound to triglyceride-rich plasma lipoproteins. J. Lipid Res. 37, 2394-2404.