Mice knock out for the histone acetyltransferase p300/CREB binding protein-associated factor develop a resistance to amyloid toxicity

Neuroscience

Volumn 167, Issue 3, 2010, Pages 850-863

  Duclot, F ^a,b,c   Meffre, J ^a,b,c   Jacquet, C ^b,d   Gongora, C ^b,e   Maurice, T ^a,b,c  

^a University of Montpellier   (France)

^b UNIV MONTPELLIER   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^e INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

Author keywords

A 25 35 peptide; Acetyltransferase PCAF; Amyloid toxicity; Memory; Neprilysin

Indexed keywords

AMYLOID BETA PROTEIN; HISTONE ACETYLTRANSFERASE PCAF; MEMBRANE METALLOENDOPEPTIDASE;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LIPID PEROXIDATION; MALE; MAZE TEST; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PYRAMIDAL NERVE CELL; SENSITIVITY ANALYSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; BRAIN; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; GENETIC PREDISPOSITION TO DISEASE; HIPPOCAMPUS; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; NEPRILYSIN; NERVE DEGENERATION; NEURONS; OXIDATIVE STRESS; P300-CBP TRANSCRIPTION FACTORS; PEPTIDE FRAGMENTS; PRESENILINS; SOMATOSTATIN;

EID: 77951277406     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.02.055     Document Type: Article

References (66)

1. Beglopoulos V., Shen J. Regulation of CRE-dependent transcription by presenilins: prospects for therapy of Alzheimer's disease. Trends Pharmacol Sci 2006, 27:33-40.
2. Belyaev N.D., Nalivaeva N.N., Makova N.Z., Turner A.J. Neprilysin gene expression requires binding of the amyloid precursor protein intracellular domain to its promoter: implications for Alzheimer disease. EMBO Rep 2009, 10:94-100.
3. 25-35-induced alterations of the somatostatin signaling pathway in the rat temporal cortex. Neuroscience 2008, 154:1458-1466.
4. 25-35-induced reduction of somatostatin and neprilysin content in rat temporal cortex. Life Sci 2009, 84:205-210.
5. Burgos-Ramos E., Puebla-Jiménez L., Hernández-Pinto A., Arilla-Ferreiro E. Sulfadiazine partially protects the rat temporal cortex from amyloid β peptide (25-35)-induced alterations of the somatostatinergic system. Neuroendocrinology 2009, 89:400-410.
6. Cao X., Südhof T.C. A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 2001, 293:115-120.
7. Chen A.C., Selkoe D.J. Response to: Pardossi-Piquard et al., "Presenilin-dependent transcriptional control of the Aβ-degrading enzyme neprilysin by intracellular domains of βAPP and APLP.". Neuron. Neuron 2007, 53:479-483.
8. Chérasse Y., Maurin A.C., Chaveroux C., Jousse C., Carraro V., Parry L., Deval C., Chambon C., Fafournoux P., Bruhat A. The p300/CBP-associated factor (PCAF) is a cofactor of ATF4 for amino acid-regulated transcription of CHOP. Nucleic Acids Res 2007, 35:5954-5965.
9. Currie J.R., Chen-Hwang M.C., Denman R., Smedman M., Potempska A., Ramakrishna N., Rubenstein R., Wisniewski H.M., Miller D.L. Reduction of histone cytotoxicity by the Alzheimer β-amyloid peptide precursor. Biochim Biophys Acta 1997, 1355:248-258.
10. Davies P., Katzman R., Terry R.D. Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 1980, 288:279-280.
11. Davies P., Terry R.D. Cortical somatostatin-like immunoreactivity in cases of Alzheimer's disease and senile dementia of the Alzheimer type. Neurobiol Aging 1981, 2:9-14.
12. De Strooper B., Saftig P., Craessaerts K., Vanderstichele H., Guhde G., Annaert W., Von Figura K., Van Leuven F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 1998, 391:387-390.
13. Delobette S., Privat A., Maurice T. In vitro aggregation facilities β-amyloid peptide-(25-35)-induced amnesia in the rat. Eur J Pharmacol 1997, 319:1-4.
14. Eckman E.A., Eckman C.B. Aβ-degrading enzymes: modulators of Alzheimer's disease pathogenesis and targets for therapeutic intervention. Biochem Soc Trans 2005, 33:1101-1105.
15. El-Amouri S.S., Zhu H., Yu J., Gage F.H., Verma I.M., Kindy M.S. Neprilysin protects neurons against Aβ peptide toxicity. Brain Res 2007, 1152:191-200.
16. Evin G., Weidemann A. Biogenesis and metabolism of Alzheimer's disease Aβ amyloid peptides. Peptides 2002, 23:1285-1297.
17. Ferreiro E., Resende R., Costa R., Oliveira C.R., Pereira C.M. An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-β peptides neurotoxicity. Neurobiol Dis 2006, 23:669-678.
18. 25-35 oligomers, S100β and neurotransmitters. J Neuroimmunol 2007, 186:181-192.
19. Hayashi M., Yamashita A., Shimizu K. Somatostatin and brain-derived neurotrophic factor mRNA expression in the primate brain: decreased levels of mRNAs during aging. Brain Res 1997, 749:283-289.
20. Hellström-Lindahl E., Ravid R., Nordberg A. Age-dependent decline of neprilysin in Alzheimer's disease and normal brain: inverse correlation with Aβ levels. Neurobiol Aging 2008, 29:210-221.
21. Hernandez-Hernandez A., Ray P., Litos G., Ciro M., Ottolenghi S., Beug H., Boyes J. Acetylation and MAPK phosphorylation cooperate to regulate the degradation of active GATA-1. EMBO J 2006, 25:3264-3274.
22. Herreman A., Hartmann D., Annaert W., Saftig P., Craessaerts K., Serneels L., Umans L., Schrijvers V., Checler F., Vanderstichele H., Baekelandt V., Dressel R., Cupers P., Huylebroeck D., Zwijsen A., Van Leuven F., De Strooper B. Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc Natl Acad Sci U S A 1999, 96:11872-11877.
23. Ikezu T., Okamoto T., Komatsuzaki K., Matsui T., Martyn J.A., Nishimoto I. Negative transactivation of cAMP response element by familial Alzheimer's mutants of APP. EMBO J 1996, 15:2468-2475.
24. 1-42-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat Med 2000, 6:143-150.
25. Jeong J.W., Bae M.K., Ahn M.Y., Kim S.H., Sohn T.K., Bae M.H., Yoo M.A., Song E.J., Lee K.J., Kim K.W. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 2002, 111:709-720.
26. Kiernan R., Brès V., Ng R.W., Coudart M.P., El Messaoudi S., Sardet C., Jin D.Y., Emiliani S., Benkirane M. Post-activation turn-off of NF-K{green}B-dependent transcription is regulated by acetylation of p65. J Biol Chem 2003, 278:2758-2766.
27. Kinoshita A., Whelan C.M., Berezovska O., Hyman B.T. The γ secretase-generated carboxyl-terminal domain of the amyloid precursor protein induces apoptosis via Tip60 in H4 cells. J Biol Chem 2002, 277:28530-28536.
28. 25-35. Neuroscience 2007, 145:209-224.
29. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
30. 25-35/40) and fragment presence in the brains of Alzheimer's patients. J Neurosci Res 2002, 70:474-483.
31. Leduc C., Claverie P., Eymin B., Col E., Khochbin S., Brambilla E., Gazzeri S. p14ARF promotes RB accumulation through inhibition of its Tip60-dependent acetylation. Oncogene 2006, 25:4147-4154.
32. Liao M.Q., Tzeng Y.J., Chang L.Y., Huang H.B., Lin T.H., Chyan C.L., Chen Y.C. The correlation between neurotoxicity, aggregative ability and secondary structure studied by sequence truncated Aβ peptides. FEBS Lett 2007, 581:1161-1165.
33. Linares L.K., Kiernan R., Triboulet R., Chable-Bessia C., Latreille D., Cuvier O., Lacroix M., Le Cam L., Coux O., Benkirane M. Intrinsic ubiquitination activity of PCAF controls the stability of the oncoprotein Hdm2. Nat Cell Biol 2007, 9:331-338.
34. Lowry O.H., Rosebrough N.J., Farr A.I., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
35. Marr R.A., Guan H., Rockenstein E., Kindy M., Gage F.H., Verma I., Masliah E., Hersh L.B. Neprilysin regulates amyloid β peptide levels. J Mol Neurosci 2004, 22:5-11.
36. Marr R.A., Rockenstein E., Mukherjee A., Kindy M.S., Hersh L.B., Gage F.H. Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J Neurosci 2003, 23:1992-1996.
37. Maurice T., Duclot F., Meunier J., Naert G., Givalois L., Meffre J., Célérier A., Jacquet C., Copois V., Mechti N., Ozato K., Gongora C. Altered memory capacities and response to stress in p300/CBP-associated factor (PCAF) histone acetylase knock out mice. Neuropsychopharmacology 2008, 33:1584-1602.
38. Maurice T., Lockhart B.P., Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 1996, 706:181-193.
39. 25-35-amyloid peptide-induced amnesia by NMDA receptor-associated glycine site agonists. Brain Res 1996, 731:249-253.
40. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001, 21:1249-1259.
41. 1 receptor. Br J Pharmacol 2006, 149:998-1012.
42. 25-35-amyloid peptide-induced endoplasmic reticulum stress. Neuroscience Meeting Planner 2006, Society for Neuroscience, Atlanta, GA, Program No. 272.6.
43. Mouri A., Zou L.B., Iwata N., Saido T.C., Wang D., Wang M.W., Noda Y., Nabeshima T. Inhibition of neprilysin by thiorphan (i.c.v.) causes an accumulation of amyloid β and impairment of learning and memory. Behav Brain Res 2006, 168:83-91.
44. Pardossi-Piquard R., Dunys J., Kawarai T., Sunyach C., Alves da Costa C., Vincent B., Sévalle J., Pimplikar S., St.George-Hyslop P., Checler F. Response to correspondence: Pardossi-Piquard et al., "Presenilin-dependent transcriptional control of the Aβ-degrading enzyme neprilysin by intracellular domains of βAPP and APLP." Neuron 46: 541-554. Neuron. Neuron 2007, 53:483-486.
45. Pardossi-Piquard R., Petit A., Kawarai T., Sunyach C., Alves da Costa C., Vincent B., Ring S., D'Adamio L., Shen J., Müller U., St.George Hyslop P., Checler F. Presenilin-dependent transcriptional control of the Aβ-degrading enzyme neprilysin by intracellular domains of βAPP and APLP. Neuron 2005, 46:541-554.
46. 25-35 region to aggregation and neurotoxicity. J Neurochem 1995, 64:253-265.
47. Potempska A., Ramakrishna N., Wisniewski H.M., Miller D.L. Interaction between the β-amyloid peptide precursor and histones. Arch Biochem Biophys 1993, 304:448-453.
48. Rose J.B., Crews L., Rockenstein E., Adame A., Mante M., Hersh L.B., Gage F.H., Spencer B., Potkar R., Marr R.A., Masliah E. Neuropeptide Y fragments derived from neprilysin processing are neuroprotective in a transgenic model of Alzheimer's disease. J Neurosci 2009, 29:1115-1125.
49. Rouaux C., Jokic N., Mbebi C., Boutillier S., Loeffler J.P., Boutillier A.L. Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J 2003, 22:6537-6549.
50. Schapansky J., Olson K., Van der Ploeg R., Glazner G. NF-K{green}B activated by ER calcium release inhibits Aβ-mediated expression of CHOP protein: enhancement by ad-linked mutant presenilin 1. Exp Neurol 2007, 208:169-176.
51. Shirotani K., Tsubuki S., Iwata N., Takaki Y., Harigaya W., Maruyama K., Kiryu-Seo S., Kiyama H., Iwata H., Tomita T., Iwatsubo T., Saido T.C. Neprilysin degrades both amyloid β peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J Biol Chem 2001, 276:21895-21901.
52. Spange S., Wagner T., Heinzel T., Krämer O.H. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol 2009, 41:185-198.
53. 25-35 peptide induces impairment in short-term rather than long-term memory in rats. Brain Res Bull 2003, 61:197-205.
54. Stepanichev M.Y., Zdobnova I.M., Zarubenko L.N., Gulyaeva N.V. Studies of the effects of central administration of β-amyloid peptide (25-35): pathomorphological changes in the hippocampus and impairment of spatial memory. Neurosci Behav Physiol 2006, 36:101-106.
55. 25-35-induced memory impairments correlate with cell loss in rat hippocampus. Physiol Behav 2004, 80:647-655.
56. Sterner D.E., Berger S.L. Acetylation and transcription-related factors. Microbiol Mol Biol Rev 2000, 64:435-459.
57. Takaki Y., Iwata N., Tsubuki S., Taniguchi S., Toyoshima S., Lu B., Gerard N.P., Gerard C., Lee H.J., Shirotani K., Saido T.C. Biochemical identification of the neutral endopeptidase family member responsible for the catabolism of amyloid β peptide in the brain. J Biochem 2000, 128:897-902.
58. Tamatani M., Mitsuda N., Matsuzaki H., Okado H., Miyake S., Vitek M.P., Yamaguchi A., Tohyama M. A pathway of neuronal apoptosis induced by hypoxia/reoxygenation: roles of nuclear factor-K{green}B and Bcl-2. J Neurochem 2000, 75:683-693.
59. 25-35-induced toxicity in mice. Neuropsychopharmacology 2009, 34:1552-1566.
60. Wang R., Wang S., Malter J.S., Wang D.S. Effects of HNE-modification induced by Abeta on neprilysin expression and activity in SH-SY5Y cells. J Neurochem 2009, 108:1072-1082.
61. Wood M.A., Kaplan M.P., Park A., Blanchard E.J., Oliveira A.M., Lombardi T.L., Abel T. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 2005, 12:111-119.
62. 1-42-induced learning and memory deficits in rats: implication of oxidative stress in beta-amyloid-induced neurotoxicity in vivo. Eur J Neurosci 1999, 11:83-90.
63. Yamauchi T., Yamauchi J., Kuwata T., Tamura T., Yamashita T., Bae N., Westphal H., Ozato K., Nakatani Y. Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAF-B/GCN5 in mouse embryogenesis. Proc Natl Acad Sci U S A 2000, 97:11303-11306.
64. Yang X.J. Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays 2004, 26:1076-1087.
65. Zou L.B., Mouri A., Iwata N., Saido T.C., Wang D., Wang M.W., Mizoguchi H., Noda Y., Nabeshima T. Inhibition of neprilysin by infusion of thiorphan into the hippocampus causes an accumulation of amyloid β and impairment of learning and memory. J Pharmacol Exp Ther 2006, 317:334-340.
66. Zussy C., Brureau A., Maurice T., Givalois L. Hippocampus alteration induced by a single icv injection of a β-amyloid peptide. Neuroscience Meeting Planner 2009, Society for Neuroscience, Chicago, IL, Program No. 725.6.