LRAD3, a novel low-density lipoprotein receptor family member that modulates amyloid precursor protein trafficking

Journal of Neuroscience

Volumn 31, Issue 30, 2011, Pages 10836-10846

  Ranganathan, Sripriya ^a   Noyes, Nathaniel C ^a   Migliorini, Mary ^a   Winkles, Jeffrey A ^a   Battey, Frances D ^a   Hyman, Bradley T ^b   Smith, Elizabeth ^a   Yepes, Manuel ^c   Mikhailenko, Irina ^a   Strickland, Dudley K ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SECRETASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN ALPHA; BETA SECRETASE; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR CLASS A DOMAIN CONTAINING 3; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ANIMAL CELL; ARTICLE; BINDING ASSAY; BINDING SITE; BRAIN CORTEX; CELL MIGRATION; CONTROLLED STUDY; HALF LIFE TIME; HIPPOCAMPUS; HUMAN; HUMAN CELL; INTERNALIZATION; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; TISSUE DISTRIBUTION;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CEREBRAL CORTEX; CRICETINAE; EMBRYO, MAMMALIAN; ENDOCYTOSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOPRECIPITATION; MICE; MOLECULAR WEIGHT; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, LDL; RNA, MESSENGER; SEQUENCE ANALYSIS, PROTEIN; TRANSFECTION;

EID: 79960935129     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5065-10.2011     Document Type: Article

References (58)

1. Bacskai BJ, Xia MQ, Strickland DK, Rebeck GW, Hyman BT (2000) The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 97:11551-11556.
2. Bates P, Young JA, Varmus HE (1993) A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell 74:1043-1051.
3. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795.
4. Borg JP, Yang Y, De Taddéo-Borg M, Margolis B, Turner RS (1998) The X11alpha protein slows cellular amyloid precursor protein processing and reduces Abeta40 and Abeta42 secretion. J Biol Chem 273:14761-14766.
5. Bork P, Sudol M (1994) The WW domain: a signalling site in dystrophin? Trends Biochem Sci 19:531-533.
6. Brown MS, Ye J, Rawson RB, Goldstein JL (2000) Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100:391-398.
7. Cao X, Südhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293 [Erratum (2001) 293:1436]:115-120.
8. Chen HI, Sudol M (1995) The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc Natl Acad Sci U S A 92:7819-7823.
9. Cohen GB, Ren R, Baltimore D (1995) Modular binding domains in signal transduction proteins. Cell 80:237-248.
10. Davis CG, Goldstein JL, Südhof TC, Anderson RG, Russell DW, Brown MS (1987) Acid-dependent ligand dissociation and recylcing of LDL receptor mediated by growth factor homology region. Nature 326:760-765.
11. De Strooper B (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gammsAPPα complex. Neuron 38:9-12.
12. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS, Schroeter EH, Schrijvers V, Wolfe MS, Ray WJ, Goate A, Kopan R (1999) A presenilin-1-dependent gamms-secretase-like protease mediates release of Notch intracellular domain. Nature 398:518-522.
13. Dittrich E, Haft CR, Muys L, Heinrich PC, Graeve L (1996) A di-leucine motif andanupstream serinein the interleukin-6 (IL-6) signal transducer gp130 mediate ligand-induced endocytosis and down-regulation of the IL-6 receptor. J Biol Chem 271:5487-5494.
14. Fisher C, Beglova N, Blacklow SC (2006) Structure of an LDLR-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol Cell 22:277-283.
15. Fitz Gerald DJ, Fryling CM, Zdanovsky A, Saelinger CB, Kounnas M, Winkles JA, Strickland D, Leppla S (1995) Pseudomonas exotoxin-mediated selection yields cells with altered expression of low-density lipoprotein receptor-related protein. J Cell Biol 129:1533-1541.
16. Haft CR, Klausner RD, Taylor SI (1994) Involvement of dileucine motifs in the internalization and degradation of the insulin receptor. J Biol Chem 269:26286-26294.
17. Hamer I, Haft CR, Paccaud JP, Maeder C, Taylor S, Carpentier JL (1997) Dual roleof adileucine motif in insulin receptor endocytosis. J Biol Chem 272:21685-21691.
18. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
19. Herz J, Strickland DK (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108:779-784.
20. Ho DH, Vu H, Brown SA, Donohue PJ, Hanscom HN, Winkles JA (2004) Soluble tumor necrosis factor-like weak inducer of apoptosis overexpres-sion in HEK293 cells promotes tumor growth and angiogenesis in athy-mic nude mice. Cancer Res 64:8968-8972.
21. Hu K, Yang J, Tanaka S, Gonias SL, Mars WM, Liu Y (2006) Tissue-type plasminogen activator acts as a cytokine that triggers intracellular signal transduction and induces matrix metalloproteinase-9 gene expression. J Biol Chem 281:2120-2127.
22. Hunziker W, Fumey C (1994) A di-leucinemotifmediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO J 13:2963-2969.
23. Kinoshita A, Whelan CM, Smith CJ, Mikhailenko I, Rebeck GW, Strickland DK, Hyman BT (2001) Demonstration by fluorescence resonance energy transfer of two sites of interaction between the low-density lipoprotein receptor-related protein and the amyloid precursor protein: role of the intracellular adapter protein Fe65. J Neurosci 21:8354-8361.
24. Knauer MF, Orlando RA, Glabe CG (1996) Cell surface APP751 forms complexes with protease nexin 2 ligands and is internalized via the low density lipoprotein receptor-related protein (LRP). Brain Res 740:6-14.
25. Kounnas MZ, Moir RD, Rebeck GW, Bush AI, Argraves WS, Tanzi RE, Hyman BT, Strickland DK (1995) LDL receptor-related protein, a multifunctional apoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82:331-340.
26. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580.
27. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinfor-matics 23:2947-2948.
28. Lee D, Walsh JD, Mikhailenko I, Yu P, Migliorini M, Wu Y, Krueger S, Curtis JE, Harris B, Lockett S, Blacklow SC, Strickland DK, Wang YX (2006) RAP uses a histidine switch to regulate its interaction with LRP in the ER and Golgi. Mol Cell 22:423-430.
29. Letourneur F, Klausner RD (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69:1143-1157.
30. Liu Q, Zerbinatti CV, Zhang J, Hoe HS, Wang B, Cole SL, Herz J, Muglia L, Bu G (2007) Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1. Neuron 56:66-78.
31. Mikhailenko I, Kounnas MZ, Strickland DK (1995) Low density lipoprotein receptor-related protein/a2-macroglobulin receptor mediates the cellular internalization and degradation of thrombospondin. A process facilitated by cell-surface proteoglycans. J Biol Chem 270:9543-9549.
32. Mikhailenko I, Considine W, Argraves KM, Loukinov D, Hyman BT, Strickland DK (1999) Functional domains of the very low density lipoprotein receptor: molecular analysis of ligand binding and acid-dependent ligand dissociation mechanisms. J Cell Sci 112:3269-3281.
33. Mikhailenko I, Battey FD, Migliorini M, Ruiz JF, Argraves K, Moayeri M, Strickland DK (2001) Recognition of alpha 2-macroglobulin by the low density lipoprotein receptor-related protein requires the cooperation of two ligand binding cluster regions. J Biol Chem 276:39484-39491.
34. Misra UK, Chu CT, Gawdi G, Pizzo SV (1994) Evidence for a second alpha 2-macroglobulin receptor. J Biol Chem 269:12541-12547.
35. Newton CS, Loukinova E, Mikhailenko I, Ranganathan S, Gao Y, Hauden-schild C, Strickland DK (2005) Platelet-derived growth factor receptor-beta (PDGFR-beta) activation promotes its association with the low density lipoprotein receptor-related protein (LRP). Evidence for co-receptor function. J Biol Chem 280:27872-27878.
36. Nguyen DH, Hussaini IM, Gonias SL (1998) Binding of urokinase-type plasminogen activator to its receptor in MCF- 7 cells activates extracellular signal-regulated kinase 1 and 2 which is required for increased cellular motility. J Biol Chem 273:8502-8507.
37. Otsuki T, Ota T, Nishikawa T, Hayashi K, Suzuki Y, Yamamoto J, Wakamatsu A, Kimura K, Sakamoto K, Hatano N, Kawai Y, Ishii S, Saito K, Kojima S, Sugiyama T, Ono T, Okano K, Yoshikawa Y, Aotsuka S, Sasaki N, et al. (2005) Signal sequence and keyword trap in silico for selection of full-length human cDNAs encoding secretion or membrane proteins from oligo-capped cDNA libraries. DNARes 12:117-126.
38. Pawson T (1995) Protein modules and signalling networks. Nature 373:573-580.
39. Pawson T, Scott JD (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
40. Pietrzik CU, Busse T, Merriam DE, Weggen S, Koo EH (2002) The cytoplasmic domain of the LDL receptor-related protein regulates multiple steps in APP processing. EMBO J 21:5691-5700.
41. Pietrzik CU, Yoon IS, Jaeger S, Busse T, Weggen S, Koo EH (2004) FE65 constitutes the functional link between the low-density lipoprotein receptor-related protein and the amyloid precursor protein. J Neurosci 24:4259-4265.
42. Ranganathan S, Liu CX, Migliorini MM, Von Arnim CA, Peltan ID, Mikhailenko I, Hyman BT, Strickland DK (2004) Serine and threonine phosphorylation of the low density lipoprotein receptor-related protein by protein kinase Calpha regulates endocytosis and association with adaptor molecules. J Biol Chem 279:40536-40544.
43. Riddell DR, Graham A, Owen JS (1997) Apolipoprotein E inhibits platelet aggregation through the L-arginine:nitric oxide pathway. Implications for vascular disease. J Biol Chem 272:89-95.
44. Rudenko G, Henry L, Henderson K, Ichtchenko K, Brown MS, Goldstein JL, Deisenhofer J (2002) Structure of the LDL receptor extracellular domain at endosomal pH. Science 298:2353-2358.
45. Sabo SL, Lanier LM, Ikin AF, Khorkova O, Sahasrabudhe S, Greengard P, Buxbaum JD (1999) Regulation of β-amyloid secretion by FE65, an amyloid protein precursor-binding protein. J Biol Chem 274:7952-7957.
46. Schonbaum CP, Lee S, Mahowald AP (1995) The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proc Natl Acad Sci USA 92:1485-1489.
47. Sheikh H, Isacke CM (1996) A di-hydrophobic Leu-Val motif regulates the basolateral localization of CD44 in polarized Madin-Darby canine kidney epithelial cells. J Biol Chem 271:12185-12190.
48. Sisodia SS, Price DL (1995) Role of the β-amyloid protein in Alzheimer's disease. FASEB J 9:366-370.
49. Strickland DK, Ashcom JD, Williams S, Battey F, Behre E, McTigue K, Battey JF, Argraves WS (1991) Primary structure of α2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J Biol Chem 266:13364-13369.
50. Sudol M (1996) Structure and function of the WW domain. Prog Biophys Mol Biol 65:113-132.
51. Ulery PG, Beers J, Mikhailenko I, Tanzi RE, Rebeck GW, Hyman BT, Strickland DK (2000) Modulation of beta-amyloid precursor protein processing by the low density lipoprotein receptor-related protein (LRP). Evidence that lrp contributes to the pathogenesis of alzheimer's disease. J Biol Chem 275:7410-7415.
52. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, et al. (1999) BetsAPPα cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286:735-741.
53. Wiley HS, Cunningham DD (1982) The endocytotic rate constant. A cellular parameter for quantitating receptor-mediated endocytosis. J Biol Chem 257:4222-4229.
54. 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.
55. Willnow TE, Rohlmann A, Horton J, Otani H, Braun JR, Hammer RE, Herz J (1996) RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J 15:2632-2639.
56. Willnow TE, Nykjaer A, Herz J (1999) Lipoprotein receptors: new roles for ancient proteins. Nat Cell Biol 1:E157-E162.
57. Yamamoto T, Davis CG, Brown MS, Schneider WJ, Casey ML, Goldstein JL, Russell DW (1984) The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39:27-38.
58. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 112:1533-1540.