Increased extracellular amyloid deposition and neurodegeneration in human amyloid precursor protein transgenic mice deficient in receptor-associated protein

Journal of Neuroscience

Volumn 22, Issue 21, 2002, Pages 9298-9304

  Van Uden, Emily ^a,b   Mallory, Margaret ^a,b   Veinbergs, Isaac ^a,b   Alford, Michael ^a,b   Rockenstein, Edward ^a,b   Masliah, Eliezer ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid precursor protein; Amyloid protein; Apopoliprotein E; Low density lipoprotein receptor; Receptor associated protein; Transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CELL SURFACE RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; SENILE PLAQUE; TRANSGENIC MOUSE;

EID: 0036848549     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-21-09298.2002     Document Type: Article

References (59)

1. Bales K, Verina T, Dodel R, Du Y, Altstiel L, Bender M, Hyslop P, Johnstone E, Little S, Cummins D, Piccardo P, Ghetti B, Paul S (1997) Lack of apolipoprotein E dramatically reduces amyloid β-peptide deposition. Nat Genet 17:263-264.
2. Blacker D, Wilcox MA, Laird NM, Rodes L, Horvath SM, Go RC, Perry R, Watson Jr B, Bassett SS, McInnis MG, Albert MS, Hyman BT, Tanzi RE (1998) Alpha-2 macroglobulin is genetically associated with Alzheimer disease. Nat Genet 19:357-360.
3. Borth W (1992) Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J 6:3345-3353.
4. Bu G (1998) Receptor-associated protein: A specialized chaperone and antagonist for members of the LDL receptor gene family. Curr Opin Lipidol 9:149-155.
5. Bu G (2001) The roles of receptor-associated protein (RAP) as a molecular chaperone for members of the LDL receptor family. Int Rev Cytol 209:79-116.
6. Bu G, Geuze H, Strous G, Schwartz A (1995) 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J 14:2269-2280.
7. Checler F (1995) Processing of the β-amyloid precursor protein and its regulation in Alzheimer's disease. J Neurochem 65:1431-1444.
8. Christie RH, Chung H, Rebeck GW, Strickland D, Hyman BT (1996) Expression of the very low-density lipoprotein receptor (VLDL-r), an apolipoprotein-E receptor, in the central nervous system and in Alzheimer's disease. J Neuropathol Exp Neurol 55:491-498.
9. DeKosky S, Scheff S (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 27:457-464.
10. Dickson D, Crystal H, Bevona C, Honer W, Vincent I, Davies P (1995) Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol Aging 16:285-304.
11. El Khoury J, Hickman SE, Thomas CA, Loike JD, Silverstein SC (1998) Microglia, scavenger receptors, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 19:S81-S84.
12. Fabrizi C, Businaro R, Lauro G, Starace G, Fumagalli L (1999) Activated alpha2-microglobulin increases β-amyloid (25-35)-induced toxicity in LAN5 human neuroblastoma cells. Exp Neurol 155:252-259.
13. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemes J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527.
14. Goate A, Chartier-Harlin M-C, Mullan M, Brown J, Crawford F, Fidani L, Guiffra L, Haynes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Williamson R, Rossor M, Owen M, Hardy J (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706.
15. Helbecque N, Berr C, Cottel D, Fromentin-David I, Sazdovitch V, Ricolfi F, Ducimetiere P, Di Menza C, Amouyel P (2001) VLDL receptor polymorphism, cognitive impairment, and dementia. Neurology 56:1183-1188.
16. Herz J (2001a) The LDL receptor gene family: (Un)expected signal transducers in the brain. Neuron 29:571-581.
17. Herz J (2001b) Lipoprotein receptors: Beacons to neurons? Trends Neurosci 24:193-195.
18. Herz J, Beffert U (2000) Apolipoprotein E receptors: Linking brain development and Alzheimer's disease. Nat Rev Neurosci 1:51-58.
19. Herz J, Strickland DK (2001) LRP: A multifunctional scavenger and signaling receptor. J Clin Invest 108:779-784.
20. Herz J, Goldstein J, Strickland D, Ho Y, Brown M (1991) The 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J Biol Chem 266:21232-21238.
21. Hsia AY, Masliah E, McConlogue L, Yu G-Q, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
22. Huang F, Buttini M, Wyss-Coray T, McConlogue L, Kodama T, Pitas RE, Mucke L (1999) Elimination of the class A scavenger receptor does not affect amyloid plaque formation or neurodegeneration in transgenic mice expressing human amyloid protein precursors. Am J Pathol 155:1741-1747.
23. Huse JT, Doms RW (2001) Neurotoxic traffic: Uncovering the mechanics of amyloid production in Alzheimer's disease. Traffic 2:75-81.
24. Hussain MM, Strickland DK, Bakillah A (1999) The mammalian low-density lipoprotein receptor family. Annu Rev Nutr 19:141-172.
25. Irizarry MC, Cheung BS, Rebeck GW, Paul SM, Bales KR, Hyman BT (2000) Apolipoprotein E affects the amount, form, and anatomical distribution of amyloid beta-peptide deposition in homozygous APP(V717F) transgenic mice. Acta Neuropathol (Berl) 100:451-458.
26. Joachim C, Games D, Morris J, Ward P, Frenkel D, Selkoe D (1991) Antibodies to non-beta regions of the beta-amyloid precursor protein detect a subset of senile plaques. Am J Pathol 138:373-384.
27. Kang D, Saitoh T, Chen X, Xia Y, Masliah E, Hansen L, Thomas R, Thai L, Katzman R (1997) Genetic association of the low density lipoprotein receptor related protein gene (LRP), an apoE receptor, with late-onset Alzheimer's disease. Neurology 49:56-61.
28. Kang DE, Pietrzik CU, Baum L, Chevallier N, Merriam DE, Kounnas MZ, Wagner SL, Troncoso JC, Kawas CH, Katzman R, Koo EH (2000) Modulation of amyloid beta-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. J Clin Invest 106:1159-1166.
29. 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.
30. Kounnas M, Moir R, Rebeck G, Bush A, Argaves W, Tanzi R, Hyman B, Strickland D (1995) LDL receptor-related protein, a multifunctional apoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82:331-340.
31. LaDu MJ, Shah JA, Reardon CA, Getz GS, Bu G, Hu J, Guo L, van Eldik LJ (2000) Apolipoprotein E receptors mediate the effects of beta-amyloid on astrocyte cultures. J Biol Chem 275:33974-33980.
32. Mucke L, Yu GQ, McConlogue L, Rockenstein EM, Abraham CR, Masliah E (2000a) Astroglial expression of human alpha(1)-antichymotrypsin enhances alzheimer-like pathology in amyloid protein precursor transgenic mice. Am J Pathol 157:2003-2010.
33. Mucke L, Masliah E, Yu G-Q, Mallory M, Rockenstein E, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L (2000b) High-level neuronal expression of Aβ 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
34. Narita M, Bu G, Holtzman D, Schwartz A (1997a) The low-density lipoprotein receptor-related protein, a multifunctional apolipoprotein E receptor, modulates hippocampal neurite development. J Neurochem 68:587-595.
35. Narita M, Holtzman DM, Schwartz AL, Bu G (1997b) Alpha2-macroglobulin complexes with and mediates the endocytosis of beta-amyloid peptide via cell surface low-density lipoprotein receptor-related protein. J Neurochem 69:1904-1911.
36. Paresce DM, Ghosh RN, Maxfield FR (1996) Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 17:553-565.
37. Qiu Z, Strickland DK, Hyman BT, Rebeck GW (1999) Alpha2-macroglobulin enhances the clearance of endogenous soluble beta-amyloid peptide via low-density lipoprotein receptor-related protein in cortical neurons. J Neurochem 73:1393-1398.
38. Rebeck G, Harr S, Strickland D, Hyman B (1995) Multiple, diverse senile plaque-associated proteins are ligands of an apolipoprotein E receptor, the alpha 2-macroglobulin receptor/low-density-lipoprotein receptor-related protein. Ann Neurol 37:211-217.
39. Rebeck GW, Moir RD, Mui S, Strickland DK, Tanzi RE, Hyman BT (2001) Association of membrane-bound amyloid precursor protein APP with the apolipoprotein E receptor LRP. Mol Brain Res 87:238-245.
40. Rockenstein E, Mallory M, Mante M, Sisk A, Masliah E (2001) Early formation of mature amyloid-b proteins deposits in a mutant APP transgenic model depends on levels of Abl-42. J Neurosci Res 66:573-582.
41. Saunders A, Strittmatter W, Schmechel D, St. George-Hyslop P, Pericak-Vance M, Joo S, Rosi B, Gusella J, Crapper-MacLachlan D, Alberts M, Hulette C, Crain B, Goldgaber D, Roses A (1993) Association of apolipoprotein E allele E4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43:1467-1472.
42. Selkoe DJ, Yamazaki T, Citron M, Podlisny MB, Koo EH, Teplow DB, Haass C (1996) The role of APP processing and trafficking pathways in the formation of amyloid beta-protein. Ann NY Acad Sci 777:57-64.
43. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, Ghiso J, Zlokovic BV (2000) Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106:1489-1499.
44. Sinha S, Anderson J, John V, McConlogue L, Basi G, Thorsett E, Schenk D (2000) Recent advances in the understanding of the processing of APP to beta amyloid peptide. Ann NY Acad Sci 920:206-208.
45. Terry R, Masliah E, Salmon D, Butters N, DeTeresa R, Hill R, Hansen L, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
46. Trommsdorff M, Borg J, Margolis B, Herz J (1998) Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J Biol Chem 273:33556-33560.
47. Ulery P, Beers J, Mikhailenko I, Tanzi R, Rebeck G, Hyman B, Strickland D (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.
48. Umans L, Overbergh L, Serneels L, Tesseur I, Van Leuven F, Group EG (1999) Analysis of expression of genes involved in apolipoprotein E-based lipoprotein metabolism in pregnant mice deficient in the receptor-associated protein, the low density lipoprotein receptor, or apolipoprotein E. Biol Reprod 61:1216-1225.
49. Van Uden E, Veinbergs I, Mallory M, Orlando R, Masliah E (1999a) A novel role for receptor-associated protein in somatostatin modulation: Implications for Alzheimer's disease. Neuroscience 88:687-700.
50. Van Uden E, Carlson G, St. George-Hyslop P, Westaway D, Orlando R, Mallory M, Rockenstein E, Masliah E (1999b) Aberrant Presenilin-1 expression downregulates LDL receptor-related protein (LRP): Is LRP central to Alzheimer's disease pathogenesis? Mol Cell Neurosci 14:129-140.
51. Van Uden E, Sagara Y, Van Uden J, Orlando R, Mallory M, Rockenstein E, Masliah E (2000) A protective role of the low density lipoprotein receptor-related protein against amyloid β-protein toxicity. J Biol Chem 275:30525-30530.
52. Veinbergs I, Van Uden E, Mallory M, Alford M, McGiffert C, DeTeresa R, Orlando R, Masliah E (2001) Role of apolipoprotein E receptors in regulating the differential in vivo neurotrophic effects of apolipoprotein E. Exp Neurol 170:15-26.
53. Willnow T, Armstrong S, Hammer R, Herz J (1995) Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo. Proc Natl Acad Sci USA 92:4537-4541.
54. Willnow T, Rohlmann A, Horton J, Otani H, Braun J, Hammer R, 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.
55. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
56. Yang DS, Small DH, Seydel U, Smith JD, Hallmayer J, Gandy SE, Martins RN (1999) Apolipoprotein E promotes the binding and uptake of beta-amyloid into Chinese hamster ovary cells in an isoform-specific manner. Neuroscience 90:1217-1226.
57. Yazawa H, Yu ZX, Takeda, Le Y, Gong W, Ferrans VJ, Oppenheim JJ, Li CC, Wang JM (2001) Beta amyloid peptide (Abeta42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages. FASEB J 15:2454-2462.
58. Zhan S, Beyreuther K, Schmitt H (1993) Quantitative assessment of the synaptophysin immuno-reactivity of the cortical neuropil in various neurodegenerative disorders with dementia. Dementia 4:66-74.
59. Zhuo M, Holtzman DM, Li Y, Osaka H, DeMaro J, Jacquin M, Bu G (2000) Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J Neurosci 20:542-549.