Cdk5 protein inhibition and Aβ42 increase BACE1 protein level in primary neurons by a post-transcriptional mechanism: Implications of CDK5 as a therapeutic target for Alzheimer disease

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7224-7235

  Sadleir, Katherine R ^a   Vassar, Robert ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; CASPASE-3; CORTICAL NEURONS; DOSE-DEPENDENT MANNER; NEURODEGENERATION; POST-TRANSCRIPTIONAL MECHANISMS; PROTEIN INHIBITION; PROTEIN LEVEL; ROSCOVITINE; SECRETASES; THERAPEUTIC TARGETS; TRANSGENIC MICE;

MAMMALS; NEURODEGENERATIVE DISEASES; OLIGOMERS;

ENZYME INHIBITION;

AMYLOID BETA PROTEIN[1-42]; BETA SECRETASE 1; CASPASE 3; CASPASE 3 INHIBITOR; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; MESSENGER RNA; PROTEIN P25; PROTEIN P35; ROSCOVITINE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA SECRETASE 1 GENE; BRAIN NERVE CELL; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BRAIN; CASPASE 3; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; MALE; MICE; NEURONS; OLIGOPEPTIDES; PROTEIN KINASE INHIBITORS; PURINES;

MUS MUSCULUS;

EID: 84857713442     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.333914     Document Type: Article

References (64)

1. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R., Luo, Y., Fisher, S., Fuller, J., Edenson, S., Lile, J., Jarosinski, M. A., Biere, A. L., Curran, E., Burgess, T., Louis, J. C., Collins, F., Treanor, J., Rogers, G., and Citron, M. (1999) β-Secretase cleavage of Alzheimer amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741
2. Cai, H., Wang, Y., McCarthy, D., Wen, H., Borchelt, D. R., Price, D. L., and Wong, P. C. (2001) BACE1 is the major β-secretase for generation of Aßpeptides by neurons. Nat. Neurosci. 4, 233-234 (Pubitemid 32194867)
3. Luo, Y., Bolon, B., Kahn, S., Bennett, B. D., Babu-Khan, S., Denis, P., Fan, W., Kha, H., Zhang, J., Gong, Y., Martin, L., Louis, J. C., Yan, Q., Richards, W. G., Citron, M., and Vassar, R. (2001) Mice deficient in BACE1, the Alzheimer β-secretase, have normal phenotype and abolished β-amyloid generation. Nat. Neurosci. 4, 231-232 (Pubitemid 32194866)
4. Roberds, S. L., Anderson, J., Basi, G., Bienkowski, M. J., Branstetter, D. G., Chen, K. S., Freedman, S. B., Frigon, N. L., Games, D., Hu, K., Johnson- Wood, K., Kappenman, K. E., Kawabe, T. T., Kola, I., Kuehn, R., Lee, M., Liu, W., Motter, R., Nichols, N. F., Power, M., Robertson, D. W., Schenk, D., Schoor, M., Shopp, G. M., Shuck, M. E., Sinha, S., Svensson, K. A., Tatsuno, G., Tintrup, H., Wijsman, J., Wright, S., and McConlogue, L. (2001) BACE knockout mice are healthy despite lacking the primary β-secretase activity in brain. Implications for Alzheimer disease therapeutics. Hum. Mol. Genet. 10, 1317-1324 (Pubitemid 32600485)
5. Kao, S. C., Krichevsky, A. M., Kosik, K. S., and Tsai, L. H. (2004) BACE1 suppression by RNA interference in primary cortical neurons. J. Biol. Chem. 279, 1942-1949 (Pubitemid 38084465)
6. Laird, F. M., Cai, H., Savonenko, A. V., Farah, M. H., He, K., Melnikova, T., Wen, H., Chiang, H. C., Xu, G., Koliatsos, V. E., Borchelt, D. R., Price, D. L., Lee, H. K., and Wong, P. C. (2005) BACE1, a major determinant of selective vulnerability of the brain to amyloid-β amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J. Neurosci. 25, 11693-11709 (Pubitemid 43098462)
7. Singer, O., Marr, R. A., Rockenstein, E., Crews, L., Coufal, N. G., Gage, F. H., Verma, I. M., and Masliah, E. (2005) Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat. Neurosci. 8, 1343-1349 (Pubitemid 41630422)
8. Bodendorf, U., Danner, S., Fischer, F., Stefani, M., Sturchler-Pierrat, C., Wiederhold, K. H., Staufenbiel, M., and Paganetti, P. (2002) Expression of human β-secretase in the mouse brain increases the steady-state level of β-amyloid. J. Neurochem. 80, 799-806 (Pubitemid 34809232)
9. Chiocco, M. J., Kulnane, L. S., Younkin, L., Younkin, S., Evin, G., and Lamb, B. T. (2004) Altered amyloid-β metabolism and deposition in genomic-based β-secretase transgenic mice. J. Biol. Chem. 279, 52535-52542 (Pubitemid 39662732)
10. Lee, E. B., Zhang, B., Liu, K., Greenbaum, E. A., Doms, R. W., Trojanowski, J. Q., and Lee, V. M. (2005) BACE overexpression alters the subcellular processing of APP and inhibits Aβ deposition in vivo. J. Cell Biol. 168, 291-302 (Pubitemid 40248226)
11. Mohajeri, M. H., Saini, K. D., and Nitsch, R. M. (2004) Transgenic BACE expression in mouse neurons accelerates amyloid plaque pathology. J. Neural Transm. 111, 413-425 (Pubitemid 38316613)
12. Mullan, M., Crawford, F., Axelman, K., Houlden, H., Lilius, L., Winblad, B., and Lannfelt, L. (1992) A pathogenic mutation for probable Alzheimer disease in the APP gene at the N terminus of β-amyloid. Nat. Genet. 1, 345-347
13. Citron, M., Oltersdorf, T., Haass, C., McConlogue, L., Hung, A. Y., Seubert, P., Vigo-Pelfrey, C., Lieberburg, I., and Selkoe, D. J. (1992) Mutation of the β-amyloid precursor protein in familial Alzheimer disease increases β-protein production. Nature 360, 672-674 (Pubitemid 23007680)
14. Fukumoto, H., Cheung, B. S., Hyman, B. T., and Irizarry, M. C. (2002) β-Secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch. Neurol. 59, 1381-1389 (Pubitemid 35014802)
15. Holsinger, R. M., McLean, C. A., Beyreuther, K., Masters, C. L., and Evin, G. (2002) Increased expression of the amyloid precursor β-secretase in Alzheimer disease. Ann. Neurol. 51, 783-786 (Pubitemid 34568861)
16. Li, R., Lindholm, K., Yang, L. B., Yue, X., Citron, M., Yan, R., Beach, T., Sue, L., Sabbagh, M., Cai, H., Wong, P., Price, D., and Shen, Y. (2004) Amyloid β peptide load is correlated with increased β-secretase activity in sporadic Alzheimer disease patients. Proc. Natl. Acad. Sci. U.S.A. 101, 3632-3637 (Pubitemid 38338246)
17. O'Connor, T., Sadleir, K. R., Maus, E., Velliquette, R. A., Zhao, J., Cole, S. L., Eimer, W. A., Hitt, B., Bembinster, L. A., Lammich, S., Lichtenthaler, S. F., Hébert, S. S., De Strooper, B., Haass, C., Bennett, D. A., and Vassar, R. (2008) Phosphorylation of the translation initiation factor eIF2α increases BACE1 levels and promotes amyloidogenesis. Neuron 60, 988-1009
18. Zhao, J., Fu, Y., Yasvoina, M., Shao, P., Hitt, B., O'Connor, T., Logan, S., Maus, E., Citron, M., Berry, R., Binder, L., and Vassar, R. (2007) β-Site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques. Implications for Alzheimer disease pathogenesis. J. Neurosci. 27, 3639-3649 (Pubitemid 46557686)
19. Dominguez, D., Tournoy, J., Hartmann, D., Huth, T., Cryns, K., Deforce, S., Serneels, L., Camacho, I. E., Marjaux, E., Craessaerts, K., Roebroek, A. J., Schwake, M., D'Hooge, R., Bach, P., Kalinke, U., Moechars, D., Alzheimer, C., Reiss, K., Saftig, P., and De Strooper, B. (2005) Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice. J. Biol. Chem. 280, 30797-30806 (Pubitemid 41291810)
20. Harrison, S. M., Harper, A. J., Hawkins, J., Duddy, G., Grau, E., Pugh, P. L., Winter, P. H., Shilliam, C. S., Hughes, Z. A., Dawson, L. A., Gonzalez, M. I., Upton, N., Pangalos, M. N., and Dingwall, C. (2003) BACE1 (β-secretase) transgenic and knockout mice. Identification of neurochemical deficits and behavioral changes. Mol. Cell. Neurosci. 24, 646-655 (Pubitemid 37506009)
21. Ohno, M., Chang, L., Tseng, W., Oakley, H., Citron, M., Klein, W. L., Vassar, R., and Disterhoft, J. F. (2006) Temporal memory deficits in Alzheimer mouse models. Rescue by genetic deletion of BACE1. Eur. J. Neurosci. 23, 251-260
22. Ohno, M., Sametsky, E. A., Younkin, L. H., Oakley, H., Younkin, S. G., Citron, M., Vassar, R., and Disterhoft, J. F. (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer disease. Neuron 41, 27-33 (Pubitemid 38071826)
23. Savonenko, A. V., Melnikova, T., Laird, F. M., Stewart, K. A., Price, D. L., and Wong, P. C. (2008) Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc. Natl. Acad. Sci. U.S.A. 105, 5585-5590 (Pubitemid 351753906)
24. Hu, X., Hicks, C. W., He, W., Wong, P., Macklin, W. B., Trapp, B. D., and Yan, R. (2006) Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 9, 1520-1525 (Pubitemid 44862660)
25. Willem, M., Garratt, A. N., Novak, B., Citron, M., Kaufmann, S., Rittger, A., DeStrooper, B., Saftig, P., Birchmeier, C., and Haass, C. (2006) Control of peripheral nerve myelination by the β-secretase BACE1. Science 314, 664-666 (Pubitemid 44646394)
26. Zhang, X. M., Cai, Y., Xiong, K., Cai, H., Luo, X. G., Feng, J. C., Clough, R. W., Struble, R. G., Patrylo, P. R., and Yan, X. X. (2009) β-Secretase-1 elevation in transgenic mouse models of Alzheimer disease is associated with synaptic/axonal pathology and amyloidogenesis. Implications for neuritic plaque development. Eur. J. Neurosci. 30, 2271-2283
27. Lee, M. S., Kwon, Y. T., Li, M., Peng, J., Friedlander, R. M., and Tsai, L. H. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364 (Pubitemid 30337070)
28. Patrick, G. N., Zukerberg, L., Nikolic, M., de la Monte, S., Dikkes, P., and Tsai, L. H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622 (Pubitemid 129516324)
29. Cruz, J. C., Kim, D., Moy, L. Y., Dobbin, M. M., Sun, X., Bronson, R. T., and Tsai, L. H. (2006) p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid β in vivo. J. Neurosci. 26, 10536-10541 (Pubitemid 44564604)
30. Wen, Y., Planel, E., Herman, M., Figueroa, H. Y., Wang, L., Liu, L., Lau, L. F., Yu, W. H., and Duff, K. E. (2008) Interplay between cyclin-dependent kinase 5 and glycogen synthase kinase 3β mediated by neuregulin signaling leads to differential effects on Tau phosphorylation and amyloid precursor protein processing. J. Neurosci. 28, 2624-2632 (Pubitemid 351348188)
31. Wen, Y., Yu, W. H., Maloney, B., Bailey, J., Ma, J., Marié, I., Maurin, T., Wang, L., Figueroa, H., Herman, M., Krishnamurthy, P., Liu, L., Planel, E., Lau, L. F., Lahiri, D. K., and Duff, K. (2008) Transcriptional regulation of β-secretase by p25/cdk5 leads to enhanced amyloidogenic processing. Neuron 57, 680-690 (Pubitemid 351335351)
32. Louneva, N., Cohen, J. W., Han, L. Y., Talbot, K., Wilson, R. S., Bennett, D. A., Trojanowski, J. Q., and Arnold, S. E. (2008) Caspase-3 is enriched in postsynaptic densities and increased in Alzheimer disease. Am. J. Pathol. 173, 1488-1495
33. Selznick, L. A., Holtzman, D. M., Han, B. H., Gökden, M., Srinivasan, A. N., Johnson, E. M., Jr., and Roth, K. A. (1999) In situ immunodetection of neuronal caspase-3 activation in Alzheimer disease. J. Neuropathol. Exp. Neurol. 58, 1020-1026 (Pubitemid 29441930)
34. Stadelmann, C., Deckwerth, T. L., Srinivasan, A., Bancher, C., Brück, W., Jellinger, K., and Lassmann, H. (1999) Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer disease. Evidence for apoptotic cell death. Am. J. Pathol. 155, 1459-1466
35. Su, J. H., Zhao, M., Anderson, A. J., Srinivasan, A., and Cotman, C. W. (2001) Activated caspase-3 expression in Alzheimer and aged control brain. Correlation with Alzheimer pathology. Brain Res. 898, 350-357 (Pubitemid 32299965)
36. Tesco, G., Koh, Y. H., Kang, E. L., Cameron, A. N., Das, S., Sena-Esteves, M., Hiltunen, M., Yang, S. H., Zhong, Z., Shen, Y., Simpkins, J. W., and Tanzi, R. E. (2007) Depletion of GGA3 stabilizes BACE and enhances β-secretase activity. Neuron 54, 721-737 (Pubitemid 46843521)
37. Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet- Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., Berry, R., and Vassar, R. (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer disease mutations. Potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140 (Pubitemid 44527407)
38. Stine, W. B., Jr., Dahlgren, K. N., Krafft, G. A., and LaDu, M. J. (2003) In vitro characterization of conditions for amyloid-β peptide oligomerization and fibrillogenesis. J. Biol. Chem. 278, 11612-11622 (Pubitemid 36792723)
39. Tseng, H. C., Zhou, Y., Shen, Y., and Tsai, L. H. (2002) A survey of Cdk5 activator p35 and p25 levels in Alzheimer disease brains. FEBS Lett. 523, 58-62 (Pubitemid 34786058)
40. Borghi, R., Giliberto, L., Assini, A., Delacourte, A., Perry, G., Smith, M. A., Strocchi, P., Zaccheo, D., and Tabaton, M. (2002) Increase of cdk5 is related to neurofibrillary pathology in progressive supranuclear palsy. Neurology 58, 589-592 (Pubitemid 34164941)
41. Nguyen, K. C., Rosales, J. L., Barboza, M., and Lee, K. Y. (2002) Controversies over p25 in Alzheimer disease. J. Alzheimer's Dis. 4, 123-126
42. Takashima, A., Murayama, M., Yasutake, K., Takahashi, H., Yokoyama, M., and Ishiguro, K. (2001) Involvement of cyclin-dependent kinase5 activator p25 on Tau phosphorylation in mouse brain. Neurosci. Lett. 306, 37-40 (Pubitemid 32524292)
43. Tandon, A., Yu, H., Wang, L., Rogaeva, E., Sato, C., Chishti, M. A., Kawarai, T., Hasegawa, H., Chen, F., Davies, P., Fraser, P. E., Westaway, D., and St George-Hyslop, P. H. (2003) Brain levels of CDK5 activator p25 are not increased in Alzheimer or other neurodegenerative diseases with neurofibrillary tangles. J. Neurochem. 86, 572-581
44. Taniguchi, S., Fujita, Y., Hayashi, S., Kakita, A., Takahashi, H., Murayama, S., Saido, T. C., Hisanaga, S., Iwatsubo, T., and Hasegawa, M. (2001) Calpain- mediated degradation of p35 to p25 in postmortem human and rat brains. FEBS Lett. 489, 46-50 (Pubitemid 32176003)
45. Yoo, B. C., and Lubec, G. (2001) p25 protein in neurodegeneration. Nature 411, 763-764
46. Bennett, D. A., Schneider, J. A., Buchman, A. S., Mendes de Leon, C., Bienias, J. L., and Wilson, R. S. (2005) The Rush Memory and Aging Project. Study design and base-line characteristics of the study cohort. Neuroepidemiology 25, 163-175 (Pubitemid 41540657)
47. Lacor, P. N., Buniel, M. C., Chang, L., Fernandez, S. J., Gong, Y., Viola, K. L., Lambert, M. P., Velasco, P. T., Bigio, E. H., Finch, C. E., Krafft, G. A., and Klein, W. L. (2004) Synaptic targeting by Alzheimer-related amyloid βoligomers. J. Neurosci. 24, 10191-10200 (Pubitemid 39492046)
48. Lacor, P. N., Buniel, M. C., Furlow, P. W., Clemente, A. S., Velasco, P. T., Wood, M., Viola, K. L., and Klein, W. L. (2007) Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer disease. J. Neurosci. 27, 796-807 (Pubitemid 46174498)
49. Lambert, M. P., Velasco, P. T., Chang, L., Viola, K. L., Fernandez, S., Lacor, P. N., Khuon, D., Gong, Y., Bigio, E. H., Shaw, P., De Felice, F. G., Krafft, G. A., and Klein, W. L. (2007) Monoclonal antibodies that target pathological assemblies of Aβ. J. Neurochem. 100, 23-35 (Pubitemid 46085837)
50. Lesné, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M., and Ashe, K. H. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440, 352-357
51. Lesné, S., Kotilinek, L., and Ashe, K. H. (2008) Plaque-bearing mice with reduced levels of oligomeric amyloid-β assemblies have intact memory function. Neuroscience 151, 745-749
52. Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., and Sabatini, B. L. (2007) Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 27, 2866-2875 (Pubitemid 46438992)
53. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-βprotein dimers isolated directly from Alzheimer brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842
54. Snyder, E. M., Nong, Y., Almeida, C. G., Paul, S., Moran, T., Choi, E. Y., Nairn, A. C., Salter, M. W., Lombroso, P. J., Gouras, G. K., and Greengard, P. (2005) Regulation of NMDA receptor trafficking by amyloid-β. Nat. Neurosci. 8, 1051-1058 (Pubitemid 41061516)
55. Lee, M. S., Kao, S. C., Lemere, C. A., Xia, W., Tseng, H. C., Zhou, Y., Neve, R., Ahlijanian, M. K., and Tsai, L. H. (2003) APP processing is regulated by cytoplasmic phosphorylation. J. Cell Biol. 163, 83-95 (Pubitemid 37271436)
56. Zheng, Y. L., Li, B. S., Amin, N. D., Albers, W., and Pant, H. C. (2002) A peptide derived from cyclin-dependent kinase activator (p35) specifically inhibits Cdk5 activity and phosphorylation of Tau protein in transfected cells. Eur. J. Biochem. 269, 4427-4434
57. Kerokoski, P., Suuronen, T., Salminen, A., Soininen, H., and Pirttilä, T. (2001) The levels of cdk5 and p35 proteins and Tau phosphorylation are reduced during neuronal apoptosis. Biochem. Biophys. Res. Commun. 280, 998-1002 (Pubitemid 32924438)
58. Zempel, H., Thies, E., Mandelkow, E., and Mandelkow, E. M. (2010) Aßoligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J. Neurosci. 30, 11938-11950
59. Ma, Q. L., Yang, F., Rosario, E. R., Ubeda, O. J., Beech, W., Gant, D. J., Chen, P. P., Hudspeth, B., Chen, C., Zhao, Y., Vinters, H. V., Frautschy, S. A., and Cole, G. M. (2009) β-Amyloid oligomers induce phosphorylation of Tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling. Suppression by omega-3 fatty acids and curcumin. J. Neurosci. 29, 9078-9089
60. Yamin, G. (2009) NMDA receptor-dependent signaling pathways that underlie amyloid β-protein disruption of LTP in the hippocampus. J. Neurosci. Res. 87, 1729-1736
61. Mengesdorf, T., Jensen, P. H., Mies, G., Aufenberg, C., and Paschen, W. (2002) Down-regulation of Parkin protein in transient focal cerebral ischemia. A link between stroke and degenerative disease? Proc. Natl. Acad. Sci. U.S.A. 99, 15042-15047 (Pubitemid 35334606)
62. Sheng, J. G., Price, D. L., and Koliatsos, V. E. (2003) The β-amyloid-related proteins presenilin 1 and BACE1 are axonally transported to nerve terminals in the brain. Exp. Neurol. 184, 1053-1057 (Pubitemid 38182836)
63. Koffie, R. M., Meyer-Luehmann, M., Hashimoto, T., Adams, K. W., Mielke, M. L., Garcia-Alloza, M., Micheva, K. D., Smith, S. J., Kim, M. L., Lee, V. M., Hyman, B. T., and Spires-Jones, T. L. (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl. Acad. Sci. U.S.A. 106, 4012-4017
64. Jacobs, E. H., Williams, R. J., and Francis, P. T. (2006) Cyclin-dependent kinase 5, Munc18a, and Munc18-interacting protein 1/X11α protein upregulation in Alzheimer disease. Neuroscience 138, 511-522 (Pubitemid 43255561)