Impaired LDL receptor-related protein 1 translocation correlates with improved dyslipidemia and atherosclerosis in apoE-deficient mice

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Gordts, Philip L S M ^a   Bartelt, Alexander ^b,c   Nilsson, Stefan K ^d   Annaert, Wim ^a,e   Christoffersen, Christina ^f   Nielsen, Lars Bo ^f,g   Heeren, Joerg ^b   Roebroek, Anton J M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Department of Biochemistry and Molecular Cell Biology ^*  (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UMEÅ UNIVERSITY   (Sweden)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CHYLOMICRON REMNANT; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DYSLIPIDEMIA; EMBRYO; ENDOCYTOSIS; GENE TARGETING; IN VIVO STUDY; LIPID METABOLISM; LIVER CELL; LIVER CLEARANCE; MALE; MOUSE; NONHUMAN; POSTPRANDIAL STATE; PROTEIN DEFECT; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; UPREGULATION; WILD TYPE; ANIMAL; BLOOD; CELL FRACTIONATION; CROSS BREEDING; FLUORESCENCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALIA; MUS;

AMINO ACID MOTIFS; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL FRACTIONATION; CROSSES, GENETIC; DYSLIPIDEMIAS; FLUORESCENCE; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HEPATOCYTES; IMMUNOBLOTTING; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MICE; MICE, TRANSGENIC; POSTPRANDIAL PERIOD; PROTEIN TRANSPORT; STATISTICS, NONPARAMETRIC; TRIGLYCERIDES;

EID: 84862023929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038330     Document Type: Article

References (49)

1. Libby P, (2002) Inflammation in atherosclerosis. Nature 420: 868-874.
2. Tabas I, Williams KJ, Boren J, (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116: 1832-1844.
3. Mahley RW, Huang Y, Rall SC Jr, (1999) Pathogenesis of type III hyperlipoproteinemia (dysbetalipoproteinemia). Questions, quandaries, and paradoxes. J Lipid Res 40: 1933-1949.
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. Kowal RC, Herz J, Goldstein JL, Esser V, Brown MS, (1989) Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc Natl Acad Sci U S A 86: 5810-5814.
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. Gordts PL, Reekmans S, Lauwers A, Van Dongen A, Verbeek L, et al. (2009) Inactivation of the LRP1 intracellular NPxYxxL motif in LDLR-deficient mice enhances postprandial dyslipidemia and atherosclerosis. Arterioscler Thromb Vasc Biol 29: 1258-1264.
8. 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.
9. 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.
10. 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.
11. Laatsch A, Merkel M, Talmud PJ, Grewal T, Beisiegel U, et al. (2009) Insulin stimulates hepatic low density lipoprotein receptor-related protein 1 (LRP1) to increase postprandial lipoprotein clearance. Atherosclerosis 204: 105-111.
12. Schaefer JR, (2009) Unraveling hyperlipidemia type III (dysbetalipoproteinemia), slowly. Eur J Hum Genet 17: 541-542.
13. Schneider WJ, Kovanen PT, Brown MS, Goldstein JL, Utermann G, et al. (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.
14. Mahley RW, Rall SC Jr, (2000) Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1: 507-537.
15. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, et al. (2010) Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466: 707-713.
16. Moon JH, Kang SB, Park JS, Lee BW, Kang ES, et al. (2011) Up-regulation of hepatic low-density lipoprotein receptor-related protein 1: a possible novel mechanism of antiatherogenic activity of hydroxymethylglutaryl-coenzyme A reductase inhibitor Atorvastatin and hepatic LRP1 expression. Metabolism 60: 930-940.
17. Hui DY, Basford JE, (2005) Distinct signaling mechanisms for apoE inhibition of cell migration and proliferation. Neurobiol Aging 26: 317-323.
18. Boucher P, Herz J, (2011) Signaling through LRP1: Protection from atherosclerosis and beyond. Biochem Pharmacol 81: 1-5.
19. Zhou L, Choi HY, Li WP, Xu F, Herz J, (2009) LRP1 controls cPLA2 phosphorylation, ABCA1 expression and cellular cholesterol export. PLoS One 4: e6853.
20. Yancey PG, Blakemore J, Ding L, Fan D, Overton CD, et al. (2010) Macrophage LRP-1 controls plaque cellularity by regulating efferocytosis and Akt activation. Arterioscler Thromb Vasc Biol 30: 787-795.
21. Yancey PG, Ding Y, Fan D, Blakemore JL, Zhang Y, et al. (2011) Low-density lipoprotein receptor-related protein 1 prevents early atherosclerosis by limiting lesional apoptosis and inflammatory Ly-6Chigh monocytosis: evidence that the effects are not apolipoprotein E dependent. Circulation 124: 454-464.
22. Roebroek AJ, Reekmans S, Lauwers A, Feyaerts N, Smeijers L, et al. (2006) Mutant Lrp1 knock-in mice generated by recombinase-mediated cassette exchange reveal differential importance of the NPXY motifs in the intracellular domain of LRP1 for normal fetal development. Mol Cell Biol 26: 605-616.
23. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N, (1992) Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci U S A 89: 4471-4475.
24. 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.
25. Otway S, Robinson DS, (1967) The use of a non-ionic detergent (Triton WR 1339) to determine rates of triglyceride entry into the circulation of the rat under different physiological conditions. J Physiol 190: 321-332.
26. Merkel M, Loeffler B, Kluger M, Fabig N, Geppert G, et al. (2005) Apolipoprotein AV accelerates plasma hydrolysis of triglyceride-rich lipoproteins by interaction with proteoglycan-bound lipoprotein lipase. J Biol Chem 280: 21553-21560.
27. Meredith MJ, (1988) Rat hepatocytes prepared without collagenase: prolonged retention of differentiated characteristics in culture. Cell Biol Toxicol 4: 405-425.
28. Dedieu S, Langlois B, Devy J, Sid B, Henriet P, et al. (2008) LRP-1 silencing prevents malignant cell invasion despite increased pericellular proteolytic activities. Mol Cell Biol 28: 2980-2995.
29. Reekmans SM, Pflanzner T, Gordts PL, Isbert S, Zimmermann P, et al. (2010) Inactivation of the proximal NPXY motif impairs early steps in LRP1 biosynthesis. Cell Mol Life Sci 67: 135-145.
30. 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.
31. Niemeier A, Gafvels M, Heeren J, Meyer N, Angelin B, et al. (1996) VLDL receptor mediates the uptake of human chylomicron remnants in vitro. J Lipid Res 37: 1733-1742.
32. 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 (Berl) 80: 576-584.
33. Niemeier A, Kassem M, Toedter K, Wendt D, Ruether W, et al. (2005) Expression of LRP1 by human osteoblasts: a mechanism for the delivery of lipoproteins and vitamin K1 to bone. J Bone Miner Res 20: 283-293.
34. Knisely JM, Lee J, Bu G, (2008) Measurement of receptor endocytosis and recycling. Methods Mol Biol 457: 319-332.
35. Schapiro FB, Soe TT, Mallet WG, Maxfield FR, (2004) Role of cytoplasmic domain serines in intracellular trafficking of furin. Mol Biol Cell 15: 2884-2894.
36. Tuma PL, Hubbard AL, (2001) Isolation of rat hepatocyte plasma membrane sheets and plasma membrane domains. Curr Protoc Cell Biol Chapter 3: Unit 32.
37. Mahley RW, Huang Y, (2007) Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. J Clin Invest 117: 94-98.
38. 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.
39. Mahley RW, Ji ZS, (1999) Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J Lipid Res 40: 1-16.
40. Brown MS, Goldstein JL, (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340.
41. Llorente-Cortes V, Royo T, Otero-Vinas M, Berrozpe M, Badimon L, (2007) Sterol regulatory element binding proteins downregulate LDL receptor-related protein (LRP1) expression and LRP1-mediated aggregated LDL uptake by human macrophages. Cardiovasc Res 74: 526-536.
42. Nilsson SK, Lookene A, Beckstead JA, Gliemann J, Ryan RO, et al. (2007) Apolipoprotein A-V interaction with members of the low density lipoprotein receptor gene family. Biochemistry 46: 3896-3904.
43. Basford JE, Wancata L, Hofmann SM, Silva RA, Davidson WS, et al. (2011) Hepatic deficiency of low density lipoprotein receptor-related protein-1 reduces high density lipoprotein secretion and plasma levels in mice. J Biol Chem 286: 13079-13087.
44. Melman L, Geuze HJ, Li Y, McCormick LM, Van Kerkhof P, et al. (2002) Proteasome regulates the delivery of LDL receptor-related protein into the degradation pathway. Mol Biol Cell 13: 3325-3335.
45. Donoso M, Cancino J, Lee J, van Kerkhof P, Retamal C, et al. (2009) Polarized traffic of LRP1 involves AP1B and SNX17 operating on Y-dependent sorting motifs in different pathways. Mol Biol Cell 20: 481-497.
46. Johnson AO, Subtil A, Petrush R, Kobylarz K, Keller SR, et al. (1998) Identification of an insulin-responsive, slow endocytic recycling mechanism in Chinese hamster ovary cells. J Biol Chem 273: 17968-17977.
47. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, et al. (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71: 343-353.
48. Ericsson S, Eriksson M, Vitols S, Einarsson K, Berglund L, et al. (1991) Influence of age on the metabolism of plasma low density lipoproteins in healthy males. J Clin Invest 87: 591-596.
49. Field PA, Gibbons GF, (2000) Decreased hepatic expression of the low-density lipoprotein (LDL) receptor and LDL receptor-related protein in aging rats is associated with delayed clearance of chylomicrons from the circulation. Metabolism 49: 492-498.