ApoE4 and Aβ oligomers reduce BDNF expression via HDAC nuclear translocation

Journal of Neuroscience

Volumn 35, Issue 19, 2015, Pages 7538-7551

  Sen, Abhik ^a   Nelson, Thomas J ^a   Alkon, Daniel L ^a  

^a Blanchette Rockefeller Neurosciences Institute   (United States)

Author keywords

Alzheimer s disease; ApoE; BDNF; Histone deacetylase; LRP1; PKC

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E4; BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE DEACETYLASE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEIN KINASE C; APOLIPOPROTEIN E; CHOLESTEROL; LRP1 PROTEIN, HUMAN;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; UPREGULATION; VERY ELDERLY; WESTERN BLOTTING; ANIMAL; BRAIN; CASE CONTROL STUDY; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; NERVE CELL; NEUROBLASTOMA; NUCLEOLUS; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR CELL LINE; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CASE-CONTROL STUDIES; CELL LINE, TUMOR; CELL NUCLEOLUS; CELLS, CULTURED; CHOLESTEROL; FEMALE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEUROBLASTOMA; NEURONS; PROTEIN KINASE C; PROTEIN TRANSPORT; RNA INTERFERENCE;

EID: 84929353447     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0260-15.2015     Document Type: Article

References (76)

1. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T (2007) Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85:525-535. CrossRef Medline
2. Allen SJ, Watson JJ, Dawbarn D (2011) The neurotrophins and their role in Alzheimer's disease. Curr Neuropharmacol 9:559-573. CrossRef Medline
3. Alvarez A, Aleixandre M, Linares C, Masliah E, Moessler H (2014) Apathy and APOE4 are associated with reduced BDNF levels in Alzheimer's disease. J Alzheimers Dis 42:1347-1355. Medline
4. An JJ, Gharami K, Liao GY, Woo NH, Lau AG, Vanevski F, Torre ER, Jones KR, Feng Y, Lu B, Xu B (2008) Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134:175-187. CrossRef Medline
5. Baj G, Leone E, Chao MV, Tongiorgi E (2011) Spatial segregation of BDNF transcripts enables BDNF to differentially shape distinct dendritic compartments. Proc Natl Acad Sci USA 108:16813-16818. CrossRef Medline
6. Baj G, D'Alessandro V, Musazzi L, Mallei A, Sartori CR, Sciancalepore M, Tardito D, Langone F, Popoli M, Tongiorgi E (2012) Physical exercise and antidepressants enhance BDNF targeting in hippocampal CA3 dendrites: further evidence of a spatial code for BDNF splice variants. Neuropsychopharmacology 37:1600-1611. CrossRef Medline
7. Boulle F, van den Hove DL, Jakob SB, Rutten BP, Hamon M, van Os J, Lesch KP, Lanfumey L, Steinbusch HW, Kenis G (2012) Epigenetic regulation of the BDNF gene: implications for psychiatric disorders. Mol Psychiatry 17:584-596. CrossRef Medline
8. Bredy TW, Wu H, Crego C, Zellhoefer J, Sun YE, Barad M (2007) Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 14:268-276. CrossRef Medline
9. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 10:333-344.
10. Buttini M, Yu GQ, Shockley K, Huang Y, Jones B, Masliah E, Mallory M, Yeo T, Longo FM, Mucke L (2002) Modulation of Alzheimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid [beta] peptides but not on plaque formation. J Neurosci 22:10539-10548. Medline
11. Chartier-Harlin MC, Parfitt M, Legrain S, Pérez-Tur J, Brousseau T, Evans A, Berr C, Vidal O, Roques P, Gourlet V, Fruchart JC, Delacourte A, Rossor M, Amouyel P (1994) Apolipoprotein E, [ ε ] 4 allele as a major risk factor for sporadic early and late-onset forms of Alzheimer's disease: analysis of the 19ql3.2 chromosomal region. Hum Mol Genet 3:569-574. CrossRef Medline
12. Corbett GT, Roy A, Pahan K (2013) Sodium phenylbutyrate enhances astrocytic neurotrophin synthesis via protein kinase C (PKC)-mediated activation of cAMP-response element-binding protein (CREB): implications for Alzheimer disease therapy. J Biol Chem 288:8299-8312. CrossRef Medline
13. Ding H, Dolan PJ, Johnson GV (2008) Histone deacetylase 6 interacts with the micro tubule-associated protein tau. J Neurochem 106:2119-2130. CrossRef Medline
14. Dong LM, Innerarity TL, Arnold KS, Newhouse YM, Weisgraber KH (1998) The carboxyl terminus in apolipoprotein E2 and the seven amino acid repeat in apolipoprotein E-Leiden: role in receptor-binding activity. J Lipid Res 39:1173-1180. Medline
15. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178-182. CrossRef Medline
16. Fischer A, Sananbenesi F, Mungenast A, Tsai LH (2010) Targeting the correct HDAC(s) to treat cognitive disorders. Trends Pharmacol Sci 31:605-617. CrossRef Medline
17. Gräff 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 neuro-degenerating brain. Nature 483:222-226. CrossRef Medline
18. Harris-White ME, Frautschy SA (2005) Low density lipoprotein receptor-related proteins (LRPs), Alzheimer's and cognition. Curr Drug Targets CNS Neurol Disord 4:469-480. CrossRef Medline
19. Herrup K, Li J, Chen J (2013) The role of ATM and DNA damage in neurons: upstream and downstream connections. DNA Repair (Amst) 12: 600-604. CrossRef Medline
20. Holsinger RM, Schnarr J, Henry P, Castelo VT, Fahnestock M (2000) Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer's disease. Brain Res Mol Brain Res 76:347-354. CrossRef Medline
21. Holtzman DM, Herz J, Bu G (2012) Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb Perspect Med 2:a006312. Medline
22. Hongpaisan J, Sun MK, Alkon DL (2011) PKC epsilon activation prevents synaptic loss, Abeta elevation, and cognitive deficits in Alzheimer's disease transgenic mice. J Neurosci 31:630-643. CrossRef Medline
23. Hongpaisan J, Xu C, Sen A, Nelson TJ, Alkon DL (2013) PKC activation during training restores mushroom spine synapses and memory in the aged rat. Neurobiol Dis 55:44-62. CrossRef Medline
24. Houlden H, Crook R, Backhovens H, Prihar G, Baker M, Hutton M, Rossor M, Martin JJ, Van Broeckhoven C, Hardy J (1998) ApoE genotype is a risk factor in nonpresenilin early-onset Alzheimer's disease families. Am J Med Genet 81:117-121. CrossRef Medline
25. Ishimaru N, Fukuchi M, Hirai A, Chiba Y, Tamura T, Takahashi N, Tabuchi A, Tsuda M, Shiraishi M (2010) Differential epigenetic regulation of BDNF and NT-3 genes by trichostatin A and 5-aza-2'-deoxycytidine in Neuro-2a cells. Biochem Biophys Res Commun 394:173-177. CrossRef Medline
26. Kauppi K, Nilsson LG, Persson J, Nyberg L (2014) Additive genetic effect of APOE and BDNF on hippocampus activity. Neuroimage 89:306-313. CrossRef Medline
27. Khan TK, Sen A, Hongpaisan J, Lim CS, Nelson TJ, Alkon DL (2015) PK-Cepsilon deficits in Alzheimer's disease brains and skin fibroblasts. J Alz-heimers Dis 43:491-509. Medline
28. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rum-baugh G (2010) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35:870-880. CrossRef Medline
29. Klein RC, Mace BE, Moore SD, Sullivan PM (2010) Progressive loss of synaptic integrity in human apolipoprotein E4 targeted replacement mice and attenuation by apolipoprotein E2. Neuroscience 171:1265-1272. CrossRef Medline
30. Koppel I, Timmusk T (2013) Differential regulation of Bdnf expression in cortical neurons by class-selective histone deacetylase inhibitors. Neuropharmacology 75:106-115. CrossRef Medline
31. Koryakina A, Aeberhard J, Kiefer S, Hamburger M, Küenzi P (2009) Regulation of secretases by all-trans-retinoic acid. FEBS J 276:2645-2655. CrossRef Medline
32. Kowal RC, Herz J, Weisgraber KH, Mahley RW, Brown MS, Goldstein JL (1990) Opposing effects of apolipoproteins E and C on lipoprotein binding to low density lipoprotein receptor-related protein. J Biol Chem 265: 10771-10779. Medline
33. Kramer JM, van Bokhoven H (2009) Genetic and epigenetic defects in mental retardation. Int J Biochem Cell Biol 41:96-107. CrossRef Medline
34. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE (1994) Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 269:23403-23406. Medline
35. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279:40545-40559. CrossRef Medline
36. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, Malone LM, Sweatt JD (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281:15763-15773. CrossRef Medline
37. Li G, Bien-LyN, Andrews-Zwilling Y, Xu Q, Bernardo A, Ring K, Halabisky B, Deng C, Mahley RW, Huang Y (2009) GABAergic interneuron dysfunction impairs hippocampal neurogenesis in adult apolipoprotein E4 knockin mice. Cell Stem Cell 5:634-645. CrossRef Medline
38. Lim CS, Alkon DL (2012) Protein kinase C stimulates HuD-mediated mRNA stability and protein expression of neurotrophic factors and enhances dendritic maturation of hippocampal neurons in culture. Hippocampus 22:2303-2319. CrossRef Medline
39. Lim YY, Villemagne VL, Laws SM, Pietrzak RH, Snyder PJ, Ames D, Ellis KA, Harrington K, Rembach A, Martins RN, Rowe CC, Masters CL, Maruff P (2014) APOE and BDNF polymorphisms moderate amyloid beta-related cognitive decline in preclinical Alzheimer's disease. Mol Psychiatry. In press.
40. Limon A, Reyes-Ruiz JM, Miledi R (2012) Loss of functional GABA(A) receptors in the Alzheimer diseased brain. Proc Natl Acad Sci U S A 109: 10071-10076. CrossRef Medline
41. Liu CC, Kanekiyo T, Xu H, Bu G (2013) Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol 9:106-118. CrossRef Medline
42. Mai A, Rotili D, Valente S, Kazantsev AG (2009) Histone deacetylase inhibitors and neurodegenerative disorders: holding the promise. Curr Pharm Des 15:3940-3957. CrossRef Medline
43. Maioli S, Puerta E, Merino-Serrais P, Fusari L, Gil-Bea F, Rimondini R, Cedazo-Minguez A (2012) Combination of apolipoprotein E4 and high carbohydrate diet reduces hippocampal BDNF and arc levels and impairs memory in young mice. J Alzheimers Dis 32:341-355. Medline
44. Matsushima H, Shimohama S, Chachin M, Taniguchi T, Kimura J (1996) Ca2+-dependent and Ca2 +-independent protein kinase C changes in the brain of patients with Alzheimer's disease. J Neurochem 67:317-323. Medline
45. Megías M, Emri Z, Freund TF, Gulyás AL (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540. CrossRef Medline
46. Michaelson DM (2014) APOE epsilon4: the most prevalent yet understud-ied risk factor for Alzheimer's disease. Alzheimers Dement 10:861-868. CrossRef Medline
47. Migliorini MM, Behre EH, Brew S, Ingham KC, Strickland DK (2003) Allo-steric modulation of ligand binding to low density lipoprotein receptor-related protein by the receptor-associated protein requires critical lysine residues within its carboxyl-terminal domain. J Biol Chem 278:17986-17992. CrossRef Medline
48. Nelson TJ, Alkon DL (2009) Neuroprotective versus tumorigenic protein kinase C activators. Trends Biochem Sci 34:136-145. CrossRef Medline
49. Nelson TJ, Cui C, Luo Y, Alkon DL (2009) Reduction of beta-amyloid levels by novel protein kinase C(epsilon) activators. J Biol Chem 284:34514-34521. CrossRef Medline
50. Neumann JT, Thompson JW, Raval AP, Cohan CH, Koronowski KB, Pérez-Pinzon MA (2015) Increased BDNF protein expression after ischemic or PKC epsilon preconditioning promotes electrophysiologic changes that lead to neuroprotection. J Cereb Blood Flow Metab 35:121-130. Medline
51. Noguchi A, Matsumura S, Dezawa M, Tada M, Yanazawa M, Ito A, Akioka M, Kikuchi S, Sato M, Ideno S, Noda M, Fukunari A, Muramatsu S, Itokazu Y, Sato K, Takahashi H, Teplow DB, Nabeshima Y, Kakita A, Imahori K, et al. (2009) Isolation and characterization of patient-derived, toxic, high mass amyloid beta-protein (Abeta) assembly from Alzheimer disease brains. J Biol Chem 284:32895-32905. CrossRef Medline
52. Peng S, Wuu J, Mufson EJ, Fahnestock M (2005) Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre clinical stages of Alzheimer's disease. J Neurochem 93:1412-1421. CrossRef Medline
53. Pfrieger FW (2003) Cholesterol homeostasis and function in neurons of the central nervous system. Cell Mol Life Sci 60:1158-1171. Medline
54. Pruunsild P, Kazantseva A, Aid T, Palm K, Timmusk T (2007) Dissecting the human BDNF locus: bidirectional transcription, complex splicing, and multiple promoters. Genomics 90:397-406. CrossRef Medline
55. Rhinn H, Fujita R, Qiang L, Cheng R, Lee JH, Abeliovich A (2013) Integrative genomics identifies APOE epsilon4 effectors in Alzheimer's disease. Nature 500:45-50. CrossRef Medline
56. Rissman RA, Mobley WC (2011) Implications for treatment: GABAA receptors in aging, Down syndrome and Alzheimer's disease. J Neurochem 117:613-622. Medline
57. Rissman RA, De Bias AL, Armstrong DM (2007) GABA(A) receptors in aging and Alzheimer's disease. J Neurochem 103:1285-1292. CrossRef Medline
58. Saha RN, Pahan K (2006) HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ 13:539-550. CrossRef Medline
59. Sakata K, Duke SM (2014) Lack of BDNF expression through promoter IV disturbs expression of monoamine genes in the frontal cortex and hippocampus. Neuroscience 260:265-275. CrossRef Medline
60. Sakata K, Woo NH, Martinowich K, Greene JS, Schloesser RJ, Shen L, Lu B (2009) Critical role of promoter IV-driven BDNF transcription in GABAergic transmission and synaptic plasticity in the prefrontal cortex. Proc Natl Acad Sci U S A 106:5942-5947. CrossRef Medline
61. Sando SB, Melquist S, Cannon A, Hutton ML, Sletvold O, Saltvedt I, White LR, Lydersen S, Aasly JO (2008) APOE epsilon 4 lowers age at onset and is a high risk factor for Alzheimer's disease; a case control study from central Norway. BMC Neurol 8:9. CrossRef Medline
62. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. CrossRef Medline
63. Sen A, Alkon DL, Nelson TJ (2012) Apolipoprotein E3 (ApoE3) but not ApoE4 protects against synaptic loss through increased expression of protein kinase C epsilon. J Biol Chem 287:15947-15958. CrossRef Medline
64. Siegel GJ, Chauhan NB (2000) Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res Brain Res Rev 33:199-227. CrossRef Medline
65. Simmons T, Newhouse YM, Arnold KS, Innerarity TL, Weisgraber KH (1997) Human low density lipoprotein receptor fragment. Successful refolding of a functionally active ligand-binding domain produced in Escherichia coli. J Biol Chem 272:25531-25536. CrossRef Medline
66. Simões-Pires C, Zwick V, Nurisso A, Schenker E, Carrupt PA, Cuendet M (2013) HDAC6 as a target for neurodegenerative diseases: what makes it different from the other HDACs? Mol Neurodegener 8:7. CrossRef Medline
67. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993a) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981. CrossRef Medline
68. Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, Roses AD (1993b) Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci U S A 90:8098-8102. CrossRef Medline
69. Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2 + influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726. CrossRef Medline
70. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, Smith JD, Ladu MJ, Rostagno A, Frangione B, Ghiso J (2000) Lipida-tion of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 348:359-365. CrossRef Medline
71. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN, McKinsey TA (2004) Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 24:8374-8385. CrossRef Medline
72. Verghese PB, Castellano JM, Holtzman DM (2011) Apolipoprotein E in Alzheimer's disease and other neurological disorders. Lancet Neurol 10: 241-252. CrossRef Medline
73. Weisgraber KH, Innerarity TL, Mahley RW (1982) Abnormal lipoprotein receptor-binding activity of the human E apoprotein due to cysteine-arginine interchange at a single site. J Biol Chem 257:2518-2521. Medline
74. Yang XJ, Seto E (2008) The Rpd3/Hdal family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9:206-218. Medline
75. Yong SM, Lim ML, Low CM, Wong BS (2014) Reduced neuronal signaling in the ageing apolipoprotein-E4 targeted replacement female mice. Sci Rep 4:6580. CrossRef Medline
76. Zhang X, Ozawa Y, Lee H, Wen YD, Tan TH, Wadzinski BE, Seto E (2005) Histone deacetylase 3 (HDAC3) activity is regulated by interaction with protein serine/threonine phosphatase 4. Genes Dev 19:827-839. CrossRef Medline