De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease

Human Molecular Genetics

Volumn 22, Issue 15, 2013, Pages 3077-3092

  Wong, Hon Kit Andus ^a   Veremeyko, Tatiana ^a   Patel, Nehal ^b   Lemere, Cynthia A ^a   Walsh, Dominic M ^c   Esau, Christine ^d   Vanderburg, Charles ^b   Krichevsky, Anna M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b The Harvard Center for Neurodegeneration & Repair   (United States)

^c Brigham and Women's Hospital Center for Neurologic Diseases   (United States)

^d REGULUS THERAPEUTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; MICRORNA; MICRORNA 132; MICRORNA 212; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HIPPOCAMPAL CA1 REGION; HUMAN; HUMAN TISSUE; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PC12 CELL; PRIORITY JOURNAL; RAT; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; BRAIN; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MICE; MICRORNAS; MODELS, BIOLOGICAL; NEURONS; P300-CBP TRANSCRIPTION FACTORS; PTEN PHOSPHOHYDROLASE; RATS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84880290282     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt164     Document Type: Article

References (86)

1. Turner, R.S. (2006) Alzheimer's disease. Semin. Neurol., 26, 499-506.
2. Castro, R.E., Santos, M.M., Gloria, P.M., Ribeiro, C.J., Ferreira, D.M., Xavier, J.M., Moreira, R. and Rodrigues, C.M. (2010) Cell death targets and potential modulators in Alzheimer's disease. Curr. Pharm. Des., 16, 2851-2864.
3. Krichevsky, A.M., King, K.S., Donahue, C.P., Khrapko, K. and Kosik, K.S. (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA, 9, 1274-1281.
4. Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E. and Ambros, V. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol., 5, R13.
5. Berezikov, E., Thuemmler, F., van Laake, L.W., Kondova, I., Bontrop, R., Cuppen, E. and Plasterk, R.H. (2006) Diversity of microRNAs in human and chimpanzee brain. Nat. Genet., 38, 1375-1377.
6. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A.O., Landthaler, M. et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 129, 1401-1414.
7. Ambros, V. (2004) The functions of animal microRNAs. Nature, 431, 350-355.
8. Djuranovic, S., Nahvi, A. and Green, R. (2011) A parsimonious model for gene regulation by miRNAs. Science, 331, 550-553.
9. Liu, N.K. and Xu, X.M. (2011) MicroRNA in central nervous system trauma and degenerative disorders. Physiol. Genomics, 43, 571-580.
10. Zovoilis, A., Agbemenyah, H.Y., Agis-Balboa, R.C., Stilling, R.M., Edbauer, D., Rao, P., Farinelli, L., Delalle, I., Schmitt, A., Falkai, P. et al. (2011) microRNA-34c is a novel target to treat dementias. EMBO J., 30, 4299-4308.
11. Patel, N., Hoang, D., Miller, N., Ansaloni, S., Huang, Q., Rogers, J.T., Lee, J.C. and Saunders, A.J. (2008) MicroRNAs can regulate human APP levels. Mol. Neurodegener., 3, 10.
12. Hebert, S.S., Horre, K., Nicolai, L., Bergmans, B., Papadopoulou, A.S., Delacourte, A. and De Strooper, B. (2009) MicroRNA regulation of Alzheimer's amyloid precursor protein expression. Neurobiol. Dis., 33, 422-428.
13. Vilardo, E., Barbato, C., Ciotti, M., Cogoni, C. and Ruberti, F. (2010) MicroRNA-101 regulates amyloid precursor protein expression in hippocampal neurons. J. Biol. Chem., 285, 18344-18351.
14. Liu, W., Liu, C., Zhu, J., Shu, P., Yin, B., Gong, Y., Qiang, B., Yuan, J. and Peng, X. (2010) MicroRNA-16 targets amyloid precursor protein to potentially modulate Alzheimer's-associated pathogenesis in SAMP8mice. Neurobiol. Aging, 33, 522-534.
15. Long, J.M. and Lahiri, D.K. (2011) MicroRNA-101 downregulates Alzheimer's amyloid-beta precursor protein levels in human cell cultures and is differentially expressed. Biochem. Biophys. Res. Commun., 404, 889-895.
16. Long, J.M., Ray, B. and Lahiri, D.K. (2012) MicroRNA-153 physiologically inhibits expression of amyloid-beta precursor protein in culturedhumanfetal brain cells and is dysregulated in a subset of Alzheimer disease patients. J. Biol. Chem., 287, 31298-31310.
17. Liang, C., Zhu, H., Xu, Y., Huang, L., Ma, C., Deng, W., Liu, Y. and Qin, C. (2012) MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2. Brain Res., 1455, 103-113.
18. Smith, P., Al Hashimi, A., Girard, J., Delay, C. and Hebert, S.S. (2011) In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J. Neurochem., 116, 240-247.
19. Wang, W.X., Rajeev, B.W., Stromberg, A.J., Ren, N., Tang, G., Huang, Q., Rigoutsos, I. and Nelson, P.T. (2008) The expression of microRNAmiR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J. Neurosci., 28, 1213-1223.
20. Boissonneault, V., Plante, I., Rivest, S. and Provost, P. (2009) MicroRNA-298 and microRNA-328 regulate expression of mouse beta-amyloid precursor protein-converting enzyme 1. J. Biol. Chem., 284, 1971-1981.
21. Hebert, S.S., Horre, K., Nicolai, L., Papadopoulou, A.S., Mandemakers, W., Silahtaroglu, A.N., Kauppinen, S., Delacourte, A. and De Strooper, B. (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl Acad. Sci. USA, 105, 6415-6420.
22. Zhu, H.C., Wang, L.M., Wang, M., Song, B., Tan, S., Teng, J.F. and Duan, D.X. (2012) MicroRNA-195 downregulates Alzheimer's disease amyloid-beta production by targeting BACE1. Brain Res. Bull., 88, 596-601.
23. Fang, M.,Wang, J.,Zhang, X.,Geng, Y.,Hu, Z.,Rudd, J.A.,Ling, S.,Chen, W. and Han, S. (2012) The miR-124 regulates the expression of BACE1/betasecretase correlatedwith cell death inAlzheimer's disease. Toxicol. Lett., 209, 94-105.
24. Wang, X.,Liu, P.,Zhu, H.,Xu, Y.,Ma, C.,Dai, X.,Huang, L.,Liu, Y.,Zhang, L. and Qin, C. (2009) miR-34a, a microRNA up-regulated in a double transgenic mousemodel ofAlzheimer's disease, inhibits bcl2 translation. BrainRes. Bull., 80, 268-273.
25. Magill, S.T., Cambronne, X.A., Luikart, B.W., Lioy, D.T., Leighton, B.H., Westbrook, G.L., Mandel, G. and Goodman, R.H. (2010) microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc. Natl Acad. Sci. USA, 107, 20382-20387.
26. Edbauer, D., Neilson, J.R., Foster, K.A., Wang, C.F., Seeburg, D.P., Batterton, M.N., Tada, T., Dolan, B.M., Sharp, P.A. and Sheng, M. (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron, 65, 373-384.
27. Jankowsky, J.L., Younkin, L.H., Gonzales, V., Fadale, D.J., Slunt, H.H., Lester, H.A., Younkin, S.G. and Borchelt, D.R. (2007) Rodent A beta modulates the solubility and distribution of amyloid deposits in transgenic mice. J. Biol. Chem., 282, 22707-22720.
28. Vo, N.,Klein, M.E.,Varlamova, O.,Keller, D.M.,Yamamoto, T.,Goodman, R.H. and Impey, S. (2005) A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl Acad. Sci. USA, 102, 16426-16431.
29. Wayman, G.A., Davare, M., Ando, H., Fortin, D., Varlamova, O., Cheng, H.Y., Marks, D., Obrietan, K., Soderling, T.R., Goodman, R.H. et al. (2008) An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl Acad. Sci. USA, 105, 9093-9098.
30. Nudelman, A.S., DiRocco, D.P., Lambert, T.J., Garelick, M.G., Le, J., Nathanson, N.M. and Storm, D.R. (2010) Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus, 20, 492-498.
31. Scott, H.L., Tamagnini, F., Narduzzo, K.E., Howarth, J.L., Lee, Y.B., Wong, L.F., Brown, M.W., Warburton, E.C., Bashir, Z.I. and Uney, J.B. (2012) MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci., 36, 2941-2948.
32. Davis, S., Lollo, B., Freier, S. and Esau, C. (2006) Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res., 34, 2294-2304.
33. Gabriely, G.,Wurdinger, T.,Kesari, S., Esau, C.C., Burchard, J., Linsley, P.S. and Krichevsky, A.M. (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell. Biol., 28, 5369-5380.
34. Stambolic, V., Suzuki, A., de la Pompa, J.L., Brothers, G.M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J.M., Siderovski, D.P. and Mak, T.W. (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell, 95, 29-39.
35. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J. and Greenberg, M.E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell, 96, 857-868.
36. Yang, J.Y. and Hung, M.C. (2009) A new fork for clinical application: targeting forkhead transcription factors in cancer. Clin. Cancer Res., 15, 752-757.
37. Motta, M.C., Divecha, N., Lemieux, M., Kamel, C., Chen, D., Gu, W., Bultsma, Y., McBurney, M. and Guarente, L. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell, 116, 551-563.
38. Lagos, D., Pollara, G., Henderson, S., Gratrix, F., Fabani, M., Milne, R.S., Gotch, F. and Boshoff, C. (2010) miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat. Cell Biol., 12, 513-519.
39. Grimson, A., Farh, K.K., Johnston, W.K., Garrett-Engele, P., Lim, L.P. and Bartel, D.P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell, 27, 91-105.
40. Rehmsmeier, M., Steffen, P., Hochsmann, M. and Giegerich, R. (2004) Fast and effective prediction of microRNA/target duplexes. RNA, 10, 1507-1517.
41. Ucar, A., Gupta, S.K., Fiedler, J., Erikci, E., Kardasinski, M., Batkai, S., Dangwal, S., Kumarswamy, R., Bang, C., Holzmann, A. et al.. (2012) The miRNA-212/132 family regulates both cardiac hypertrophy and cardiomyocyte autophagy. Nat. Commun., 3, 1078.
42. Sonoda, Y., Mukai, H., Matsuo, K., Takahashi, M., Ono, Y., Maeda, K., Akiyama, H. and Kawamata, T. (2010) Accumulation of tumor-suppressor PTEN in Alzheimer neurofibrillary tangles. Neurosci. Lett., 471, 20-24.
43. Zhang, X., Li, F., Bulloj, A., Zhang, Y.W., Tong, G., Zhang, Z., Liao, F.F. and Xu, H. (2006) Tumor-suppressor PTEN affects tau phosphorylation, aggregation, and binding to microtubules. FASEB J., 20, 1272-1274.
44. Rickle, A., Bogdanovic, N., Volkmann, I., Zhou, X., Pei, J.J., Winblad, B. and Cowburn, R.F. (2006) PTEN levels in Alzheimer's disease medial temporal cortex. Neurochem. Int., 48, 114-123.
45. Griffin, R.J., Moloney, A., Kelliher, M., Johnston, J.A., Ravid, R., Dockery, P., O'Connor, R. and O'Neill, C. (2005) Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J. Neurochem., 93, 105-117.
46. Cogswell, J.P., Ward, J., Taylor, I.A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C. et al. (2008) Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis., 14, 27-41.
47. Wang, W.X., Huang, Q., Hu, Y., Stromberg, A.J. and Nelson, P.T. (2011) Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol., 121, 193-205.
48. Johnson, R., Zuccato, C., Belyaev, N.D., Guest, D.J., Cattaneo, E. and Buckley, N.J. (2008) A microRNA-based gene dysregulation pathway in Huntington's disease. Neurobiol. Dis., 29, 438-445.
49. Olsen, L., Klausen, M., Helboe, L., Nielsen, F.C. and Werge, T. (2009) MicroRNAs show mutually exclusive expression patterns in the brain of adult male rats. PLoS One, 4, e7225.
50. Hollander, J.A., Im, H.I., Amelio, A.L., Kocerha, J., Bali, P., Lu, Q., Willoughby, D., Wahlestedt, C., Conkright, M.D. and Kenny, P.J. (2010) Striatal microRNA controls cocaine intake through CREB signalling. Nature, 466, 197-202.
51. Remenyi, J., Hunter, C.J., Cole, C., Ando, H., Impey, S., Monk, C.E., Martin, K.J., Barton, G.J., Hutvagner, G. and Arthur, J.S. (2010) Regulation of the miR-212/132 locus by MSK1 and CREB in response to neurotrophins. Biochem. J., 428, 281-291.
52. Somel, M., Guo, S., Fu, N., Yan, Z., Hu, H.Y., Xu, Y., Yuan, Y., Ning, Z., Hu, Y., Menzel, C. et al. (2010) MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res., 20, 1207-1218.
53. Kawashima, H., Numakawa, T., Kumamaru, E., Adachi, N., Mizuno, H., Ninomiya, M., Kunugi, H. and Hashido, K. (2010) Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience, 165, 1301-1311.
54. Cheng, H.Y., Papp, J.W., Varlamova, O., Dziema, H., Russell, B., Curfman, J.P., Nakazawa, T., Shimizu, K., Okamura, H., Impey, S. et al. (2007) microRNA modulation of circadian-clock period and entrainment. Neuron, 54, 813-829.
55. Alvarez-Saavedra, M., Antoun, G., Yanagiya, A., Oliva-Hernandez, R., Cornejo-Palma, D., Perez-Iratxeta, C., Sonenberg, N. and Cheng, H.Y. (2011) miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum. Mol. Genet., 20, 731-751.
56. Mellios, N., Sugihara, H., Castro, J., Banerjee, A., Le, C., Kumar, A., Crawford, B., Strathmann, J., Tropea, D., Levine, S.S. et al. (2011) miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat. Neurosci., 14, 1240-1242.
57. Tognini, P., Putignano, E., Coatti, A. and Pizzorusso, T. (2011) Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nat. Neurosci., 14, 1237-1239.
58. Abramov, E., Dolev, I., Fogel, H., Ciccotosto, G.D., Ruff, E. and Slutsky, I. (2009) Amyloid-beta as a positive endogenous regulator of release probability at hippocampal synapses. Nat. Neurosci., 12, 1567-1576.
59. Li, S., Hong, S., Shepardson, N.E., Walsh, D.M., Shankar, G.M. and Selkoe, D. (2009) Soluble oligomers of amyloid beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron, 62, 788-801.
60. Buckner, R.L., Snyder, A.Z., Shannon, B.J., LaRossa, G., Sachs, R., Fotenos, A.F., Sheline, Y.I., Klunk, W.E., Mathis, C.A., Morris, J.C. et al. (2005) Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci., 25, 7709-7717.
61. Forlenza, O.V., Diniz, B.S. and Gattaz, W.F. (2010) Diagnosis and biomarkers of predementia in Alzheimer's disease. BMC Med., 8, 89.
62. Forlenza, O.V., Diniz, B.S., Teixeira, A.L., Ojopi, E.B., Talib, L.L., Mendonca, V.A., Izzo, G. and Gattaz, W.F. (2010) Effect of brain-derived neurotrophic factor Val66Met polymorphism and serum levels on the progression of mild cognitive impairment. World J. Biol. Psychiatry, 11, 774-780.
63. Forlenza, O.V., Diniz, B.S., Talib, L.L., Radanovic, M., Yassuda, M.S., Ojopi, E.B. and Gattaz, W.F. (2010) Clinical and biological predictors of Alzheimer's disease in patients with amnestic mild cognitive impairment. Rev. Bras. Psiquiatr., 32, 216-222.
64. Laske, C., Stransky, E., Leyhe, T., Eschweiler, G.W., Maetzler, W., Wittorf, A., Soekadar, S., Richartz, E., Koehler, N., Bartels, M. et al. (2007) BDNF serum and CSF concentrations in Alzheimer's disease, normal pressure hydrocephalus and healthy controls. J. Psychiatr. Res., 41, 387-394.
65. Lee, J.G., Shin, B.S., You, Y.S., Kim, J.E., Yoon, S.W., Jeon, D.W., Baek, J.H., Park, S.W. and Kim, Y.H. (2009) Decreased serum brain-derived neurotrophic factor levels in elderly Korean with dementia. Psychiatry Investig., 6, 299-305.
66. Li, G., Peskind, E.R., Millard, S.P., Chi, P., Sokal, I., Yu, C.E., Bekris, L.M., Raskind, M.A., Galasko, D.R. and Montine, T.J. (2009) Cerebrospinal fluid concentration of brain-derived neurotrophic factor and cognitive function in non-demented subjects. PLoS One, 4, e5424.
67. Zhang, J., Sokal, I., Peskind, E.R., Quinn, J.F., Jankovic, J., Kenney, C., Chung, K.A., Millard, S.P., Nutt, J.G. and Montine, T.J. (2008) CSF multianalyte profile distinguishes Alzheimer and Parkinson diseases. Am. J. Clin. Pathol., 129, 526-529.
68. Impey, S., Davare, M., Lasiek, A., Fortin, D., Ando, H., Varlamova, O., Obrietan, K., Soderling, T.R., Goodman, R.H. and Wayman, G.A. (2010) An activity-inducedmicro RNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol. Cell. Neurosci., 43, 146-156.
69. Hansen, K.F., Sakamoto, K., Wayman, G.A., Impey, S. and Obrietan, K. (2010) Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One, 5, e15497.
70. Pathania, M., Torres-Reveron, J., Yan, L., Kimura, T., Lin, T.V., Gordon, V., Teng, Z.Q., Zhao, X., Fulga, T.A., Van Vactor, D. et al.. (2012) miR-132 enhances dendritic morphogenesis, spine density, synaptic integration, and survival of newborn olfactory bulb neurons. PLoS One, 7, e38174.
71. Li, Z., Jo, J., Jia, J.M., Lo, S.C., Whitcomb, D.J., Jiao, S., Cho, K. and Sheng, M. (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell, 141, 859-871.
72. Klein, M.E., Lioy, D.T., Ma, L., Impey, S., Mandel, G. and Goodman, R.H. (2007) Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci., 10, 1513-1514.
73. Im, H.I., Hollander, J.A., Bali, P. and Kenny, P.J. (2010) MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat. Neurosci., 13, 1120-1127.
74. Smith, P.Y., Delay, C., Girard, J., Papon, M.A., Planel, E., Sergeant, N., Buee, L. and Hebert, S.S. (2011) MicroRNA-132 loss is associated with tau exon 10 inclusion in progressive supranuclear palsy. Hum. Mol. Genet., 20, 4016-4024.
75. Min, S.W., Cho, S.H., Zhou, Y., Schroeder, S., Haroutunian, V., Seeley, W.W., Huang, E.J., Shen, Y., Masliah, E., Mukherjee, C. et al. (2010) Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron, 67, 953-966.
76. Shaked, I., Meerson, A., Wolf, Y., Avni, R., Greenberg, D., Gilboa-Geffen, A. and Soreq, H. (2009) MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity, 31, 965-973.
77. Blalock, E.M., Geddes, J.W., Chen, K.C., Porter, N.M., Markesbery, W.R. and Landfield, P.W. (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc. Natl Acad. Sci. USA, 101, 2173-2178.
78. Bronner, I.F., Bochdanovits, Z., Rizzu, P., Kamphorst, W., Ravid, R., van Swieten, J.C. and Heutink, P. (2009) Comprehensive mRNA expression profiling distinguishes tauopathies and identifies shared molecular pathways. PLoS One, 4, e6826.
79. Qin, W., Zhao, W., Ho, L., Wang, J., Walsh, K., Gandy, S. and Pasinetti, G.M. (2008) Regulation of forkhead transcription factor FoxO3a contributes to calorie restriction-induced prevention of Alzheimer's disease-type amyloid neuropathology and spatial memory deterioration. Ann. N. Y. Acad. Sci., 1147, 335-347.
80. Picone, P., Giacomazza, D., Vetri, V., Carrotta, R., Militello, V., San Biagio, P.L. and Di Carlo, M. (2011) Insulin-activated Akt rescues Abeta oxidative stress-induced cell death by orchestrating molecular trafficking. Aging Cell, 10, 832-843.
81. Shang, Y.C., Chong, Z.Z., Hou, J. and Maiese, K. (2009) The forkhead transcription factor FOXO3a controls microglial inflammatory activation and eventual apoptotic injury through caspase 3. Curr. Neurovasc. Res., 6, 20-31.
82. Engidawork, E., Gulesserian, T., Seidl, R., Cairns, N. and Lubec, G. (2001) Expression of apoptosis related proteins in brains of patients with Alzheimer's disease. Neurosci. Lett., 303, 79-82.
83. Biswas, S.C., Shi, Y., Vonsattel, J.P., Leung, C.L., Troy, C.M. and Greene, L.A. (2007) Bim is elevated in Alzheimer's disease neurons and is required for beta-amyloid-induced neuronal apoptosis. J. Neurosci., 27, 893-900.
84. Morishima, Y., Gotoh, Y., Zieg, J., Barrett, T., Takano, H., Flavell, R., Davis, R.J., Shirasaki, Y. and Greenberg, M.E. (2001) Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J. Neurosci., 21, 7551-7560.
85. Su, J.H., Anderson, A.J., Cribbs, D.H., Tu, C., Tong, L., Kesslack, P. and Cotman, C.W. (2003) Fas and Fas ligand are associated with neuritic degeneration in the AD brain and participate in beta-amyloid-induced neuronal death. Neurobiol. Dis., 12, 182-193.
86. Kim, W.S., Bhatia, S., Elliott, D.A., Agholme, L., Kagedal, K., McCann, H., Halliday, G.M., Barnham, K.J. and Garner, B. (2010) Increased ATP-binding cassette transporter A1 expression in Alzheimer's disease hippocampal neurons. J. Alzheimers Dis., 21, 193-205.