Phenylbutyric acid reduces amyloid plaques and rescues cognitive behavior in AD transgenic mice

Aging Cell

Volumn 10, Issue 3, 2011, Pages 418-428

  Wiley, Jesse C ^a   Pettan Brewer, Christina ^a   Ladiges, Warren C ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Alzheimer's disease; Endoplasmic reticulum; Molecular chaperone; Phenylbutyric acid; Radial water maze paradigm; Secretase

Indexed keywords

ADAM10 ENDOPEPTIDASE; AMYLOID BETA PROTEIN; BUTYRIC ACID DERIVATIVE; CHAPERONE; CHLOROTRIANISENE; DRINKING WATER; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; PHENYLBUTYRIC ACID; SECRETASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BRAIN CORTEX; COGNITION; CONTROLLED STUDY; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MOLECULAR MECHANICS; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SECRETION; PROTEIN SYNTHESIS; SPATIAL MEMORY; TRANSGENIC MOUSE; TREATMENT DURATION; WILD TYPE;

ADAM PROTEINS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; COGNITION; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; MICE; MICE, TRANSGENIC; NEURONS; NOOTROPIC AGENTS; PHENYLBUTYRATES; PLAQUE, AMYLOID; RECEPTORS, IONOTROPIC GLUTAMATE; RECEPTORS, METABOTROPIC GLUTAMATE;

MUS; MUS MUSCULUS;

EID: 79955979595     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00680.x     Document Type: Article

References (53)

1. de Almeida SF, Picarote G, Fleming JV, Carmo-Fonseca M, Azevedo JE, de Sousa M (2007) Chemical chaperones reduce endoplasmic reticulum stress and prevent mutant HFE aggregate formation. J. Biol. Chem. 282, 27905-27912.
2. Baek SH, Ohgi KA, Rose DW, Koo EH, Glass CK, Rosenfeld MG (2002) Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 110, 55-67.
3. Bentahir M, Nyabi O, Verhamme J, Tolia A, Horre K, Wiltfang J, Esselmann H, De Strooper B (2006) Presenilin clinical mutations can affect gamma-secretase activity by different mechanisms. J. Neurochem. 96, 732-742.
4. Bird TD (2008) Genetic aspects of Alzheimer disease. Genet. Med. 10, 231-239.
5. Cao X, Sudhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120.
6. Chafekar SM, Hoozemans JJ, Zwart R, Baas F, Scheper W (2007) Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid. Redox Signal. 9, 2245-2254.
7. Chafekar SM, Zwart R, Veerhuis R, Vanderstichele H, Baas F, Scheper W (2008) Increased Abeta1-42 production sensitizes neuroblastoma cells for ER stress toxicity. Curr. Alzheimer Res. 5, 469-474.
8. Costa RO, Ferreiro E, Cardoso SM, Oliveira CR, Pereira CM (2010) ER stress-mediated apoptotic pathway induced by Abeta peptide requires the presence of functional mitochondria. J. Alzheimers Dis. 20, 625-636.
9. Dries DR, Yu G (2008) Assembly, maturation, and trafficking of the gamma-secretase complex in Alzheimer's disease. Curr Alzheimer Res. 5, 132-146.
10. Filali M, Lalonde R (2009) Age-related cognitive decline and nesting behavior in an APPswe/PS1 bigenic model of Alzheimer's disease. Brain Res. 1292, 93-99.
11. Grutzendler J, Helmin K, Tsai J, Gan WB (2007) Various dendritic abnormalities are associated with fibrillar amyloid deposits in Alzheimer's disease. Ann. N Y Acad. Sci. 1097, 30-39.
12. Hebert SS, Serneels L, Tolia A, Craessaerts K, Derks C, Filippov MA, Muller U, De Strooper B (2006) Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes. EMBO Rep. 7, 739-745.
13. Herreman A, Van Gassen G, Bentahir M, Nyabi O, Craessaerts K, Mueller U, Annaert W, De Strooper B (2003) gamma-Secretase activity requires the presenilin-dependent trafficking of nicastrin through the Golgi apparatus but not its complex glycosylation. J. Cell Sci. 116, 1127-1136.
14. Hoozemans JJ, Veerhuis R, Van Haastert ES, Rozemuller JM, Baas F, Eikelenboom P, Scheper W (2005) The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol (Berl). 110, 165-172.
15. Hoozemans JJ, van Haastert ES, Nijholt DA, Rozemuller AJ, Eikelenboom P, Scheper W (2009) The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus. Am. J. Pathol. 174, 1241-1251.
16. Katayama T, Imaizumi K, Sato N, Miyoshi K, Kudo T, Hitomi J, Morihara T, Yoneda T, Gomi F, Mori Y, Nakano Y, Takeda J, Tsuda T, Itoyama Y, Murayama O, Takashima A, St George-Hyslop P, Takeda M, Tohyama M (1999) Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat. Cell Biol. 1, 479-485.
17. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rumbaugh G (2009) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35, 870-880.
18. Kim J, Kleizen B, Choy R, Thinakaran G, Sisodia SS, Schekman RW (2007) Biogenesis of gamma-secretase early in the secretory pathway. J. Cell Biol. 179, 951-963.
19. Kinoshita A, Fukumoto H, Shah T, Whelan CM, Irizarry MC, Hyman BT (2003) Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes. J. Cell Sci. 116, 3339-3346.
20. Kumar-Singh S, Theuns J, Van Broeck B, Pirici D, Vennekens K, Corsmit E, Cruts M, Dermaut B, Wang R, Van Broeckhoven C (2006) Mean age-of-onset of familial alzheimer disease caused by presenilin mutations correlates with both increased Abeta42 and decreased Abeta40. Hum. Mutat. 27, 686-695.
21. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, Viola KL, Klein WL (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 27, 796-807.
22. Lee do Y, Lee KS, Lee HJ, Kim do H, Noh YH, Yu K, Jung HY, Lee SH, Lee JY, Youn YC, Jeong Y, Kim DK, Lee WB, Kim SS (2010) Activation of PERK signaling attenuates Abeta-mediated ER stress. PLoS ONE 5, e10489.
23. Leuba G, Vernay A, Zimmermann V, Saini K, Kraftsik R, Savioz A (2009) Differential damage in the frontal cortex with aging, sporadic and familial Alzheimer's disease. Brain Res. Bull. 80, 196-202.
24. Liang WS, Reiman EM, Valla J, Dunckley T, Beach TG, Grover A, Niedzielko TL, Schneider LE, Mastroeni D, Caselli R, Kukull W, Morris JC, Hulette CM, Schmechel D, Rogers J, Stephan DA (2008) Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. USA 105, 4441-4446.
25. Lippa CF, Saunders AM, Smith TW, Swearer JM, Drachman DA, Ghetti B, Nee L, Pulaski-Salo D, Dickson D, Robitaille Y, Bergeron C, Crain B, Benson MD, Farlow M, Hyman BT, George-Hyslop SP, Roses AD, Pollen DA (1996) Familial and sporadic Alzheimer's disease: neuropathology cannot exclude a final common pathway. Neurology 46, 406-412.
26. Liu Q, Zerbinatti CV, Zhang J, Hoe HS, Wang B, Cole SL, Herz J, Muglia L, Bu G (2007) Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1. Neuron 56, 66-78.
27. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140.
28. Pardossi-Piquard R, Petit A, Kawarai T, Sunyach C, Alves da Costa C, Vincent B, Ring S, D'Adamio L, Shen J, Muller U, St George Hyslop P, Checler F (2005) Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46, 541-554.
29. Piccini A, Fassio A, Pasqualetto E, Vitali A, Borghi R, Palmieri D, Nacmias B, Sorbi S, Sitia R, Tabaton M (2004) Fibroblasts from FAD-linked presenilin 1 mutations display a normal unfolded protein response but overproduce Abeta42 in response to tunicamycin. Neurobiol. Dis. 15, 380-386.
30. Postina R, Schroeder A, Dewachter I, Bohl J, Schmitt U, Kojro E, Prinzen C, Endres K, Hiemke C, Blessing M, Flamez P, Dequenne A, Godaux E, van Leuven F, Fahrenholz F (2004) A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113, 1456-1464.
31. Ramirez-Lugo L, Jensen MS, Soderman A, West MJ (2009) Deficits in aversive but not in safe taste memory in the APPswe/PS1dE9 mice. J. Alzheimers Dis. 18, 281-293.
32. Reiserer RS, Harrison FE, Syverud DC, McDonald MP (2007) Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav. 6, 54-65.
33. Ricobaraza A, Cuadrado-Tejedor M, Perez-Mediavilla A, Frechilla D, Del Rio J, Garcia-Osta A (2009) Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34, 1721-1732.
34. Sato N, Urano F, Yoon Leem J, Kim SH, Li M, Donoviel D, Bernstein A, Lee AS, Ron D, Veselits ML, Sisodia SS, Thinakaran G (2000) Upregulation of BiP and CHOP by the unfolded-protein response is independent of presenilin expression. Nat. Cell Biol. 2, 863-870.
35. Scheper W, Hoozemans JJ (2009) Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Curr. Med. Chem. 16, 615-626.
36. Schlondorff J, Becherer JD, Blobel CP (2000) Intracellular maturation and localization of the tumour necrosis factor alpha convertase (TACE). Biochem J. 347(Pt 1), 131-138.
37. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat. Res. 569, 29-63.
38. Schroeder A, Fahrenholz F, Schmitt U (2009) Effect of a dominant-negative form of ADAM10 in a mouse model of Alzheimer's disease. J Alzheimers Dis. 16, 309-314.
39. Selkoe DJ, Podlisny MB (2002) Deciphering the genetic basis of Alzheimer's disease. Annu. Rev. Genomics Hum. Genet. 3, 67-99.
40. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842.
41. Shen J, Kelleher RJ 3rd (2007) The presenilin hypothesis of Alzheimer's disease: evidence for a loss-of-function pathogenic mechanism. Proc. Natl. Acad. Sci. USA 104, 403-409.
42. Smith DL, Pozueta J, Gong B, Arancio O, Shelanski M (2009) Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl. Acad. Sci. USA 106, 16877-16882.
43. Spires-Jones TL, Meyer-Luehmann M, Osetek JD, Jones PB, Stern EA, Bacskai BJ, Hyman BT (2007) Impaired spine stability underlies plaque-related spine loss in an Alzheimer's disease mouse model. Am. J. Pathol. 171, 1304-1311.
44. Tan MG, Chua WT, Esiri MM, Smith AD, Vinters HV, Lai MK (2009) Genome wide profiling of altered gene expression in the neocortex of Alzheimer's disease. J. Neurosci. Res. 88, 1157-1169.
45. Unterberger U, Hoftberger R, Gelpi E, Flicker H, Budka H, Voigtlander T (2006) Endoplasmic reticulum stress features are prominent in Alzheimer disease but not in prion diseases in vivo. J. Neuropathol. Exp. Neurol. 65, 348-357.
46. Volianskis A, Kostner R, Molgaard M, Hass S, Jensen MS (2008) Episodic memory deficits are not related to altered glutamatergic synaptic transmission and plasticity in the CA1 hippocampus of the APPswe/PS1DeltaE9-deleted transgenic mice model of beta-amyloidosis. Neurobiol. Aging 31, 1173-1187.
47. Wiley JC, Hudson M, Kanning KC, Schecterson LC, Bothwell M (2005) Familial Alzheimer's disease mutations inhibit gamma-secretase-mediated liberation of beta-amyloid precursor protein carboxy-terminal fragment. J. Neurochem. 94, 1189-1201.
48. Wiley JC, Meabon JS, Frankowski H, Smith EA, Schecterson LC, Bothwell M, Ladiges WC (2010) Phenylbutyric acid rescues endoplasmic reticulum stress-induced suppression of APP proteolysis and prevents apoptosis in neuronal cells. PLoS ONE 5, e9135.
49. Wolfe MS (2007) When loss is gain: reduced presenilin proteolytic function leads to increased Abeta42/Abeta40. Talking point on the role of presenilin mutations in Alzheimer disease. EMBO Rep. 8, 136-140.
50. Yam GH, Gaplovska-Kysela K, Zuber C, Roth J (2007) Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Invest. Ophthalmol. Vis. Sci. 48, 1683-1690.
51. Yang DS, Tandon A, Chen F, Yu G, Yu H, Arawaka S, Hasegawa H, Duthie M, Schmidt SD, Ramabhadran TV, Nixon RA, Mathews PM, Gandy SE, Mount HT, St George-Hyslop P, Fraser PE (2002) Mature glycosylation and trafficking of nicastrin modulate its binding to presenilins. J. Biol. Chem. 277, 28135-28142.
52. Yasuda Y, Kudo T, Katayama T, Imaizumi K, Yatera M, Okochi M, Yamamori H, Matsumoto N, Kida T, Fukumori A, Okumura M, Tohyama M, Takeda M (2002) FAD-linked presenilin-1 mutants impede translation regulation under ER stress. Biochem. Biophys. Res. Commun. 296, 313-318.
53. Zhang YW, Wang R, Liu Q, Zhang H, Liao FF, Xu H (2007) Presenilin/gamma-secretase-dependent processing of beta-amyloid precursor protein regulates EGF receptor expression. Proc. Natl. Acad. Sci. USA 104, 10613-10618.