Low density lipoprotein receptor-related protein 1 dependent endosomal trapping and recycling of apolipoprotein E

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Laatsch, Alexander ^a   Panteli, Malamatenia ^a   Sornsakrin, Marijke ^a   Hoffzimmer, Britta ^a   Grewal, Thomas ^b   Heeren, Joerg ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 MACROGLOBULIN; APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; RNA; HIGH DENSITY LIPOPROTEIN CHOLESTEROL;

ARTICLE; CONTROLLED STUDY; ENDOSOME; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIVER CELL; LYSOSOME; PROTEIN EXPRESSION; PROTEIN SECRETION; RNA INTERFERENCE; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL STRAIN HEK293; ENDOCYTOSIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSGENIC MOUSE;

ANIMALS; APOLIPOPROTEINS E; CELLS, CULTURED; CHOLESTEROL, HDL; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HEPATOCYTES; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; TRANSFECTION;

EID: 84855388684     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029385     Document Type: Article

References (41)

1. Merkel M, Eckel RH, Goldberg IJ, (2002) Lipoprotein lipase: genetics, lipid uptake, and regulation. J Lipid Res 43: 1997-2006.
2. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, et al. (2011) Brown adipose tissue activity controls triglyceride clearance. Nat Med 17: 200-205 nm.2297 [pii];10.1038/nm.2297.
3. Heeren J, Beisiegel U, Grewal T, (2006) Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis. Arterioscler Thromb Vasc Biol 26: 442-448.
4. Beisiegel U, Weber W, Ihrke G, Herz J, Stanley KK, (1989) The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341: 162-164.
5. Beisiegel U, Weber W, Bengtsson-Olivecrona G, (1991) Lipoprotein lipase enhances the binding of chylomicrons to low density lipoprotein receptor-related protein. Proc Natl Acad Sci U S A 88: 8342-8346.
6. Rohlmann A, Gotthardt M, Hammer RE, Herz J, (1998) Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest 101: 689-695.
7. Laatsch A, Merkel M, Talmud PJ, Grewal T, Beisiegel U, et al. (2008) Insulin stimulates hepatic low density lipoprotein receptor-related protein 1 (LRP1) to increase postprandial lipoprotein clearance. Atherosclerosis.
8. Stanford KI, Bishop JR, Foley EM, Gonzales JC, Niesman IR, et al. (2009) Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J Clin Invest 119: 3236-3245 38251 [pii];10.1172/JCI38251.
9. Williams KJ, Chen K, (2010) Recent insights into factors affecting remnant lipoprotein uptake. Curr Opin Lipidol 21: 218-228 10.1097/MOL.0b013e328338cabc [doi];00041433-201006000-00010 [pii].
10. Havel RJ, Hamilton RL, (2004) Hepatic catabolism of remnant lipoproteins: where the action is. Arterioscler Thromb Vasc Biol 24: 213-215.
11. MacArthur JM, Bishop JR, Stanford KI, Wang L, Bensadoun A, et al. (2007) Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest 117: 153-164.
12. Out R, Kruijt JK, Rensen PC, Hildebrand RB, de Vos P, et al. (2004) Scavenger receptor BI plays a role in facilitating chylomicron metabolism. J Biol Chem 279: 18401-18406.
13. Heeren J, Weber W, Beisiegel U, (1999) Intracellular processing of endocytosed triglyceride-rich lipoproteins comprises both recycling and degradation. J Cell Sci 112 (Pt 3): 349-359.
14. Rensen PC, Jong MC, van Vark LC, van der BH, Hendriks WL, et al. (2000) Apolipoprotein E is resistant to intracellular degradation in vitro and in vivo. Evidence for retroendocytosis. J Biol Chem 275: 8564-8571.
15. Heeren J, Grewal T, Jackle S, Beisiegel U, (2001) Recycling of apolipoprotein E and lipoprotein lipase through endosomal compartments in vivo. J Biol Chem 276: 42333-42338.
16. Swift LL, Farkas MH, Major AS, Valyi-Nagy K, Linton MF, et al. (2001) A recycling pathway for resecretion of internalized apolipoprotein E in liver cells. J Biol Chem 276: 22965-22970.
17. Heeren J, Grewal T, Laatsch A, Rottke D, Rinninger F, et al. (2003) Recycling of apoprotein E is associated with cholesterol efflux and high density lipoprotein internalization. J Biol Chem 278: 14370-14378.
18. Hasty AH, Plummer MR, Weisgraber KH, Linton MF, Fazio S, et al. (2005) The recycling of apolipoprotein E in macrophages: Influence of HDL and apolipoprotein AI. J Lipid Res 46: 1433-1439.
19. Heeren J, Grewal T, Laatsch A, Becker N, Rinninger F, et al. (2004) Impaired recycling of apolipoprotein E4 is associated with intracellular cholesterol accumulation. J Biol Chem 279: 55483-55492.
20. Rellin L, Heeren J, Beisiegel U, (2008) Recycling of apolipoprotein E is not associated with cholesterol efflux in neuronal cells. Biochim Biophys Acta 1781: 232-238.
21. Davignon J, Gregg RE, Sing CF, (1988) Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis 8: 1-21.
22. Roses AD, (1996) Apolipoprotein E alleles as risk factors in Alzheimer's disease. Annu Rev Med 47: 387-400.
23. Heeren J, Niemeier A, Merkel M, Beisiegel U, (2002) Endothelial-derived lipoprotein lipase is bound to postprandial triglyceride-rich lipoproteins and mediates their hepatic clearance in vivo. J Mol Med 80: 576-584.
24. Binder RJ, Han DK, Srivastava PK, (2000) CD91: a receptor for heat shock protein gp96. Nat Immunol 1: 151-155.
25. Binder RJ, Srivastava PK, (2004) Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci U S A 101: 6128-6133.
26. Herz J, Goldstein JL, Strickland DK, Ho YK, Brown MS, (1991) 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J Biol Chem 266: 21232-21238.
27. Willnow TE, Orth K, Herz J, (1994) Molecular dissection of ligand binding sites on the low density lipoprotein receptor-related protein. J Biol Chem 269: 15827-15832.
28. Herz J, Strickland DK, (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108: 779-784.
29. Lillis AP, Mikhailenko I, Strickland DK, (2005) Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability. J Thromb Haemost 3: 1884-1893.
30. Harasaki K, Lubben NB, Harbour M, Taylor MJ, Robinson MS, (2005) Sorting of major cargo glycoproteins into clathrin-coated vesicles. Traffic 6: 1014-1026.
31. Laatsch A, Ragozin S, Grewal T, Beisiegel U, Heeren J, (2004) Differential RNA interference: replacement of endogenous with recombinant low density lipoprotein receptor-related protein (LRP). Eur J Cell Biol 83: 113-120.
32. Willnow TE, Moehring JM, Inocencio NM, Moehring TJ, Herz J, (1996) The low-density-lipoprotein receptor-related protein (LRP) is processed by furin in vivo and in vitro. Biochem J 313 (Pt 1): 71-76.
33. Czekay RP, Orlando RA, Woodward L, Lundstrom M, Farquhar MG, (1997) Endocytic trafficking of megalin/RAP complexes: dissociation of the complexes in late endosomes. Mol Biol Cell 8: 517-532.
34. Willnow TE, Goldstein JL, Orth K, Brown MS, Herz J, (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.
35. Muller D, Nykjaer A, Willnow TE, (2003) From holoprosencephaly to osteopathology: role of multifunctional endocytic receptors in absorptive epithelia. Ann Med 35: 290-299.
36. Terrand J, Bruban V, Zhou L, Gong W, El Asmar Z, et al. (2009) LRP1 controls intracellular cholesterol storage and fatty acid synthesis through modulation of Wnt signaling. J Biol Chem 284: 381-8.
37. Boucher P, Li WP, Matz RL, Takayama Y, Auwerx J, et al. (2007) LRP1 functions as an atheroprotective integrator of TGFbeta and PDFG signals in the vascular wall: implications for Marfan syndrome. PLoS ONE 2: e448.
38. Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J, (2003) LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300: 329-332.
39. Chen Y, Durakoglugil MS, Xian X, Herz J, (2010) ApoE4 reduces glutamate receptor function and synaptic plasticity by selectively impairing ApoE receptor recycling. Proc Natl Acad Sci U S A 107: 12011-12016.
40. Meredith MJ, (1988) Rat hepatocytes prepared without collagenase: prolonged retention of differentiated characteristics in culture. Cell Biol Toxicol 4: 405-425.
41. Kounnas MZ, Argraves WS, Strickland DK, (1992) The 39-kDa receptor-associated protein interacts with two members of the low density lipoprotein receptor family, alpha 2-macroglobulin receptor and glycoprotein 330. J Biol Chem 267: 21162-21166.