Quantitative fl uorescence imaging reveals point of release for lipoproteins during LDLR-dependent uptake

Journal of Lipid Research

Volumn 54, Issue 3, 2013, Pages 744-753

  Pompey, Shanica ^a   Zhao, Zhenze ^a   Luby Phelps, Kate ^a   Michaely, Peter ^a  

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

Author keywords

Early endosome antigen 1; Endosome; Low density lipoprotein; Very low density lipoprotein

Indexed keywords

BETA VERY LOW DENSITY LIPOPROTEIN; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PROTEIN VARIANT; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; INTERMEDIATE DENSITY LIPOPROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FIBROBLAST; FLUORESCENCE IMAGING; INTERNALIZATION; LIPID STORAGE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; CELL CULTURE; FLUORESCENCE; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; METABOLISM;

CELLS, CULTURED; ENDOSOMES; FLUORESCENCE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LIPOPROTEINS; LIPOPROTEINS, IDL; LIPOPROTEINS, LDL; OPTICAL IMAGING; RECEPTORS, LDL;

EID: 84874032311     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M033548     Document Type: Article

References (45)

1. Simonsen, A., R. Lippe, S. Christoforidis, J. M. Gaullier, A. Brech, J. Callaghan, B. H. Toh, C. Murphy, M. Zerial, and H. Stenmark. 1998. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature. 394 : 494-498.
2. Mills, I. G., A. T. Jones, and M. J. Clague. 1999. Regulation of endosome fusion. Mol. Membr. Biol. 16 : 73-79.
3. Tycko, B., and F. R. Maxfi eld. 1982. Rapid acidifi cation of endocytic vesicles containing alpha 2-macroglobulin. Cell. 28 : 643-651.
4. Galloway, C. J., G. E. Dean, M. Marsh, G. Rudnick, and I. Mellman. 1983. Acidifi cation of macrophage and fi broblast endocytic vesicles in vitro. Proc. Natl. Acad. Sci. USA. 80 : 3334-3338.
5. Gerasimenko, J. V., A. V. Tepikin, O. H. Petersen, and O. V. Gerasimenko. 1998. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 8 : 1335-1338.
6. Saito, M., P. I. Hanson, and P. Schlesinger. 2007. Luminal chloridedependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J. Biol. Chem. 282 : 27327-27333.
7. Davis, C. G., J. L. Goldstein, T. C. Sudhof, R. G. Anderson, D. W. Russell, and M. S. Brown. 1987. Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature. 326 : 760-765.
8. Zhao, Z., and P. Michaely. 2009. The role of calcium in lipoprotein release by the low-density lipoprotein receptor. Biochemistry. 48 : 7313-7324.
9. Esser, V., L. E. Limbird, M. S. Brown, J. L. Goldstein, and D. W. Russell. 1988. Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J. Biol. Chem. 263 : 13282-13290.
10. Russell, D. W., M. S. Brown, and J. L. Goldstein. 1989. Different combinations of cysteine-rich repeats mediate binding of low density lipoprotein receptor to two different proteins. J. Biol. Chem. 264 : 21682-21688.
11. Fisher, C., D. Abdul-Aziz, and S. C. Blacklow. 2004. A two-module region of the low-density lipoprotein receptor suffi cient for formation of complexes with apolipoprotein E ligands. Biochemistry. 43 : 1037-1044.
12. Fass, D., S. Blacklow, P. S. Kim, and J. M. Berger. 1997. Molecular basis of familial hypercholesterolaemia from structure of LDL receptor module. Nature. 388 : 691-693.
13. Dirlam-Schatz, K. A., and A. D. Attie. 1998. Calcium induces a conformational change in the ligand binding domain of the low density lipoprotein receptor. J. Lipid Res. 39 : 402-411.
14. Cuesta-López, S., F. Falo, and J. Sancho. 2007. Computational diagnosis of protein conformational diseases: short molecular dynamics simulations reveal a fast unfolding of r-LDL mutants that cause familial hypercholesterolemia. Proteins. 66 : 87-95.
15. Guttman, M., and E. A. Komives. 2011. The structure, dynamics, and binding of the LA45 module pair of the low-density lipoprotein receptor suggest an important role for LA4 in ligand release. Biochemistry. 50 : 11001-11008.
16. Rudenko, G., L. Henry, K. Henderson, K. Ichtchenko, M. S. Brown, J. L. Goldstein, and J. Deisenhofer. 2002. Structure of the LDL receptor extracellular domain at endosomal pH. Science. 298 : 2353-2358.
17. Zhao, Z., and P. Michaely. 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.
18. Zhao, Z., and P. Michaely. 2011. Role of an intramolecular contact on lipoprotein uptake by the LDL receptor. Biochim. Biophys. Acta. 1811 : 397-408.
19. Goldstein, J. L., S. K. Basu, and M. S. Brown. 1983. Receptormediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98 : 241-260.
20. Kovanen, P. T., M. S. Brown, S. K. Basu, D. W. Bilheimer, and J. L. Goldstein. 1981. Saturation and suppression of hepatic lipoprotein receptors: a mechanism for the hypercholesterolemia of cholesterol-fed rabbits. Proc. Natl. Acad. Sci. USA. 78 : 1396-1400.
21. Costes, S. V., D. Daelemans, E. H. Cho, Z. Dobbin, G. Pavlakis, and S. Lockett. 2004. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J. 86 : 3993-4003.
22. Michaely, P., Z. Zhao, W. P. Li, R. Garuti, L. J. Huang, H. H. Hobbs, and J. C. Cohen. 2007. Identifi cation of a VLDL-induced, FDNPVYindependent internalization mechanism for the LDLR. EMBO J. 26 : 3273-3282.
23. Lombardi, P., M. Mulder, H. van der Boom, R. R. Frants, and L. M. Havekes. 1993. Ineffi cient degradation of triglyceride-rich lipoprotein by HepG2 cells is due to a retarded transport to the lysosomal compartment. J. Biol. Chem. 268 : 26113-26119.
24. Bolte, S., and F. P. Cordelieres. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224 : 213-232.
25. Woodcroft, B. J., L. Hammond, J. L. Stow, and N. A. Hamilton. 2009. Automated organelle-based colocalization in whole-cell imaging. Cytometry A. 75 : 941-950.
26. Caster, A. H., and R. A. Kahn. 2012. Computational method for calculating fl uorescence intensities within three-dimensional structures in cells. Cell. Logist. 2 : 1-13.
27. Manders, E. M., J. Stap, G. J. Brakenhoff, R. van Driel, and J. A. Aten. 1992. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103 : 857-862.
28. Manders, E. M., F. J. Verbeek, and J. A. Aten. 1993. Measurement of co-localization of objects in dual-color confocal images. J. Microsc. 169 : 375-382.
29. Hamilton, N. A. 2012. Open source tools for fl uorescent imaging. Methods Enzymol. 504 : 393-417.
30. Goldstein, J. L., M. S. Brown, and N. J. Stone. 1977. Genetics of the LDL receptor: evidence that the mutations affecting binding and internalization are allelic. Cell. 12 : 629-641.
31. Anderson, R. G., J. L. Goldstein, and M. S. Brown. 1976. Localization of low density lipoprotein receptors on plasma membrane of normal human fi broblasts and their absence in cells from a familial hypercholesterolemia homozygote. Proc. Natl. Acad. Sci. USA. 73 : 2434-2438.
32. Brown, M. S., R. G. Anderson, S. K. Basu, and J. L. Goldstein. 1982. Recycling of cell-surface receptors: observations from the LDL receptor system. Cold Spring Harb. Symp. Quant. Biol. 46 : 713-721.
33. Aulinskas, T. H., D. R. van der Westhuyzen, E. L. Bierman, W. Gevers, and G. A. Coetzee. 1981. Retro-endocytosis of low density lipoprotein by cultured bovine aortic smooth muscle cells. Biochim. Biophys. Acta. 664 : 255-265.
34. Greenspan, P., and R. W. St Clair. 1984. Retroendocytosis of low density lipoprotein. Effect of lysosomal inhibitors on the release of undegraded 125I-low density lipoprotein of altered composition from skin fi broblasts in culture. J. Biol. Chem. 259 : 1703-1713.
35. Jones, N. L., J. A. Saunders, and R. R. Mallory. 2000. Intracellular traffi cking 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.
36. Jones, C., R. E. Hammer, W. P. Li, J. C. Cohen, H. H. Hobbs, and J. Herz. 2003. Normal sorting but defective endocytosis of the low density lipoprotein receptor in mice with autosomal recessive hypercholesterolemia. J. Biol. Chem. 278 : 29024-29030.
37. Brown, M. S., and J. L. Goldstein. 1976. Analysis of a mutant strain of human fi broblasts with a defect in the internalization of receptor-bound low density lipoprotein. Cell. 9 : 663-674.
38. Aulinskas, T. H., J. F. Oram, E. L. Bierman, G. A. Coetzee, W. Gevers, and D. R. van der Westhuyzen. 1985. Retro-endocytosis of low density lipoprotein by cultured human skin fi broblasts. Arteriosclerosis. 5 : 45-54.
39. Basu, S. K., J. L. Goldstein, R. G. Anderson, and M. S. Brown. 1981. Monensin interrupts the recycling of low density lipoprotein receptors in human fi broblasts. Cell. 24 : 493-502.
40. Lo Surdo, P., M. J. Bottomley, A. Calzetta, E. C. Settembre, A. Cirillo, S. Pandit, Y. G. Ni, B. Hubbard, A. Sitlani, and A. Carfi. 2011. Mechanistic implications for LDL receptor degradationfrom the PCSK9/LDLR structure at neutral pH. EMBO Rep. 12 : 1300-1305.
41. Hobbs, H. H., M. S. Brown, and J. L. Goldstein. 1992. Molecular genetics of the LDL receptor gene in familial hypercholesterolemia. Hum. Mutat. 1 : 445-466.
42. Zelcer, N., C. Hong, R. Boyadjian, and P. Tontonoz. 2009. LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science. 325 : 100-104.
43. Zhang, D. W., T. A. Lagace, R. Garuti, Z. Zhao, M. McDonald, J. D. Horton, J. C. Cohen, and H. H. Hobbs. 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.
44. Kohli, P., N. R. Desai, R. P. Giugliano, J. B. Kim, R. Somaratne, F. Huang, B. Knusel, S. McDonald, T. Abrahamsen, S. M. Wasserman, et al. 2012. Design and rationale of the LAPLACE-TIMI 57 trial: a phase II, double-blind, placebo-controlled study of the effi cacy and tolerability of a monoclonal antibody inhibitor of PCSK9 in subjects with hypercholesterolemia on background statin therapy. Clin. Cardiol. 35 : 385-391.
45. Zhang, L., K. Reue, L. G. Fong, S. G. Young, and P. Tontonoz. 2012. Feedback regulation of cholesterol uptake by the LXR-IDOL-LDLR axis. Arterioscler. Thromb. Vasc. Biol. 32 : 2541-2546.