The role of calcium in lipoprotein release by the low-density lipoprotein receptor

Biochemistry

Volumn 48, Issue 30, 2009, Pages 7313-7324

  Zhao, Zhenze ^a   Michaely, Peter ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PH; CELL LINES; CELL SURFACES; DEPENDENT PROCESS; ENDOSOMES; LOW CONCENTRATIONS; LOW DENSITY LIPOPROTEINS; RELATIVE CONTRIBUTION; RELEASE MECHANISM;

ACIDS; CALCIUM; CELL CULTURE; CELL MEMBRANES; LIPIDS; PROTEINS;

CALCIUM ALLOYS;

CALCIUM; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; VERY LOW DENSITY LIPOPROTEIN;

ARTICLE; CALCIUM TRANSPORT; ENDOSOME; FIBROBLAST; HUMAN; HUMAN CELL; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TRANSPORT;

ANIMALS; CALCIUM; CELLS, CULTURED; ENDOCYTOSIS; ENDOSOMES; FIBROBLASTS; GENE DELETION; HUMANS; HYDROGEN-ION CONCENTRATION; LIPOPROTEINS; MICE; MONENSIN; RECEPTORS, LDL;

EID: 68049092855     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900214u     Document Type: Article

References (73)

1. Yamamoto, T., Davis, C. G., Brown, M. S., Schneider, W. J., Casey, M. L., Goldstein, J. L., and Russell, D. W. (1984) The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39, 27-38. (Pubitemid 15218222)
2. Davis, C. G., Lehrman, M. A., Russell, D. W., Anderson, R. G., Brown, M. S., and Goldstein, J. L. (1986) The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45, 15-24.
3. Lehrman, M. A., Goldstein, J. L., Brown, M. S., Russell, D. W., and Schneider, W. J. (1985) Internalization-defective LDL receptors produced by genes with nonsense and frameshift mutations that truncate the cytoplasmic domain. Cell 41, 735-743.
4. He, G., Gupta, S., Yi, M., Michaely, P., Hobbs, H. H., and Cohen, J. C. (2002) ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J. Biol. Chem. 277, 44044-44049.
5. Mishra, S.K., Watkins, S. C., and Traub, L. M. (2002) The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc. Natl. Acad. Sci. U.S.A. 99, 16099-16104.
6. Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Agostinelli, N. R., Watkins, S. C., and Traub, L. M. (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21, 4915-4926.
7. Bilheimer, D. W., Watanabe, Y., and Kita, T. (1982) Impaired receptor-mediated catabolism of low density lipoprotein in the WHHL rabbit, an animal model of familial hypercholesterolemia. Pro. Natl. Acad. Sci. U.S.A. 79, 3305-3309.
8. Kita, T., Brown, M. S., Bilheimer, D. W., and Goldstein, J. L. (1982) Delayed clearance of very low density and intermediate density lipoproteins with enhanced conversion to low density lipoprotein in WHHL rabbits. Proc. Natl. Acad. Sci. U.S.A. 79, 5693-5697.
9. Brown, M. S., and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34-47.
10. Hobbs, H. H., Brown, M. S., and Goldstein, J. L. (1992) Molecular genetics of the LDL receptor gene in familial hypercholesterolemia. Hum. Mutat. 1, 445-466.
11. Esser, V., Limbird, L. E., Brown, M. S., Goldstein, J. L., and Russell, D. W. (1988) Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J. Biol. Chem. 263, 13282-13290.
12. Daly, N. L., Scanlon, M. J., Djordjevic, J. T., Kroon, P. A., and Smith,R. (1995) Three-dimensional structure of a cysteine-rich repeat from the low-density lipoprotein receptor. Proc. Natl. Acad. Sci. U.S. A. 92, 6334-6338.
13. North, C. L., and Blacklow, S.C. (2000) Solution structure of the sixth LDL-A module of the LDL receptor. Biochemistry 39, 2564-2571.
14. Shireman, R., Kilgore, L. L., and Fisher, W. R. (1977) Solubilization of apolipoprotein B and its specific binding by the cellular receptor for low density lipoprotein. Proc. Natl. Acad. Sci. U.S.A. 74, 5150-5154.
15. Brown, M. S., Kovanen, P. T., and Goldstein, J. L. (1981) Regulation of plasma cholesterol by lipoprotein receptors. Science 212, 628-635. (Pubitemid 11066529)
16. Russell, D. W., Brown, M. S., and Goldstein, J. L. (1989) Different combinations of cysteine-rich repeats mediate binding of low density lipoprotein receptor to two different proteins. J. Biol. Chem. 264, 21682-21688.
17. 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.
18. Schneider, W. J., Kovanen, P. T., Brown, M. S., Goldstein, J. L., Utermann, G., Weber, W., Havel, R. J., Kotite, L., Kane, J. P., Innerarity, T. L., and Mahley, R. W. (1981) Familial dysbetalipoproteinemia. Abnormal binding of mutant apoprotein E to low density lipoprotein receptors of human fibroblasts and membranes from liver and adrenal of rats, rabbits, and cows. J. Clin. Invest. 68, 1075-1085.
19. Fisher, C., Abdul-Aziz, D., and Blacklow, S. C. (2004) A two-module region of the low-density lipoprotein receptor sufficient for formation of complexes with apolipoprotein E ligands. Biochemistry 43, 1037-1044. (Pubitemid 38141503)
20. Davis, C. G., Goldstein, J. L., Sudhof, T. C., Anderson, R. G., Russell, D. W., and Brown, M. S. (1987) Acid-dependent ligand dissociation and recycling ofLDL receptor mediated by growth factor homology region. Nature 326, 760-765.
21. Beglova, N., Jeon, H., Fisher, C., and Blacklow, S. C. (2004) Cooperation between fixed and low pH-inducible interfaces controls lipoprotein release by the LDL receptor. Mol. Cell 16, 281-292. (Pubitemid 39388842)
22. Jeon, H., Meng, W., Takagi, J., Eck, M. J., Springer, T. A., and Blacklow, S. C. (2001) Implications for familial hypercholesterolemia from the structure of the LDL receptor YWTD-EGF domain pair. Nat. Struct. Biol. 8, 499-504.
23. Rudenko, G., Henry, L., Henderson, K., Ichtchenko, K., Brown, M. S., Goldstein, J. L., and Deisenhofer, J. (2002) Structure of the LDL receptor extracellular domain at endosomal pH. Science 298, 2353-2358. (Pubitemid 36014201)
24. Zhao, Z., and Michaely, P. (2008) The epidermal growth factor homology domain of the LDL receptor drives lipoprotein release through an allosteric mechanism involving H190, H562, and H586. J. Biol. Chem. 283, 26528-26537.
25. 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.
26. Basu, S. K., Goldstein, J. L., and Brown, M. S. (1978) Characterization of the low density lipoprotein receptor in membranes prepared from human fibroblasts. J. Biol. Chem. 253, 3852-3856.
27. Blacklow, S. C., and Kim, P. S. (1996) Protein folding and calcium binding defects arising from familial hypercholesterolemia mutations of the LDL receptor. Nat. Struct. Biol. 3, 758-762.
28. Fass, D., Blacklow, S., Kim, P. S., and Berger, J. M. (1997) Molecular basis of familial hypercholesterolaemia from structure of LDL receptor module. Nature 388, 691-693. (Pubitemid 27366442)
29. Atkins, A. R., Brereton, I. M., Kroon, P. A., Lee, H. T., and Smith,R. (1998) Calciumis essential for the structural integrity of the cysteine-rich, ligand-binding repeat of the low-density lipoprotein receptor. Biochemistry 37, 1662-1670.
30. Dirlam-Schatz, K. A., and Attie, A. D. (1998) Calcium induces a conformational change in the ligand binding domain of the low density lipoprotein receptor. J. Lipid Res. 39, 402-411.
31. 2+ affinity of the fifth binding module of the LDL receptor. J. Biol. Chem. 283, 22670-22679.
32. Simonovic, M., Dolmer, K., Huang, W., Strickland, D. K., Volz, K., and Gettins, P. G. (2001) Calcium coordination and pH dependence of the calcium affinity of ligand-binding repeat CR7 from the LRP. Comparison with related domains from the LRP and the LDL receptor. Biochemistry 40, 15127-15134.
33. Gerasimenko, J. V., Tepikin, A. V., Petersen, O. H., and Gerasimenko, O. V. (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 8, 1335-1338.
34. Rudenko, G., and Deisenhofer, J. (2003) The low-density lipoprotein receptor: ligands, debates and lore. Curr. Opin. Struct. Biol. 13, 683-689.
35. Beglova, N., and Blacklow, S. C. (2005) The LDL receptor: how acid pulls the trigger. Trends Biochem. Sci. 30, 309-317.
36. Liu, X., Sun, Y., Constantinescu, S. N., Karam, E., Weinberg, R. A., and Lodish, H. F. (1997) Transforming growth factor beta-induced phosphorylation of Smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 94, 10669-10674.
37. 125I-containing acylating agent. Biochem. J. 133, 529-539.
38. Goldstein, J. L., Basu, S. K., and Brown, M. S. (1983) Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98, 241-260. (Pubitemid 14219888)
39. Heuser, J. E., and Anderson, R. G. (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108, 389-400.
40. Patton, C., Thompson, S., and Epel, D. (2004) Some precautions in using chelators to buffer metals in biological solutions. Cell Calcium 35, 427-431. (Pubitemid 38379530)
41. 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.
42. Michaely, P., Zhao, Z., Li, W. P., Garuti, R., Huang, L. J., Hobbs, H. H., and Cohen, J. C. (2007) Identification of a VLDL-induced, FDNPVY-independent internalization mechanism for the LDLR. EMBO J. 26, 3273-3282.
43. Morales, C. P., Holt, S. E., Ouellette, M., Kaur, K. J., Yan, Y., Wilson, K. S., White, M. A., Wright, W. E., and Shay, J. W. (1999) Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat. Genet. 21, 115-118.
44. Dirlam, K. A., Gretch, D. G., LaCount, D. J., Sturley, S. L., and Attie, A. D. (1996) Expression and characterization of a truncated, soluble, low-density lipoprotein receptor. Protein Expression Purif. 8, 489-500. (Pubitemid 27015826)
45. Jeon, H., and Shipley, G. G. (2000) Vesicle-reconstituted low density lipoprotein receptor. Visualization by cryoelectron microscopy. J. Biol. Chem. 275, 30458-30464.
46. Basu, S. K., Goldstein, J. L., Anderson, R. G., and Brown, M. S. (1981) Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 24, 493-502.
47. Michaely, P., Li, W. P., Anderson, R. G., Cohen, J. C., and Hobbs, H. H. (2004) The modular adaptor protein ARH is required for low density lipoprotein (LDL) binding and internalization but not for LDL receptor clustering in coated pits. J. Biol. Chem. 279, 34023-34031.
48. Saito, M., Hanson, P. I., and Schlesinger, P. (2007) Luminal chloride-dependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J. Biol. Chem. 282, 27327-27333.
49. Brown, M. S., Anderson, R. G., Basu, S. K., and Goldstein, J. L. (1982) Recycling of cell-surface receptors: observations from the LDL receptor system. Cold Spring Harbor Symp. Quant. Biol. 46 (Part 2), 713-721.
50. Colombo, M. I., Beron, W., and Stahl, P. D. (1997) Calmodulin regulates endosome fusion. J. Biol. Chem. 272, 7707-7712.
51. Holroyd, C., Kistner, U., Annaert, W., and Jahn, R. (1999) Fusion of endosomes involved in synaptic vesicle recycling. Mol. Biol. Cell 10, 3035-3044.
52. 2+ and N-ethylmaleimide-sensitive factor differentially regulate disassembly ofSNARE complexes on early endosomes. J. Biol. Chem. 279, 18270-18276.
53. Maziere, J. C., Maziere, C., Mora, L., Gardette, J., and Polonovski, J. (1984) Effects of the calcium ionophore A 23187 on low-density lipoprotein processing and lipid metabolism in cultured human fibroblasts. FEBS Lett. 177, 76-80. (Pubitemid 15216040)
54. 2+. J. Physiol. 565, 743-750.
55. Hemmaplardh, D., and Morgan, E. H. (1977) The role of calcium in transferrin and iron uptake by reticulocytes. Biochim. Biophys. Acta 468, 423-436.
56. Iacopetta, B., Carpentier, J. L., Pozzan, T., Lew, D. P., Gorden, P., and Orci, L. (1986) Role of intracellular calcium and protein kinase C in the endocytosis of transferrin and insulin by HL60 cells. J. Cell Biol. 103, 851-856. (Pubitemid 17177334)
57. von Gersdorff,H., and Matthews, G. (1994) Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652-655.
58. Pitas,R. E., Innerarity, T. L., Arnold, K. S., and Mahley, R. W. (1979) Rate and equilibrium constants for binding of apo-E HDLc (a cholesterol-induced lipoprotein) and low density lipoproteins to human fibroblasts: evidence for multiple receptor binding of apo-E HDLc. Proc. Natl. Acad. Sci. U.S.A. 76, 2311-2315.
59. Windler, E. E., Kovanen, P. T., Chao, Y. S., Brown, M. S., Havel, R. J., and Goldstein, J. L. (1980) The estradiol-stimulated lipoprotein receptor of rat liver. A binding site that membrane mediates the uptake of rat lipoproteins containing apoproteins B and E. J. Biol. Chem. 255, 10464-10471.
60. 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. (Pubitemid 21909995)
61. 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. (Pubitemid 20263776)
62. Jones, N. L., Saunders, J. A., and Mallory, R. R. (2000) Intracellular trafficking of pigeon beta-very low density lipoprotein and low density lipoprotein at low and high concentrations in pigeon macrophages. J. Lipid Res. 41, 1823-1831.
63. Bersot, T. P., Mahley, R. W., Brown, M. S., and Goldstein, J. L. (1976) Interaction of swine lipoproteins with the low density lipoprotein receptor in human fibroblasts. J. Biol. Chem. 251, 2395-2398.
64. Chappell, D. A., Fry, G. L., Waknitz, M. A., Muhonen, L. E., and Pladet, M. W. (1993) Low density lipoprotein receptors bind and mediate cellular catabolism of normal very low density lipoproteins in vitro. J. Biol. Chem. 268, 25487-25493.
65. Horsthemke, B., Dunning, A., and Humphries, S. (1987) Identification of deletions in the human low density lipoprotein receptor gene. J. Med. Genet. 24, 144-147.
66. Russell, D. W., Lehrman, M. A., Sudhof, T. C., Yamamoto, T., Davis, C. G., Hobbs, H. H., Brown, M. S., and Goldstein, J. L. (1986) The LDL receptor in familial hypercholesterolemia: use of human mutations to dissect a membrane protein. Cold Spring Harbor Symp. Quant. Biol. 51 (Part 2), 811-819.
67. Top, B., Koeleman, B. P., Gevers Leuven, J. A., Havekes, L. M., and Frants, R. R. (1990) Rearrangements in the LDL receptor gene in Dutch familial hypercholesterolemic patients and the presence of a common 4 kb deletion. Atherosclerosis 83, 127-136.
68. Henderson, H. E., Berger, G. M., and Marais, A. D. (1988) A new LDL receptor gene deletion mutation in the South African population. Hum. Genet. 80, 371-374.
69. Sun, X. M., Webb, J. C., Gudnason, V., Humphries, S., Seed, M., Thompson, G. R., Knight, B. L., and Soutar, A. K. (1992) Characterization of deletions in the LDL receptor gene in patients with familial hypercholesterolemia in the United Kingdom. Arterioscler. Thromb. 12, 762-770.
70. van der Westhuyzen, D. R., Stein, M. L., Henderson, H. E., Marais, A. D., Fourie, A. M., and Coetzee, G. A. (1991) Deletion of two growth-factor repeats from the low-density-lipoprotein receptor accelerates its degradation. Biochem. J. 277, 677-682.
71. Zhang, D. W., Lagace, T. A., Garuti, R., Zhao, Z., McDonald, M., Horton, J. D., Cohen, J. C., and Hobbs, H. H. (2007) Binding of proprotein convertase subtilisin/kexin type 9 to epidermal growth factor-like repeat A of low density lipoprotein receptor decreases receptor recycling and increases degradation. J. Biol. Chem. 282, 18602-18612.
72. 125I-low density lipoprotein of altered composition from skin fibroblasts in culture. J. Biol. Chem. 259, 1703-1713.
73. 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. (Pubitemid 15171665)