HDAC3 negatively regulates spatial memory in a mouse model of Alzheimer's disease

Aging Cell

Volumn 16, Issue 5, 2017, Pages 1073-1082

  Zhu, Xiaolei ^a,b,c   Wang, Sulei ^d   Yu, Linjie ^a   Jin, Jiali ^a   Ye, Xing ^a   Liu, Yi ^a   Xu, Yun ^a,b,c  

^a NANJING UNIVERSITY   (China)

^b MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^c Nanjing Neuropsychiatry Clinic Medical Center   (China)

^d Nanjing Hospital of Traditional Chinese Medicine   (China)

Author keywords

Alzheimer's disease; beta amyloid; histone deacetylase3; spatial memory

Indexed keywords

ADAM10 ENDOPEPTIDASE; AMYLOID BETA PROTEIN; AMYLOID PROTEIN; BETA SECRETASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; C99 PROTEIN; CATHEPSIN B; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 8; IBA1 PROTEIN; LAMIN B; PEN2 PROTEIN; PROTEIN; SHORT HAIRPIN RNA; SYNAPTOPHYSIN; TAU PROTEIN; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; ACRYLAMIDE DERIVATIVE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; MAPT PROTEIN, MOUSE; PHENYLENEDIAMINE DERIVATIVE; RGFP966;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL NUCLEUS; DENDRITIC SPINE; GLIA; HIPPOCAMPUS; MICROGLIA; MORRIS WATER MAZE TEST; MOUSE; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPATIAL MEMORY; WESTERN BLOTTING; WILD TYPE MOUSE; ANIMAL; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; HUMAN; LENTIVIRUS; MAZE TEST; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ACRYLAMIDES; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL NUCLEUS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GENETIC VECTORS; HIPPOCAMPUS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; LENTIVIRUS; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENYLENEDIAMINES; PHOSPHORYLATION; PLAQUE, AMYLOID; TAU PROTEINS;

EID: 85026638988     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12642     Document Type: Article

References (42)

1. Adikesavan AK, Karmakar S, Pardo P, Wang L, Liu S, Li W, Smith CL (2014) Activation of p53 transcriptional activity by SMRT: a histone deacetylase 3-independent function of a transcriptional corepressor. Mol. Cell. Biol. 34, 1246–1261.
2. Alzheimer's A (2015) 2015 Alzheimer's disease facts and figures. Alzheimers Dement. 11, 332–384.
3. Anderson KW, Chen J, Wang M, Mast N, Pikuleva IA, Turko IV (2015) Quantification of histone deacetylase isoforms in human frontal cortex, human retina, and mouse brain. PLoS ONE 10, e0126592.
4. Bardai FH, D'Mello SR (2011) Selective toxicity by HDAC3 in neurons: regulation by Akt and GSK3beta. J. Neurosci. 31, 1746–1751.
5. Benito E, Urbanke H, Ramachandran B, Barth J, Halder R, Awasthi A, Jain G, Capece V, Burkhardt S, Navarro-Sala M, Nagarajan S, Schutz AL, Johnsen SA, Bonn S, Luhrmann R, Dean C, Fischer A (2015) HDAC inhibitor-dependent transcriptome and memory reinstatement in cognitive decline models. J. Clin. Investig. 125, 3572–3584.
6. Bieszczad KM, Bechay K, Rusche JR, Jacques V, Kudugunti S, Miao W, Weinberger NM, McGaugh JL, Wood MA (2015) Histone deacetylase inhibition via RGFP966 releases the brakes on sensory cortical plasticity and the specificity of memory formation. J. Neurosci. 35, 13124–13132.
7. Broide RS, Redwine JM, Aftahi N, Young W, Bloom FE, Winrow CJ (2007) Distribution of histone deacetylases 1-11 in the rat brain. J. Mol. Neurosci. 31, 47–58.
8. Calsolaro V, Edison P (2016) Neuroinflammation in Alzheimer's disease: current evidence and future directions. Alzheimers Dement. 12, 719–732.
9. Duvic M, Dimopoulos M (2016) The safety profile of vorinostat (suberoylanilide hydroxamic acid) in hematologic malignancies: a review of clinical studies. Cancer Treat. Rev. 43, 58–66.
10. Escaffit F, Vaute O, Chevillard-Briet M, Segui B, Takami Y, Nakayama T, Trouche D (2007) Cleavage and cytoplasmic relocalization of histone deacetylase 3 are important for apoptosis progression. Mol. Cell. Biol. 27, 554–567.
11. Francis YI, Fa M, Ashraf H, Zhang H, Staniszewski A, Latchman DS, Arancio O (2009) Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer's disease. J. Alzheimers Dis. 18, 131–139.
12. Graff J, Rei D, Guan JS, Wang WY, Seo J, Hennig KM, Nieland TJ, Fass DM, Kao PF, Kahn M, Su SC, Samiei A, Joseph N, Haggarty SJ, Delalle I, Tsai LH (2012) An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 483, 222–226.
13. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JS, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert JC, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St George-Hyslop P, Singleton A, Hardy J, Alzheimer Genetic Analysis G. (2013) TREM2 variants in Alzheimer's disease. N. Engl. J. Med. 368, 117–127.
14. Herms J, Dorostkar MM (2016) Dendritic spine pathology in neurodegenerative diseases. Annu. Rev. Pathol. 11, 221–250.
15. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 13, 159–170.
16. Jiao F, Hu H, Han T, Zhuo M, Yuan C, Yang H, Wang L, Wang L (2016) Aberrant expression of nuclear HDAC3 and cytoplasmic CDH1 predict a poor prognosis for patients with pancreatic cancer. Oncotarget 7, 16505–16516.
17. Jonsson T, Stefansson H, Steinberg S, Jonsdottir I, Jonsson PV, Snaedal J, Bjornsson S, Huttenlocher J, Levey AI, Lah JJ, Rujescu D, Hampel H, Giegling I, Andreassen OA, Engedal K, Ulstein I, Djurovic S, Ibrahim-Verbaas C, Hofman A, Ikram MA, van Duijn CM, Thorsteinsdottir U, Kong A, Stefansson K (2013) Variant of TREM2 associated with the risk of Alzheimer's disease. N. Engl. J. Med. 368, 107–116.
18. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rumbaugh G (2010) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35, 870–880.
19. Krishna K, Behnisch T, Sajikumar S (2016) Inhibition of histone deacetylase 3 restores amyloid-beta oligomer-induced plasticity deficit in hippocampal CA1 pyramidal neurons. J. Alzheimer's Dis. 51, 783–791.
20. Lai MT, Chen E, Crouthamel MC, DiMuzio-Mower J, Xu M, Huang Q, Price E, Register RB, Shi XP, Donoviel DB, Bernstein A, Hazuda D, Gardell SJ, Li YM (2003) Presenilin-1 and presenilin-2 exhibit distinct yet overlapping gamma-secretase activities. J. Biol. Chem. 278, 22475–22481.
21. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, Carreiro S, Rusche JR, Wood MA (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc. Natl Acad. Sci. USA 110, 2647–2652.
22. McQuown SC, Wood MA (2011) HDAC3 and the molecular brake pad hypothesis. Neurobiol. Learn. Mem. 96, 27–34.
23. McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, Alenghat T, Mullican SE, Jones S, Rusche JR, Lazar MA, Wood MA (2011) HDAC3 is a critical negative regulator of long-term memory formation. J. Neurosci. 31, 764–774.
24. Miners JS, Barua N, Kehoe PG, Gill S, Love S (2011) Abeta-degrading enzymes: potential for treatment of Alzheimer disease. J. Neuropathol. Exp. Neurol. 70, 944–959.
25. Narayan PJ, Lill C, Faull R, Curtis MA, Dragunow M (2015) Increased acetyl and total histone levels in post-mortem Alzheimer's disease brain. Neurobiol. Dis. 74, 281–294.
26. Peixoto L, Abel T (2013) The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 38, 62–76.
27. Puzzo D, Lee L, Palmeri A, Calabrese G, Arancio O (2014) Behavioral assays with mouse models of Alzheimer's disease: practical considerations and guidelines. Biochem. Pharmacol. 88, 450–467.
28. Qing H, He G, Ly PT, Fox CJ, Staufenbiel M, Cai F, Zhang Z, Wei S, Sun X, Chen CH, Zhou W, Wang K, Song W (2008) Valproic acid inhibits Abeta production, neuritic plaque formation, and behavioral deficits in Alzheimer's disease mouse models. J. Exp. Med. 205, 2781–2789.
29. Rumbaugh G, Sillivan SE, Ozkan ED, Rojas CS, Hubbs CR, Aceti M, Kilgore M, Kudugunti S, Puthanveettil SV, Sweatt JD, Rusche J, Miller CA (2015) Pharmacological selectivity within class I histone deacetylases predicts effects on synaptic function and memory rescue. Neuropsychopharmacology 40, 2307–2316.
30. Selkoe DJ (2013) SnapShot: pathobiology of Alzheimer's disease. Cell 154, 468–468 e461.
31. Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol. Med. 8, 595–608.
32. Sharma M, Shetty MS, Arumugam TV, Sajikumar S (2015) Histone deacetylase 3 inhibition re-establishes synaptic tagging and capture in aging through the activation of nuclear factor kappa B. Sci. Rep. 5, 16616.
33. Spangenberg EE, Lee RJ, Najafi AR, Rice RA, Elmore MR, Blurton-Jones M, West BL, Green KN (2016) Eliminating microglia in Alzheimer's mice prevents neuronal loss without modulating amyloid-beta pathology. Brain 139, 1265–1281.
34. Sun Z, Feng D, Fang B, Mullican SE, You SH, Lim HW, Everett LJ, Nabel CS, Li Y, Selvakumaran V, Won KJ, Lazar MA (2013) Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol. Cell 52, 769–782.
35. Wang S, Yu L, Yang H, Li C, Hui Z, Xu Y, Zhu X (2016) Oridonin attenuates synaptic loss and cognitive deficits in an Abeta1-42-induced mouse model of Alzheimer's disease. PLoS ONE 11, e0151397.
36. Xia M, Zhao Q, Zhang H, Chen Y, Yuan Z, Xu Y, Zhang M (2017) Proteomic analysis of HDAC3 selective inhibitor in the regulation of inflammatory response of primary microglia. Neural. Plast. 2017, 6237351.
37. Yang WM, Tsai SC, Wen YD, Fejer G, Seto E (2002) Functional domains of histone deacetylase-3. J. Biol. Chem. 277, 9447–9454.
38. Yang W, Chauhan A, Mehta S, Mehta P, Gu F, Chauhan V (2014) Trichostatin A increases the levels of plasma gelsolin and amyloid beta-protein in a transgenic mouse model of Alzheimer's disease. Life Sci. 99, 31–36.
39. You SH, Lim HW, Sun Z, Broache M, Won KJ, Lazar MA (2013) Nuclear receptor co-repressors are required for the histone-deacetylase activity of HDAC3 in vivo. Nat. Struct. Mol. Biol. 20, 182–187.
40. Youmans KL, Leung S, Zhang J, Maus E, Baysac K, Bu G, Vassar R, Yu C, LaDu MJ (2011) Amyloid-beta42 alters apolipoprotein E solubility in brains of mice with five familial AD mutations. J. Neurosci. Methods 196, 51–59.
41. Zhao H, Wang SL, Qian L, Jin JL, Li H, Xu Y, Zhu XL (2013) Diammonium glycyrrhizinate attenuates Abeta(1-42) -induced neuroinflammation and regulates MAPK and NF-kappaB pathways in vitro and in vivo. CNS Neurosci. Ther. 19, 117–124.
42. Zhu X, Wang S, Yu L, Yang H, Tan R, Yin K, Jin J, Zhao H, Guan D, Xu Y (2014) TL-2 attenuates beta-amyloid induced neuronal apoptosis through the AKT/GSK-3beta/beta-catenin pathway. Int. J. Neuropsychopharmacol. 17, 1511–1519.