Phospho-eIF2α level is important for determining abilities of BACE1 reduction to rescue cholinergic neurodegeneration and memory defects in 5XFAD mice

PLoS ONE

Volumn 5, Issue 9, 2010, Pages

  Devi, Latha ^a   Ohno, Masuo ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; BETA SECRETASE 1; INITIATION FACTOR 2ALPHA; ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; INITIATION FACTOR 2; SECRETASE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE; CONTROLLED STUDY; GENE DELETION; GENE DOSAGE; HETEROZYGOTE; HIPPOCAMPUS; KNOCKOUT MOUSE; MAZE TEST; MEMORY DISORDER; MOUSE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; FEMALE; GENETICS; HUMAN; MALE; MEMORY; METABOLISM; MOUSE MUTANT; NERVE DEGENERATION; PATHOLOGY; PHOSPHORYLATION; PSYCHOLOGICAL ASPECT;

MUS; MUS MUSCULUS;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CHOLINERGIC FIBERS; DISEASE MODELS, ANIMAL; EUKARYOTIC INITIATION FACTOR-2; FEMALE; HUMANS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE DEGENERATION; PHOSPHORYLATION;

EID: 77958530620     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012974     Document Type: Article

References (60)

1. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-185.
2. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356.
3. Citron M (2004) β-Secretase inhibition for the treatment of Alzheimer's disease- promise and challenge. Trends Pharmacol Sci 25: 92-97.
4. Ohno M (2006) Genetic and pharmacological basis for therapeutic inhibition of β- and γ-secretases in mouse models of Alzheimer's memory deficits. Rev Neurosci 17: 429-454.
5. Ohno M (2008) β-Secretase as a prime therapeutic target for Alzheimer's disease: a perspective from mouse model studies. In: Araki W, ed. Recent Advances in the Biology of Secretases, Key Proteases in Alzheimer's Disease. Kerala: Research Signpost. pp 1-25.
6. Cole SL, Vassar R (2007) The Alzheimer's disease β-secretase enzyme, BACE1. Mol Neurodegener 2: 22.
7. Ohno M, Sametsky EA, Younkin LH, Oakley H, Younkin SG, et al. (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 41: 27-33.
8. Ohno M, Chang L, Tseng W, Oakley H, Citron M, et al. (2006) Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. Eur J Neurosci 23: 251-260.
9. Ohno M, Cole SL, Yasvoina M, Zhao J, Citron M, et al. (2007) BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice. Neurobiol Dis 26: 134-145.
10. Laird FM, Cai H, Savonenko AV, Farah MH, He K, et al. (2005) BACE1, a major determinant of selective vulnerability of the brain to amyloid-b amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J Neurosci 25: 11693-11709.
11. John V (2006) Human β-secretase (BACE) and BACE inhibitors: progress report. Curr Top Med Chem 6: 569-578.
12. Ghosh AK, Gemma S, Tang J (2008) β-Secretase as a therapeutic target for Alzheimer's disease. Neurotherapeutics 5: 399-408.
13. Hunt CE, Turner AJ (2009) Cell biology, regulation and inhibition of β-secretase (BACE-1). FEBS J 276: 1845-1859.
14. De Strooper B, Vassar R, Golde T (2010) The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 6: 99-107.
15. Frisardi V, Solfrizzi V, Imbimbo PB, Capurso C, D'Introno A, et al. (2010) Towards disease-modifying treatment of Alzheimer's disease: drugs targeting beta-amyloid. Curr Alzheimer Res 7: 40-55.
16. Hussain I, Hawkins J, Harrison D, Hille C, Wayne G, et al. (2007) Oral administration of a potent and selective non-peptidic BACE-1 inhibitor decreases β-cleavage of amyloid precursor protein and amyloid-β production in vivo. J Neurochem 100: 802-809.
17. Sankaranarayanan S, Holahan MA, Colussi D, Crouthamel MC, Devanarayan V, et al. (2009) First demonstration of cerebrospinal fluid and plasma Aβ lowering with oral administration of a β-site amyloid precursor protein-cleaving enzyme 1 inhibitor in nonhuman primates. J Pharmacol Exp Ther 328: 131-140.
18. Singer O, Marr RA, Rockenstein E, Crews L, Coufal NG, et al. (2005) Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat Neurosci 8: 1343-1349.
19. Chang WP, Downs D, Huang XP, Da H, Fung KM, et al. (2007) Amyloid-b reduction by memapsin 2 (β-secretase) immunization. FASEB J 21: 3184-3196.
20. McConlogue L, Buttini M, Anderson JP, Brigham EF, Chen KS, et al. (2007) Partial reduction of BACE1 has dramatic effects on Alzheimer plaque and synaptic pathology in APP transgenic mice. J Biol Chem 282: 26326-26334.
21. Devi L, Ohno M (2010) Genetic reductions of β-site amyloid precursor proteincleaving enzyme 1 and amyloid-β ameliorate impairment of conditioned taste aversion memory in 5XFAD Alzheimer's disease model mice. Eur J Neurosci 31: 110-118.
22. Kimura R, Devi L, Ohno M (2010) Partial reduction of BACE1 improves synaptic plasticity, recent and remote memories in Alzheimer's disease transgenic mice. J Neurochem 113: 248-261.
23. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC (2002) β-Secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59: 1381-1389.
24. Li R, Lindholm K, Yang LB, Yue X, Citron M, et al. (2004) Amyloid b peptide load is correlated with increased β-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 101: 3632-3637.
25. Yang LB, Lindholm K, Yan R, Citron M, Xia W, et al. (2003) Elevated bsecretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9: 3-4.
26. Zhao J, Fu Y, Yasvoina M, Shao P, Hitt B, et al. (2007) β-Site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J Neurosci 27: 3639-3649.
27. Ahmed RR, Holler CJ, Webb RL, Li F, Beckett TL, et al. (2010) BACE1 and BACE2 enzymatic activities in Alzheimer's disease. J Neurochem 112: 1045-1053.
28. Oakley H, Cole SL, Logan S, Maus E, Shao P, et al. (2006) Intraneuronal bamyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26: 10129-10140.
29. Kimura R, Ohno M (2009) Impairments in remote memory stabilization precede hippocampal synaptic and cognitive failures in 5XFAD Alzheimer mouse model. Neurobiol Dis 33: 229-235.
30. Ohno M (2009) Failures to reconsolidate memory in a mouse model of Alzheimer's disease. Neurobiol Learn Mem 92: 455-459.
31. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O (2010) Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Ab aggregation in the 5XFAD mouse model of Alzheimer's disease. Neurobiol Aging. In press.
32. Chang RC, Wong AK, Ng HK, Hugon J (2002) Phosphorylation of eukaryotic initiation factor-2a (eIF2a) is associated with neuronal degeneration in Alzheimer's disease. Neuroreport 13: 2429-2432.
33. O'Connor T, Sadleir KR, Maus E, Velliquette RA, Zhao J, et al. (2008) Phosphorylation of the translation initiation factor eIF2a increases BACE1 levels and promotes amyloidogenesis. Neuron 60: 988-1009.
34. Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26: 91-104.
35. Ohno M, Yamamoto T, Watanabe S (1992) Effects of intrahippocampal injections of N-methyl-D-aspartate receptor antagonists and scopolamine on working and reference memory assessed in rats by a three-panel runway task. J Pharmacol Exp Ther 263: 943-950.
36. Feasey-Truger KJ, Li BH, ten Bruggencate G (1992) Lesions of the medial septum which produce deficits in working/spatial memory do not impair longterm potentiation in the CA3 region of the rat hippocampus in vivo. Brain Res 591: 296-304.
37. Chang Q, Gold PE (2004) Impaired and spared cholinergic functions in the hippocampus after lesions of the medial septum/vertical limb of the diagonal band with 192 IgG-saporin. Hippocampus 14: 170-179.
38. Sarajarvi T, Haapasalo A, Viswanathan J, Makinen P, Laitinen M, et al. (2009) Down-regulation of seladin-1 increases BACE1 levels and activity through enhanced GGA3 depletion during apoptosis. J Biol Chem 284: 34433-34443.
39. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, et al. (2007) Depletion of GGA3 stabilizes BACE and enhances β-secretase activity. Neuron 54: 721-737.
40. Wen Y, Yu WH, Maloney B, Bailey J, Ma J, et al. (2008) Transcriptional regulation of β-secretase by p25/cdk5 leads to enhanced amyloidogenic processing. Neuron 57: 680-690.
41. Cruz JC, Kim D, Moy LY, Dobbin MM, Sun X, et al. (2006) p25/cyclindependent kinase 5 induces production and intraneuronal accumulation of amyloid b in vivo. J Neurosci 26: 10536-10541.
42. Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, et al. (2008) Loss of microRNA cluster miR-29a/β-1 in sporadic Alzheimer's disease correlates with increased BACE1/β-secretase expression. Proc Natl Acad Sci U S A 105: 6415-6420.
43. Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, et al. (2008) The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of β-site amyloid precursor protein-cleaving enzyme 1. J Neurosci 28: 1213-1223.
44. Zhang X-M, Cai Y, Xiong K, Cai H, Luo X-G, et al. (2009) β-Secretase-1 elevation in transgenic mouse models of Alzheimer's disease is associated with synaptic/axonal pathology and amyloidogenesis: implications for neuritic plaque development. Eur J Neurosci 30: 2271-2283.
45. Lee KW, Im JY, Song JS, Lee SH, Lee HJ, et al. (2006) Progressive neuronal loss and behavioral impairments of transgenic C57BL/6 inbred mice expressing the carboxy terminus of amyloid precursor protein. Neurobiol Dis 22: 10-24.
46. Nalbantoglu J, Tirado-Santiago G, Lahsaini A, Poirier J, Goncalves O, et al. (1997) Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387: 500-505.
47. Berger-Sweeney J, McPhie DL, Arters JA, Greenan J, Oster-Granite ML, et al. (1999) Impairments in learning and memory accompanied by neurodegeneration in mice transgenic for the carboxyl-terminus of the amyloid precursor protein. Brain Res Mol Brain Res 66: 150-162.
48. Song DK, Won MH, Jung JS, Lee JC, Kang TC, et al. (1998) Behavioral and neuropathologic changes induced by central injection of carboxyl-terminal fragment of β-amyloid precursor protein in mice. J Neurochem 71: 875-878.
49. Choi SH, Park CH, Koo JW, Seo JH, Kim HS, et al. (2001) Memory impairment and cholinergic dysfunction by centrally administered Ab and carboxyl-terminal fragment of Alzheimer's APP in mice. FASEB J 15: 1816-1818.
50. Contestabile A, Ciani E, Contestabile A (2008) The place of choline acetyltransferase activity measurement in the "cholinergic hypothesis" of neurodegenerative diseases. Neurochem Res 33: 318-327.
51. Bellucci A, Luccarini I, Scali C, Prosperi C, Giovannini MG, et al. (2006) Cholinergic dysfunction, neuronal damage and axonal loss in TgCRND8 mice. Neurobiol Dis 23: 260-272.
52. Christensen DZ, Bayer TA, Wirths O (2010) Intracellular Ab triggers neuron loss in the cholinergic system of the APP/PS1KI mouse model of Alzheimer's disease. Neurobiol Aging 31: 1153-1163.
53. Boncristiano S, Calhoun ME, Kelly PH, Pfeifer M, Bondolfi L, et al. (2002) Cholinergic changes in the APP23 transgenic mouse model of cerebral amyloidosis. J Neurosci 22: 3234-3243.
54. Perez SE, Dar S, Ikonomovic MD, DeKosky ST, Mufson EJ (2007) Cholinergic forebrain degeneration in the APPswe/PS1DE9 transgenic mouse. Neurobiol Dis 28: 3-15.
55. Fernandez de Sevilla D, Nunez A, Borde M, Malinow R, Buno W (2008) Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J Neurosci 28: 1469-1478.
56. Ovsepian SV, Anwyl R, Rowan MJ (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: in vivo study. Eur J Neurosci 20: 1267-1275.
57. Sanchez G, Alvares Lde O, Oberholzer MV, Genro B, Quillfeldt J, et al. (2009) M4 muscarinic receptors are involved in modulation of neurotransmission at synapses of Schaffer collaterals on CA1 hippocampal neurons in rats. J Neurosci Res 87: 691-700.
58. Shinoe T, Matsui M, Taketo MM, Manabe T (2005) Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25: 11194-11200.
59. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, et al. (2001) BACE1 is the major β-secretase for generation of Ab peptides by neurons. Nat Neurosci 4: 233-234.
60. Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates. New York: Academic Press.