Low-density lipoprotein receptor represents an apolipoprotein E-independent pathway of Aβ uptake and degradation by astrocytes

Journal of Biological Chemistry

Volumn 287, Issue 17, 2012, Pages 13959-13971

  Basak, Jacob M ^a   Verghese, Philip B ^a   Yoon, Hyejin ^a   Kim, Jungsu ^a   Holtzman, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; APOLIPOPROTEIN E (APOE); APOLIPOPROTEINS; CELL SURFACE RECEPTORS; CELLULAR DEGRADATION; CELLULAR UPTAKE; GLIAL CELLS; LOW DENSITY LIPOPROTEINS; VESICULAR TRANSPORT;

CELL MEMBRANES;

DEGRADATION;

AMYLOID BETA PROTEIN; APOLIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; GLIA CELL; INTRACELLULAR SIGNALING; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR BINDING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; ASTROCYTES; BRAIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; LYSOSOMES; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN ISOFORMS; RECEPTORS, LDL;

EID: 84859980871     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.288746     Document Type: Article

References (50)

1. Holtzman, D. M., Morris, J. C., and Goate, A. M. (2011) Alzheimer disease, the challenge of the second century. Sci. Transl. Med. 3, 77sr1
2. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer disease. Progress and problems on the road to therapeutics. Science 297, 353-356
3. De Strooper, B. (2010) Proteases and proteolysis in Alzheimer disease. A multifactorial view on the disease process. Physiol. Rev. 90, 465-494
4. Hardy, J. (2006) A hundred years of Alzheimer disease research. Neuron 52, 3-13
5. Selkoe, D. J. (2001) Clearing the brain's amyloid cobwebs. Neuron 32, 177-180
6. Mawuenyega, K. G., Sigurdson, W., Ovod, V., Munsell, L., Kasten, T., Morris, J. C., Yarasheski, K. E., and Bateman, R. J. (2010) Decreased clearance of CNS β-amyloid in Alzheimer disease. Science 330, 1774
7. Tanzi, R. E., Moir, R. D., and Wagner, S. L. (2004) Clearance of Alzheimer Aβ peptide. The many roads to perdition. Neuron 43, 605-608
8. Zlokovic, B. V. (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201
9. Mandybur, T. I., and Chuirazzi, C. C. (1990) Astrocytes and the plaques of Alzheimer disease. Neurology 40, 635-639
10. Pike, C. J., Cummings, B. J., and Cotman, C. W. (1995) Early association of reactive astrocytes with senile plaques in Alzheimer disease. Exp. Neurol. 132, 172-179
11. Itagaki, S., McGeer, P. L., Akiyama, H., Zhu, S., and Selkoe, D. (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J. Neuroimmunol. 24, 173-182 (Pubitemid 19271472)
12. Nagele, R. G., D'Andrea, M. R., Lee, H., Venkataraman, V., and Wang, H. Y. (2003) Astrocytes accumulate Aβ42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res. 971, 197-209 (Pubitemid 36423321)
13. Funato, H., Yoshimura, M., Yamazaki, T., Saido, T. C., Ito, Y., Yokofujita, J., Okeda, R., and Ihara, Y. (1998) Astrocytes containing amyloid β-protein (Aβ)-positive granules are associated with Aβ40-positive diffuse plaques in the aged human brain. Am. J. Pathol. 152, 983-992 (Pubitemid 28173360)
14. Thal, D. R., Schultz, C., Dehghani, F., Yamaguchi, H., Braak, H., and Braak, E. (2000) Amyloid β-protein (Aβ)-containing astrocytes are located preferentially near N-terminal-truncated Aβ deposits in the human entorhinal cortex. Acta Neuropathol. 100, 608-617
15. Thal, D. R., Härtig, W., and Schober, R. (1999) Diffuse plaques in the molecular layer show intracellular Aβ(8-17)-immunoreactive deposits in subpial astrocytes. Clin. Neuropathol. 18, 226-231 (Pubitemid 29422202)
16. Shaffer, L. M., Dority, M. D., Gupta-Bansal, R., Frederickson, R. C., Younkin, S. G., and Brunden, K. R. (1995) Amyloid β protein (Aβ) removal by neuroglial cells in culture. Neurobiol. Aging 16, 737-745
17. Wyss-Coray, T., Loike, J. D., Brionne, T. C., Lu, E., Anankov, R., Yan, F., Silverstein, S. C., and Husemann, J. (2003) Adult mouse astrocytes degrade amyloid-β in vitro and in situ. Nat. Med. 9, 453-457 (Pubitemid 36460080)
18. Koistinaho, M., Lin, S., Wu, X., Esterman, M., Koger, D., Hanson, J., Higgs, R., Liu, F., Malkani, S., Bales, K. R., and Paul, S. M. (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid- β peptides. Nat. Med. 10, 719-726 (Pubitemid 38937637)
19. Nielsen, H. M., Veerhuis, R., Holmqvist, B., and Janciauskiene, S. (2009) Binding and uptake of Aβ(1-42) by primary human astrocytes in vitro. Glia 57, 978-988
20. Mahley, R. W. (1988) Apolipoprotein E, cholesterol transport protein with expanding role in cell biology. Science 240, 622-630
21. Verghese, P. B., Castellano, J. M., and Holtzman, D. M. (2011) Apolipoprotein E in Alzheimer disease and other neurological disorders. Lancet Neurol. 10, 241-252
22. Kim, J., Basak, J. M., and Holtzman, D. M. (2009) The role of apolipoprotein E in Alzheimer disease. Neuron 63, 287-303
23. Bales, K. R., Verina, T., Dodel, R. C., Du, Y., Altstiel, L., Bender, M., Hyslop, P., Johnstone, E. M., Little, S. P., Cummins, D. J., Piccardo, P., Ghetti, B., and Paul, S. M. (1997) Lack of apolipoprotein E dramatically reduces amyloid β-peptide deposition. Nat. Genet. 17, 263-264
24. Bales, K. R., Verina, T., Cummins, D. J., Du, Y., Dodel, R. C., Saura, J., Fishman, C. E., DeLong, C. A., Piccardo, P., Petegnief, V., Ghetti, B., and Paul, S. M. (1999) Apolipoprotein E is essential for amyloid deposition in the APP(V717F) transgenic mouse model of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 96, 15233-15238 (Pubitemid 30019795)
25. Herz, J., and Bock, H. H. (2002) Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71, 405-434 (Pubitemid 34800226)
26. Brown, M. S., and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34-47 (Pubitemid 16037973)
27. Kim, J., Castellano, J. M., Jiang, H., Basak, J. M., Parsadanian, M., Pham, V., Mason, S. M., Paul, S. M., and Holtzman, D. M. (2009) Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular Aβ clearance. Neuron 64, 632-644
28. Li, M., Husic, N., Lin, Y., Christensen, H., Malik, I., McIver, S., Daniels, C. M., Harris, D. A., Kotzbauer, P. T., Goldberg, M. P., and Snider, B. J. (2010) Optimal promoter usage for lentiviral vector-mediated transduction of cultured central nervous system cells. J. Neurosci. Methods 189, 56-64
29. -/-, and human apoE transgenic mice. J. Biol. Chem. 274, 30001-30007
30. Kanekiyo, T., Zhang, J., Liu, Q., Liu, C. C., Zhang, L., and Bu, G. (2011) Heparan sulfate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-β uptake. J. Neurosci. 31, 1644-1651
31. Kanekiyo, T., and Bu, G. (2009) Receptor-associated protein interacts with amyloid-β peptide and promotes its cellular uptake. J. Biol. Chem. 284, 33352-33359
32. Yin, K. J., Cirrito, J. R., Yan, P., Hu, X., Xiao, Q., Pan, X., Bateman, R., Song, H., Hsu, F. F., Turk, J., Xu, J., Hsu, C. Y., Mills, J. C., Holtzman, D. M., and Lee, J. M. (2006) Matrix metalloproteinases expressed by astrocytes mediate extracellular amyloid-β peptide catabolism. J. Neurosci. 26, 10939-10948 (Pubitemid 44772184)
33. Jiang, Q., Lee, C. Y., Mandrekar, S., Wilkinson, B., Cramer, P., Zelcer, N., Mann, K., Lamb, B., Willson, T. M., Collins, J. L., Richardson, J. C., Smith, J. D., Comery, T. A., Riddell, D., Holtzman, D. M., Tontonoz, P., and Landreth, G. E. (2008) ApoE promotes the proteolytic degradation of Aβ. Neuron 58, 681-693
34. Goldstein, J. L., Brown, M. S., Anderson, R. G., Russell, D. W., and Schneider, W. J. (1985) Receptor-mediated endocytosis. Concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1, 1-39
35. Dunn, K. W., and Maxfield, F. R. (1992) Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J. Cell Biol. 117, 301-310
36. Fryer, J. D., Demattos, R. B., McCormick, L. M., O'Dell, M. A., Spinner, M. L., Bales, K. R., Paul, S. M., Sullivan, P. M., Parsadanian, M., Bu, G., and Holtzman, D. M. (2005) The low-density lipoprotein receptor regulates the level of central nervous system human and murine apolipoprotein E but does not modify amyloid plaque pathology in PDAPP mice. J. Biol. Chem. 280, 25754-25759 (Pubitemid 40962285)
37. Cao, D., Fukuchi, K., Wan, H., Kim, H., and Li, L. (2006) Lack of LDL receptor aggravates learning deficits and amyloid deposits in Alzheimer transgenic mice. Neurobiol. Aging 27, 1632-1643 (Pubitemid 44344838)
38. LaDu, M. J., Falduto, M. T., Manelli, A. M., Reardon, C. A., Getz, G. S., and Frail, D. E. (1994) Isoform-specific binding of apolipoprotein E to β-amyloid. J. Biol. Chem. 269, 23403-23406
39. Tokuda, T., Calero, M., Matsubara, E., Vidal, R., Kumar, A., Permanne, B., Zlokovic, B., Smith, J. D., Ladu, M. J., Rostagno, A., Frangione, B., and Ghiso, J. (2000) Lipidation of apolipoprotein E influences its isoformspecific interaction with Alzheimer amyloid β peptides. Biochem. J. 348, 359-365 (Pubitemid 30345209)
40. Strittmatter, W. J., Weisgraber, K. H., Huang, D. Y., Dong, L. M., Salvesen, G. S., Pericak-Vance, M., Schmechel, D., Saunders, A. M., Goldgaber, D., and Roses, A. D. (1993) Binding of human apolipoprotein E to synthetic amyloid β peptide. Isoform-specific effects and implications for late-onset Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90, 8098-8102 (Pubitemid 23260862)
41. Mandrekar, S., Jiang, Q., Lee, C. Y., Koenigsknecht-Talboo, J., Holtzman, D. M., and Landreth, G. E. (2009) Microglia mediate the clearance of soluble Aβ through fluid phase macropinocytosis. J. Neurosci. 29, 4252-4262
42. Saavedra, L., Mohamed, A., Ma, V., Kar, S., and de Chaves, E. P. (2007) Internalization of β-amyloid peptide by primary neurons in the absence of apolipoprotein E. J. Biol. Chem. 282, 35722-35732 (Pubitemid 350277136)
43. Deane, R., Wu, Z., Sagare, A., Davis, J., Du Yan, S., Hamm, K., Xu, F., Parisi, M., LaRue, B., Hu, H. W., Spijkers, P., Guo, H., Song, X., Lenting, P. J., Van Nostrand, W. E., and Zlokovic, B. V. (2004) LRP/amyloid β-peptide interaction mediates differential brain efflux of Aβ isoforms. Neuron 43, 333-344 (Pubitemid 39061126)
44. Yamada, K., Hashimoto, T., Yabuki, C., Nagae, Y., Tachikawa, M., Strickland, D. K., Liu, Q., Bu, G., Basak, J. M., Holtzman, D. M., Ohtsuki, S., Terasaki, T., and Iwatsubo, T. (2008) The low-density lipoprotein receptor- related protein 1 mediates uptake of amyloid β peptides in an in vitro model of the blood-brain barrier cells. J. Biol. Chem. 283, 34554-34562
45. Lee, C. Y., and Landreth, G. E. (2010) The role of microglia in amyloid clearance from the AD brain. J. Neural. Transm. 117, 949-960
46. Deane, R., Sagare, A., Hamm, K., Parisi, M., Lane, S., Finn, M. B., Holtzman, D. M., and Zlokovic, B. V. (2008) ApoE-isoform specific disruption of amyloid β-peptide clearance from mouse brain. J. Clin. Invest. 118, 4002-4013
47. Castellano, J. M., Kim, J., Stewart, F. R., Jiang, H., DeMattos, R. B., Patterson, B. W., Fagan, A. M., Morris, J. C., Mawuenyega, K. G., Cruchaga, C., Goate, A. M., Bales, K. R., Paul, S. M., Bateman, R. J., and Holtzman, D. M. (2011) Human apoE isoforms differentially regulate brain amyloid-β peptide clearance. Sci. Transl. Med. 3, 89ra57
48. DeMattos, R. B., Cirrito, J. R., Parsadanian, M., May, P. C., O'Dell, M. A., Taylor, J. W., Harmony, J. A., Aronow, B. J., Bales, K. R., Paul, S. M., and Holtzman, D. M. (2004) ApoE and clusterin cooperatively suppress Aβ levels and deposition. Evidence that ApoE regulates extracellular Aβ metabolism in vivo. Neuron 41, 193-202
49. Elder, G. A., Cho, J. Y., English, D. F., Franciosi, S., Schmeidler, J., Sosa, M. A., Gasperi, R. D., Fisher, E. A., Mathews, P. M., Haroutunian, V., and Buxbaum, J. D. (2007) Elevated plasma cholesterol does not affect brain Aβ in mice lacking the low-density lipoprotein receptor. J. Neurochem. 102, 1220-1231 (Pubitemid 47174226)
50. Katsouri, L., and Georgopoulos, S. (2011) Lack of LDL receptor enhances amyloid deposition and decreases glial response in an Alzheimer disease mouse model. PLoS One 6, e21880