Mechanisms that lessen benefits of β-secretase reduction in a mouse model of Alzheimer's disease

Translational Psychiatry

Volumn 3, Issue , 2013, Pages

  Devi, L ^a   Ohno, M ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

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

Author keywords

Amyloid; BACE1; ElF2 ; Learning and memory; Neprilysin; PERK

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE 1; INITIATION FACTOR 2ALPHA; MEMBRANE METALLOENDOPEPTIDASE; PROTEIN KINASE R; ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; SECRETASE;

ALZHEIMER DISEASE; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME MECHANISM; GENE DOSAGE; HAPLOINSUFFICIENCY; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CONDITIONED REFLEX; DISEASE MODEL; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; KNOCKOUT MOUSE; MEMORY DISORDER; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; DRUG ANTAGONISM;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BRAIN; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; HAPLOINSUFFICIENCY; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC;

EID: 84880529702     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.59     Document Type: Article

References (65)

1. Vassar R. The b-secretase, BACE: a prime drug target for Alzheimer's disease. J Mol Neurosci 2001; 17: 157-170.
2. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992; 256: 184-185.
3. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297: 353-356.
4. Ohno M. Genetic and pharmacological basis for therapeutic inhibition of β-and γ-secretases in mouse models of Alzheimer's memory deficits. Rev Neurosci 2006; 17: 429-454.
5. Ohno M. 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. Research Signpost: Kerala, India, 2008. pp 1-25.
6. Cole SL, Vassar R. The Alzheimer's disease β-secretase enzyme, BACE1. Mol Neurodegener 2007; 2: 22.
7. Vassar R, Kovacs DM, Yan R, Wong PC. The β-secretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J Neurosci 2009; 29: 12787-12794.
8. Ohno M, Sametsky EA, Younkin LH, Oakley H, Younkin SG, Citron M et al. BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 2004; 41: 27-33.
9. Ohno M, Chang L, Tseng W, Oakley H, Citron M, Klein WL et al. Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. Eur J Neurosci 2006; 23: 251-260.
10. Ohno M, Cole SL, Yasvoina M, Zhao J, Citron M, Berry R et al. BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice. Neurobiol Dis 2007; 26: 134-145.
11. Laird FM, Cai H, Savonenko AV, Farah MH, He K, Melnikova T et al. BACE1, a major determinant of selective vulnerability of the brain to amyloid-β amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J Neurosci 2005; 25: 11693-11709.
12. De Strooper B, Vassar R, Golde T. The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 2010; 6: 99-107.
13. Frisardi V, Solfrizzi V, Imbimbo PB, Capurso C, D'Introno A, Colacicco AM et al. Towards disease-modifying treatment of Alzheimer's disease: drugs targeting β-amyloid. Curr Alzheimer Res 2010; 7: 40-55.
14. Luo X, Yan R. Inhibition of BACE1 for therapeutic use in Alzheimer's disease. Int J Clin Exp Pathol 2010; 3: 618-628.
15. Chang WP, Koelsch G, Wong S, Downs D, Da H, Weerasena V et al. In vivo inhibition of Aβ production by memapsin 2 (β-secretase) inhibitors. J Neurochem 2004; 89: 1409-1416.
16. Hussain I, Hawkins J, Harrison D, Hille C, Wayne G, Cutler L et al. 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 2007; 100: 802-809.
17. Sankaranarayanan S, Holahan MA, Colussi D, Crouthamel MC, Devanarayan V, Ellis J et al. 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 2009; 328: 131-140.
18. Lerchner A, Machauer R, Betschart C, Veenstra S, Rueeger H, McCarthy C et al. Macrocyclic BACE-1 inhibitors acutely reduce Aβ in brain after po application. Bioorg Med Chem Lett 2010; 20: 603-607.
19. Jeppsson F, Eketjall S, Janson J, Karlstrom S, Gustavsson S, Olsson LL et al. Discovery of AZD3839, a potent and selective BACE1 clinical candidate for the treatment of Alzheimer disease. J Biol Chem 2012; 287: 41245-41257.
20. May PC, Dean RA, Lowe SL, Martenyi F, Sheehan SM, Boggs LN et al. Robust central reduction of amyloid-β in humans with an orally available, non-peptidic β-secretase inhibitor. J Neurosci 2011; 31: 16507-16516.
21. Takahashi H, Fukumoto H, Maeda R, Terauchi J, Kato K, Miyamoto M. Ameliorative effects of a non-competitive BACE1 inhibitor TAK-070 on Aβ peptide levels and impaired learning behavior in aged rats. Brain Res 2010; 1361: 146-156.
22. McConlogue L, Buttini M, Anderson JP, Brigham EF, Chen KS, Freedman SB et al. Partial reduction of BACE1 has dramatic effects on Alzheimer plaque and synaptic pathology in APP transgenic mice. J Biol Chem 2007; 282: 26326-26334.
23. Devi L, Ohno M. Genetic reductions of β-site amyloid precursor protein-cleaving enzyme 1 and amyloid-β ameliorate impairment of conditioned taste aversion memory in 5XFAD Alzheimer's disease model mice. Eur J Neurosci 2010; 31: 110-118.
24. Kimura R, Devi L, Ohno M. Partial reduction of BACE1 improves synaptic plasticity, recent and remote memories in Alzheimer's disease transgenic mice. J Neurochem 2010; 113: 248-261.
25. Devi L, Ohno M. Phospho-eIF2a level is important for determining abilities of BACE1 reduction to rescue cholinergic neurodegeneration and memory defects in 5XFAD mice. PLoS One 2010; 5: e12974.
26. Devi L, Ohno M. Mitochondrial dysfunction and accumulation of the β-secretase-cleaved C-terminal fragment of APP in Alzheimer's disease transgenic mice. Neurobiol Dis 2012; 45: 417-424.
27. Chabrier MA, Blurton-Jones M, Agazaryan AA, Nerhus JL, Martinez-Coria H, LaFerla FM. Soluble Aβ promotes wild-type tau pathology in vivo. J Neurosci 2012; 32: 17345-17350.
28. Fukumoto H, Takahashi H, Tarui N, Matsui J, Tomita T, Hirode M et al. A noncompetitive BACE1 inhibitor TAK-070 ameliorates Aβ pathology and behavioral deficits in a mouse model of Alzheimer's disease. J Neurosci 2010; 30: 11157-11166.
29. Chang WP, Huang X, Downs D, Cirrito JR, Koelsch G, Holtzman DM et al. β-Secretase inhibitor GRL-8234 rescues age-related cognitive decline in APP transgenic mice. FASEB J 2011; 25: 775-784.
30. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J et al. Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 2006; 26: 10129-10140.
31. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL et al. BACE1 is the major bsecretase for generation of Aβ peptides by neurons. Nat Neurosci 2001; 4: 233-234.
32. Zhao J, Fu Y, Yasvoina M, Shao P, Hitt B, O'Connor T et al. β-Site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J Neurosci 2007; 27: 3639-3649.
33. Zhang X-M, Cai Y, Xiong K, Cai H, Luo X-G, Feng J-C et al. 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 2009; 30: 2271-2283.
34. Ohno M, Frankland PW, Chen AP, Costa RM, Silva AJ. Inducible, pharmacogenetic approaches to the study of learning and memory. Nat Neurosci 2001; 4: 1238-1243.
35. Kimura R, Ohno M. Impairments in remote memory stabilization precede hippocampal synaptic and cognitive failures in 5XFAD Alzheimer mouse model. Neurobiol Dis 2009; 33: 229-235.
36. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 3rd edn Academic Press: New York, USA, 2008.
37. Devi L, Alldred MJ, Ginsberg SD, Ohno M. Sex-and brain region-specific acceleration of bamyloidogenesis following behavioral stress in a mouse model of Alzheimer's disease. Mol Brain 2010; 3: 34.
38. Ohno M. Failures to reconsolidate memory in a mouse model of Alzheimer's disease. Neurobiol Learn Mem 2009; 92: 455-459.
39. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O. Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer's disease. Neurobiol Aging 2012; 33: 196.e129-196.e140.
40. Fanselow MS. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 2000; 110: 73-81.
41. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 2001; 24: 897-931.
42. Chang RC, Wong AK, Ng HK, Hugon J. Phosphorylation of eukaryotic initiation factor-2a (eIF2a) is associated with neuronal degeneration in Alzheimer's disease. Neuro Report 2002; 13: 2429-2432.
43. O'Connor T, Sadleir KR, Maus E, Velliquette RA, Zhao J, Cole SL et al. Phosphorylation of the translation initiation factor eIF2α increases BACE1 levels and promotes amyloidogenesis. Neuron 2008; 60: 988-1009.
44. Mouton-Liger F, Paquet C, Dumurgier J, Bouras C, Pradier L, Gray F et al. Oxidative stress increases BACE1 protein levels through activation of the PKR-eIF2α pathway. Biochim Biophys Acta 2012; 1822: 885-896.
45. Devi L, Alldred MJ, Ginsberg SD, Ohno M. Mechanisms underlying insulin deficiencyinduced acceleration of β-amyloidosis in a mouse model of Alzheimer's disease. PLoS One 2012; 7: e32792.
46. Wang S, Wang R, Chen L, Bennett DA, Dickson DW, Wang DS. Expression and functional profiling of neprilysin, insulin-degrading enzyme, and endothelin-converting enzyme in prospectively studied elderly and Alzheimer's brain. J Neurochem 2010; 115: 47-57.
47. Puzzo D, Privitera L, Leznik E, Fa M, Staniszewski A, Palmeri A et al. Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J Neurosci 2008; 28: 14537-14545.
48. Puzzo D, Privitera L, Fa M, Staniszewski A, Hashimoto G, Aziz F et al. Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann Neurol 2011; 69: 819-830.
49. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD et al. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006; 9: 1520-1525.
50. Savonenko AV, Melnikova T, Laird FM, Stewart KA, Price DL, Wong PC. Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc Natl Acad Sci USA 2008; 105: 5585-5590.
51. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC. β-Secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 2002; 59: 1381-1389.
52. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G. Increased expression of the amyloid precursor β-secretase in Alzheimer's disease. Ann Neurol 2002; 51: 783-786.
53. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL et al. Elevated β-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 2003; 9: 3-4.
54. Saido TC, Leissring MA. Proteolytic degradation of amyloid-β protein. In Selkoe DJ, Mandelkow E, Holtzman DM (eds) The Biology of Alzheimer Disease. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, USA, 2012. pp 387-404.
55. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC et al. Decreased clearance of CNS β-amyloid in Alzheimer's disease. Science 2010; 330: 1774.
56. Huang SM, Mouri A, Kokubo H, Nakajima R, Suemoto T, Higuchi M et al. Neprilysinsensitive synapse-associated amyloid-β peptide oligomers impair neuronal plasticity and cognitive function. J Biol Chem 2006; 281: 17941-17951.
57. Farris W, Schutz SG, Cirrito JR, Shankar GM, Sun X, George A et al. Loss of neprilysin function promotes amyloid plaque formation and causes cerebral amyloid angiopathy. Am J Pathol 2007; 171: 241-251.
58. Leroy K, Ando K, Laporte V, Dedecker R, Suain V, Authelet M et al. Lack of tau proteins rescues neuronal cell death and decreases amyloidogenic processing of APP in APP/PS1 mice. Am J Pathol 2012; 181: 1928-1940.
59. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X et al. Enhanced proteolysis of β-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 2003; 40: 1087-1093.
60. Meilandt WJ, Cisse M, Ho K, Wu T, Esposito LA, Scearce-Levie K et al. Neprilysin overexpression inhibits plaque formation but fails to reduce pathogenic Aβ oligomers and associated cognitive deficits in human amyloid precursor protein transgenic mice. J Neurosci 2009; 29: 1977-1986.
61. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, Rittger A et al. Control of peripheral nerve myelination by the β-secretase BACE1. Science 2006; 314: 664-666.
62. Wang H, Song L, Laird F, Wong PC, Lee HK. BACE1 knock-outs display deficits in activitydependent potentiation of synaptic transmission at mossy fiber to CA3 synapses in the hippocampus. J Neurosci 2008; 28: 8677-8681.
63. Cai J, Qi X, Kociok N, Skosyrski S, Emilio A, Ruan Q et al. β-Secretase (BACE1) inhibition causes retinal pathology by vascular dysregulation and accumulation of age pigment. EMBO Mol Med 2012; 4: 980-991.
64. -/- mice exhibit seizure activity that does not correlate with sodium channel level or axonal localization. Mol Neurodegener 2010; 5: 31.
65. Rajapaksha TW, Eimer WA, Bozza TC, Vassar R. The Alzheimer's β-secretase enzyme BACE1 is required for accurate axon guidance of olfactory sensory neurons and normal glomerulus formation in the olfactory bulb. Mol Neurodegener 2011; 6: 88.