Translating memories: The role of protein biosynthesis in synpatic plasticity

Protein Biosynthesis

Volumn , Issue , 2009, Pages 195-224

  Westmark, Cara J ^a   Malter, James S ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84895338139     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (241)

1. Hebb DO. (1949) The organization of behavior. New York: John Wiley and Sons.
2. Ramon y Cajal, S. (1989) Recollections of my life. Cambridge: The MIT Press.
3. Chen X, Vinade L, Leapman RD, Petersen JD, Nakagawa T, et al. (2005) Mass of the postsynaptic density and enumeration of three key molecules. Proc Natl Acad Sci U S A 102(32): 11551-11556.
4. Satoh K, Takeuchi M, Oda Y, Deguchi-Tawarada M, Sakamoto Y, et al. (2002) Identification of activity-regulated proteins in the postsynaptic density fraction. Genes Cells 7(2): 187-197.
5. Gong R, Park CS, Abbassi NR, Tang SJ. (2006) Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J Biol Chem 281(27): 18802-18815.
6. Banko JL, Hou L, Klann E. (2004) NMDA receptor activation results in PKA-and ERK-dependent Mnk1 activation and increased eIF4E phosphorylation in hippocampal area CA1. J Neurochem 91(2): 462-470.
7. Hou L, Klann E. (2004) Activation of the phosphoinositide 3-kinase-akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24(28): 6352-6361.
8. Klintsova AY, Greenough WT. (1999) Synaptic plasticity in cortical systems. Curr Opin Neurobiol 9(2): 203-208.
9. Kandel ER. (2001) The molecular biology of memory storage: A dialog between genes and synapses. Biosci Rep 21(5): 565-611.
10. Klann E, Dever TE. (2004) Biochemical mechanisms for translational regulation in synaptic plasticity. Nat Rev Neurosci 5(12): 931-942.
11. Kelleher RJ,3rd, Govindarajan A, Tonegawa S. (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44(1): 59-73.
12. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, et al. (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell 91(7): 927-938.
13. Frey U, Morris RG. (1997) Synaptic tagging and long-term potentiation. Nature 385(6616): 533-536.
14. Manahan-Vaughan D, Kulla A, Frey JU. (2000) Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J Neurosci 20(22): 8572-8576.
15. Steward O, Schuman EM. (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24: 299-325.
16. Sossin WS, DesGroseillers L. (2006) Intracellular trafficking of RNA in neurons. Traffic 7(12): 1581-1589.
17. Tiedge H, Bloom FE, Richter D. (2001) Molecular kinesis in cellular function and plasticity. Proc Natl Acad Sci U S A 98(13): 6997-6998.
18. Job C, Eberwine J. (2001) Identification of sites for exponential translation in living dendrites. Proc Natl Acad Sci U S A 98(23): 13037-13042.
19. Tiedge H, Brosius J. (1996) Translational machinery in dendrites of hippocampal neurons in culture. J Neurosci 16(22): 7171-7181.
20. Inamura N, Hoshino S, Uchiumi T, Nawa H, Takei N. (2003) Cellular and subcellular distributions of translation initiation, elongation and release factors in rat hippocampus. Brain Res Mol Brain Res 111(1-2): 165-174.
21. Ostroff LE, Fiala JC, Allwardt B, Harris KM. (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35(3): 535-545.
22. Steward O, Levy WB. (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2(3): 284-291.
23. Mader S, Lee H, Pause A, Sonenberg N. (1995) The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 15(9): 4990-4997.
24. Smart FM, Edelman GM, Vanderklish PW. (2003) BDNF induces translocation of initiation factor 4E to mRNA granules: Evidence for a role of synaptic microfilaments and integrins. Proc Natl Acad Sci U S A 100(24): 14403-14408.
25. Haghighat A, Mader S, Pause A, Sonenberg N. (1995) Repression of cap-dependent translation by 4E-binding protein 1: Competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J 14(22): 5701-5709.
26. Banko JL, Poulin F, Hou L, DeMaria CT, Sonenberg N, et al. (2005) The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci 25(42): 9581-9590.
27. Costa-Mattioli M, Gobert D, Stern E, Gamache K, Colina R, et al. (2007) eIF2alpha phosphorylation bidirectionally regulates the switch from short-to long-term synaptic plasticity and memory. Cell 129(1): 195-206.
28. Horton AC, Ehlers MD. (2003) Dual modes of endoplasmic reticulum-to-golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23(15): 6188-6199.
29. Gardiol A, Racca C, Triller A. (1999) Dendritic and postsynaptic protein synthetic machinery. J Neurosci 19(1): 168-179.
30. Pierce JP, van Leyen K, McCarthy JB. (2000) Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat Neurosci 3(4): 311-313.
31. Eberwine J, Belt B, Kacharmina JE, Miyashiro K. (2002) Analysis of subcellularly localized mRNAs using in situ hybridization, mRNA amplification, and expression profiling. Neurochem Res 27(10): 1065-1077.
32. Tian QB, Nakayama K, Okano A, Suzuki T. (1999) Identification of mRNAs localizing in the postsynaptic region. Brain Res Mol Brain Res 72(2): 147-157.
33. Zhong J, Zhang T, Bloch LM. (2006) Dendritic mRNAs encode diversified functionalities in hippocampal pyramidal neurons. BMC Neurosci 7: 17.
34. Matsumoto M, Setou M, Inokuchi K. (2007) Transcriptome analysis reveals the population of dendritic RNAs and their redistribution by neural activity. Neurosci Res 57(3): 411-423.
35. Steward O, Wallace CS, Lyford GL, Worley PF. (1998) Synaptic activation causes the mRNA for the IEG arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21(4): 741-751.
36. Steward O, Worley PF. (2001) A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci U S A 98(13): 7062-7068.
37. Mayford M, Baranes D, Podsypanina K, Kandel ER. (1996) The 3'-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci U S A 93(23): 13250-13255.
38. Blichenberg A, Schwanke B, Rehbein M, Garner CC, Richter D, et al. (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J Neurosci 19(20): 8818-8829.
39. Kislauskis EH, Zhu X, Singer RH. (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J Cell Biol 127(2): 441-451.
40. Sutton MA, Schuman EM. (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127(1): 49-58.
41. Huang EP. (1999) Synaptic plasticity: Regulated translation in dendrites. Curr Biol 9(5): R168-70.
42. Tang SJ, Schuman EM. (2002) Protein synthesis in the dendrite. Philos Trans R Soc Lond B Biol Sci 357(1420): 521-529.
43. Glanzer JG, Eberwine JH. (2003) Mechanisms of translational control in dendrites. Neurobiol Aging 24(8): 1105-1111.
44. Bramham CR, Wells DG. (2007) Dendritic mRNA: Transport, translation and function. Nat Rev Neurosci 8(10): 776-789.
45. Kiebler MA, Bassell GJ. (2006) Neuronal RNA granules: Movers and makers. Neuron 51(6): 685-690.
46. Kiebler MA, DesGroseillers L. (2000) Molecular insights into mRNA transport and local translation in the mammalian nervous system. Neuron 25(1): 19-28.
47. Krichevsky AM, Kosik KS. (2001) Neuronal RNA granules: A link between RNA localization and stimulation-dependent translation. Neuron 32(4): 683-696.
48. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, et al. (2002) Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36(3): 507-519.
49. Scheetz AJ, Nairn AC, Constantine-Paton M. (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3(3): 211-216.
50. Chen CY, Shyu AB. (1995) AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem Sci 20(11): 465-470.
51. Deshler JO, Highett MI, Abramson T, Schnapp BJ. (1998) A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol 8(9): 489-496.
52. Jang SK, Pestova TV, Hellen CU, Witherell GW, Wimmer E. (1990) Cap-independent translation of picornavirus RNAs: Structure and function of the internal ribosomal entry site. Enzyme 44(1-4): 292-309.
53. Paynton BV, Bachvarova R. (1994) Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol Reprod Dev 37(2): 172-180.
54. Myer VE, Fan XC, Steitz JA. (1997) Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J 16(8): 2130-2139.
55. Zhang W, Wagner BJ, Ehrenman K, Schaefer AW, DeMaria CT, et al. (1993) Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol 13(12): 7652-7665.
56. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ. (2000) Interactions of CCCH zinc finger proteins with mRNA. binding of tristetraprolin-related zinc finger proteins to au-rich elements and destabilization of mRNA. J Biol Chem 275(23): 17827-17837.
57. Gherzi R, Lee KY, Briata P, Wegmuller D, Moroni C, et al. (2004) A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14(5): 571-583.
58. Levy NS, Chung S, Furneaux H, Levy AP. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273(11): 6417-6423.
59. Fan XC, Steitz JA. (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17(12): 3448-3460.
60. Peng SS, Chen CY, Xu N, Shyu AB. (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17(12): 3461-3470.
61. Buzby JS, Brewer G, Nugent DJ. (1999) Developmental regulation of RNA transcript destabilization by A + U-rich elements is AUF1-dependent. J Biol Chem 274(48): 33973-33978.
62. Liao B, Hu Y, Brewer G. (2007) Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat Struct Mol Biol 14(6): 511-518.
63. Gu W, Pan F, Zhang H, Bassell GJ, Singer RH. (2002) A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J Cell Biol 156(1): 41-51.
64. Pinkstaff JK, Chappell SA, Mauro VP, Edelman GM, Krushel LA. (2001) Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc Natl Acad Sci U S A 98(5): 2770-2775.
65. Chiang PW, Carpenter LE, Hagerman PJ. (2001) The 5'-untranslated region of the FMR1 message facilitates translation by internal ribosome entry. J Biol Chem 276(41): 37916-37921.
66. Bence M, Arbuckle MI, Dickson KS, Grant SG. (2005) Analyses of murine postsynaptic density-95 identify novel isoforms and potential translational control elements. Brain Res Mol Brain Res 133(1): 143-152.
67. Todd PK, Mack KJ, Malter JS. (2003) The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci U S A 100(24): 14374-14378.
68. Rehbein M, Wege K, Buck F, Schweizer M, Richter D, et al. (2002) Molecular characterization of MARTA1, a protein interacting with the dendritic targeting element of MAP2 mRNAs. J Neurochem 82(5): 1039-1046.
69. Huang YS, Carson JH, Barbarese E, Richter JD. (2003) Facilitation of dendritic mRNA transport by CPEB. Genes Dev 17(5): 638-653.
70. Bassell GJ, Singer RH, Kosik KS. (1994) Association of poly(A) mRNA with microtubules in cultured neurons. Neuron 12(3): 571-582.
71. Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, et al. (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417(6884): 83-87.
72. Hirokawa N. (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26(27): 7139-7142.
73. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, et al. (2001) Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31(2): 261-275.
74. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, et al. (2001) Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31(2): 261-275.
75. Goetze B, Tuebing F, Xie Y, Dorostkar MM, Thomas S, et al. (2006) The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J Cell Biol 172(2): 221-231.
76. Tang SJ, Meulemans D, Vazquez L, Colaco N, Schuman E. (2001) A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32(3): 463-475.
77. Vickers CA, Wyllie DJ. (2007) Late-phase, protein synthesis-dependent long-term potentiation in hippocampal CA1 pyramidal neurones with destabilized microtubule networks. Br J Pharmacol 151(7): 1071-1077.
78. Stebbins-Boaz B, Richter JD. (1994) Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early xenopus development. Mol Cell Biol 14(9): 5870-5880.
79. Pique M, Lopez JM, Foissac S, Guigo R, Mendez R. (2008) A combinatorial code for CPE-mediated translational control. Cell 132(3): 434-448.
80. Jung MY, Lorenz L, Richter JD. (2006) Translational control by neuroguidin, a eukaryotic initiation factor 4E and CPEB binding protein. Mol Cell Biol 26(11): 4277-4287.
81. Du L, Richter JD. (2005) Activity-dependent polyadenylation in neurons. RNA 11(9): 1340-1347.
82. Knight SW, Bass BL. (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in caenorhabditis elegans. Science 293(5538): 2269-2271.
83. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409(6818): 363-366.
84. Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS, et al. (2004) Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci U S A 101(1): 360-365.
85. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, et al. (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439(7074): 283-289.
86. Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J, et al. (2004) Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 7(2): 113-117.
87. Kiebler MA, DesGroseillers L. (2000) Molecular insights into mRNA transport and local translation in the mammalian nervous system. Neuron 25(1): 19-28.
88. Guil S, Long JC, Caceres JF. (2006) hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol Cell Biol 26(15): 5744-5758.
89. Maggipinto M, Rabiner C, Kidd GJ, Hawkins AJ, Smith R, et al. (2004) Increased expression of the MBP mRNA binding protein HnRNP A2 during oligodendrocyte differentiation. J Neurosci Res 75(5): 614-623.
90. Anderson P, Kedersha N. (2006) RNA granules. J Cell Biol 172(6): 803-808.
91. Shiina N, Shinkura K, Tokunaga M. (2005) A novel RNA-binding protein in neuronal RNA granules: Regulatory machinery for local translation. J Neurosci 25(17): 4420-4434.
92. Brengues M, Teixeira D, Parker R. (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310(5747): 486-489.
93. Barbee SA, Estes PS, Cziko AM, Hillebrand J, Luedeman RA, et al. (2006) Staufen-and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52(6): 997-1009.
94. Lebeau G, Maher-Laporte M, Topolnik L, Laurent CE, Sossin W, et al. (2008) Staufen1 regulation of protein synthesis-dependent long-term potentiation and synaptic function in hippocampal pyramidal cells. Mol Cell Bio in press
95. Hillebrand J, Barbee SA, Ramaswami M. (2007) P-body components, microRNA regulation, and synaptic plasticity. ScientificWorldJournal 7: 178-190.
96. Richter JD. (2007) CPEB: A life in translation. Trends Biochem Sci 32(6): 279-285.
97. Minshall N, Thom G, Standart N. (2001) A conserved role of a DEAD box helicase in mRNA masking. RNA 7(12): 1728-1742.
98. Nakahata S, Katsu Y, Mita K, Inoue K, Nagahama Y, et al. (2001) Biochemical identification of xenopus pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a nanos homolog, xcat-2, and a cytoplasmic polyadenylation element-binding protein. J Biol Chem 276(24): 20945-20953.
99. Costa A, Wang Y, Dockendorff TC, Erdjument-Bromage H, Tempst P, et al. (2005) The drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. Dev Cell 8(3): 331-342.
100. Si K, Lindquist S, Kandel ER. (2003) A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115(7): 879-891.
101. McEvoy M, Cao G, Llopis PM, Kundel M, Jones K, et al. (2007) Cytoplasmic polyadenylation element binding protein 1-mediated mRNA translation in purkinje neurons is required for cerebellar long-term depression and motor coordination. J Neurosci 27(24): 6400-6411.
102. Bakker CE, de Diego Otero Y, Bontekoe C, Raghoe P, Luteijn T, et al. (2000) Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse. Exp Cell Res 258(1): 162-170.
103. Khandjian EW, Fortin A, Thibodeau A, Tremblay S, Cote F, et al. (1995) A heterogeneous set of FMR1 proteins is widely distributed in mouse tissues and is modulated in cell culture. Hum Mol Genet 4(5): 783-789.
104. Siomi MC, Zhang Y, Siomi H, Dreyfuss G. (1996) Specific sequences in the fragile X syndrome protein FMR1 and the FXR proteins mediate their binding to 60S ribosomal subunits and the interactions among them. Mol Cell Biol 16(7): 3825-3832.
105. Eberhart DE, Malter HE, Feng Y, Warren ST. (1996) The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum Mol Genet 5(8): 1083-1091.
106. Stefani G, Fraser CE, Darnell JC, Darnell RB. (2004) Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J Neurosci 24(33): 7272-7276.
107. Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, et al. (2003) The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112(3): 317-327.
108. Ceman S, Brown V, Warren ST. (1999) Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Mol Cell Biol 19(12): 7925-7932.
109. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, et al. (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107(4): 477-487.
110. Miyashiro KY, Beckel-Mitchener A, Purk TP, Becker KG, Barret T, et al. (2003) RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37(3): 417-431.
111. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U. (2001) Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10(4): 329-338.
112. Li Z, Zhang Y, Ku L, Wilkinson KD, Warren ST, et al. (2001) The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res 29(11): 2276-2283.
113. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, et al. (2002) Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11(24): 3007-3017.
114. Antar LN, Bassell GJ. (2003) Sunrise at the synapse: The FMRP mRNP shaping the synaptic interface. Neuron 37(4): 555-558.
115. Bagni C, Greenough WT. (2005) From mRNP trafficking to spine dysmorphogenesis: The roots of fragile X syndrome. Nat Rev Neurosci 6(5): 376-387.
116. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, et al. (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107(4): 489-499.
117. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, et al. (2003) CLIP identifies nova-regulated RNA networks in the brain. Science 302(5648): 1212-1215.
118. Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, et al. (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Natl Acad Sci U S A 94(10): 5395-5400.
119. Westmark CJ, Malter JS. (2007) FMRP mediates mGluR5-dependent translation of amyloid precursor protein. PLoS Biol 5(3): e52.
120. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290(5495): 1364-1368.
121. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, et al. (1997) Fragile X mental retardation protein: Nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17(5): 1539-1547.
122. Feng Y, Absher D, Eberhart DE, Brown V, Malter HE, et al. (1997) FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell 1(1): 109-118.
123. Lu R, Wang H, Liang Z, Ku L, O'donnell WT, et al. (2004) The fragile X protein controls microtubule-associated protein 1B translation and microtubule stability in brain neuron development. Proc Natl Acad Sci U S A 101(42): 15201-15206.
124. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, et al. (2002) Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11(24): 3007-3017.
125. Vanderklish PW, Edelman GM. (2005) Differential translation and fragile X syndrome. Genes Brain Behav 4(6): 360-384.
126. Jin P, Warren ST. (2003) New insights into fragile X syndrome: From molecules to neurobehaviors. Trends Biochem Sci 28(3): 152-158.
127. Levenson JM, Sweatt JD. (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6(2): 108-118.
128. Sara SJ, Vankov A, Herve A. (1994) Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory. Brain Res Bull 35(5-6): 457-465.
129. Chenal J, Pellerin L. (2007) Noradrenaline enhances the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of PI3K/Akt and the mTOR/S6K pathway. J Neurochem 102(2): 389-397.
130. Kokaia M, Asztely F, Olofsdotter K, Sindreu CB, Kullmann DM, et al. (1998) Endogenous neurotrophin-3 regulates short-term plasticity at lateral perforant path-granule cell synapses. J Neurosci 18(21): 8730-8739.
131. Shin CY, Kundel M, Wells DG. (2004) Rapid, activity-induced increase in tissue plasminogen activator is mediated by metabotropic glutamate receptor-dependent mRNA translation. J Neurosci 24(42): 9425-9433.
132. Yu TP, McKinney S, Lester HA, Davidson N. (2001) Gamma-aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses. Proc Natl Acad Sci U S A 98(9): 5264-5269.
133. Kang H, Schuman EM. (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273(5280): 1402-1406.
134. Aakalu G, Smith WB, Nguyen N, Jiang C, Schuman EM. (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30(2): 489-502.
135. Liao L, Pilotte J, Xu T, Wong CC, Edelman GM, et al. (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: An analysis using high-throughput proteomics. J Proteome Res 6(3): 1059-1071.
136. Bagni C, Mannucci L, Dotti CG, Amaldi F. (2000) Chemical stimulation of synaptosomes modulates alpha -Ca2+/calmodulin-dependent protein kinase II mRNA association to polysomes. J Neurosci 20(10): RC76.
137. Yin Y, Edelman GM, Vanderklish PW. (2002) The brain-derived neurotrophic factor enhances synthesis of arc in synaptoneurosomes. Proc Natl Acad Sci U S A 99(4): 2368-2373.
138. Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B. (1996) Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381(6584): 706-709.
139. Gooney M, Lynch MA. (2001) Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB. J Neurochem 77(5): 1198-1207.
140. Kanhema T, Dagestad G, Panja D, Tiron A, Messaoudi E, et al. (2006) Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: Evidence for compartment-specific translation control. J Neurochem 99(5): 1328-1337.
141. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME. (2004) BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci 24(33): 7366-7377.
142. Ali DW, Salter MW. (2001) NMDA receptor regulation by src kinase signalling in excitatory synaptic transmission and plasticity. Curr Opin Neurobiol 11(3): 336-342.
143. Kullmann DM, Erdemli G, Asztely F. (1996) LTP of AMPA and NMDA receptor-mediated signals: Evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17(3): 461-474.
144. O'Mara SM, Rowan MJ, Anwyl R. (1995) Metabotropic glutamate receptor-induced homosynaptic long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro. Neuropharmacology 34(8): 983-989.
145. Kalia LV, Gingrich JR, Salter MW. (2004) Src in synaptic transmission and plasticity. Oncogene 23(48): 8007-8016.
146. Huang Y, Lu W, Ali DW, Pelkey KA, Pitcher GM, et al. (2001) CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29(2): 485-496.
147. Huang YS, Jung MY, Sarkissian M, Richter JD. (2002) N-methyl-D-aspartate receptor signaling results in aurora kinase-catalyzed CPEB phosphorylation and alpha CaMKII mRNA polyadenylation at synapses. EMBO J 21(9): 2139-2148.
148. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, et al. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17(19): 7503-7522.
149. Dietrich D, Kral T, Clusmann H, Friedl M, Schramm J. (2002) Presynaptic group II metabotropic glutamate receptors reduce stimulated and spontaneous transmitter release in human dentate gyrus. Neuropharmacology 42(3): 297-305.
150. Hou L, Klann E. (2004) Activation of the phosphoinositide 3-kinase-akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24(28): 6352-6361.
151. Antion MD, Hou L, Wong H, Hoeffer CA, Klann E. (2008) mGluR-dependent long-term depression is associated with increased phosphorylation of S6 and synthesis of elongation factor 1A but remains expressed in S6K-deficient mice. Mol Cell Biol 28(9): 2996-3007.
152. Camodeca N, Breakwell NA, Rowan MJ, Anwyl R. (1999) Induction of LTD by activation of group I mGluR in the dentate gyrus in vitro. Neuropharmacology 38(10): 1597-1606.
153. Wu J, Rowan MJ, Anwyl R. (2004) Synaptically stimulated induction of group I metabotropic glutamate receptor-dependent long-term depression and depotentiation is inhibited by prior activation of metabotropic glutamate receptors and protein kinase C. Neuroscience 123(2): 507-514.
154. Polakiewicz RD, Schieferl SM, Gingras AC, Sonenberg N, Comb MJ. (1998) Mu-opioid receptor activates signaling pathways implicated in cell survival and translational control. J Biol Chem 273(36): 23534-23541.
155. Volk LJ, Pfeiffer BE, Gibson JR, Huber KM. (2007) Multiple gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 27(43): 11624-11634.
156. Chen N, Napoli JL. (2008) All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RARalpha. FASEB J 22(1): 236-245.
157. Yaka R, Thornton C, Vagts AJ, Phamluong K, Bonci A, et al. (2002) NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc Natl Acad Sci U S A 99(8): 5710-5715.
158. Ehlers MD. (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6(3): 231-242.
159. Ronesi JA, Huber KM. (2008) Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation. J Neurosci 28(2): 543-547.
160. Pfeiffer BE, Huber KM. (2006) Current advances in local protein synthesis and synaptic plasticity. J Neurosci 26(27): 7147-7150.
161. Parsons RG, Gafford GM, Helmstetter FJ. (2006) Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J Neurosci 26(50): 12977-12983.
162. Takei N, Inamura N, Kawamura M, Namba H, Hara K, et al. (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24(44): 9760-9769.
163. Brunn GJ, Hudson CC, Sekulic A, Williams JM, Hosoi H, et al. (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277(5322): 99-101.
164. Lawrence JC, Jr, Abraham RT. (1997) PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem Sci 22(9): 345-349.
165. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, et al. (1994) PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266(5185): 653-656.
166. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, et al. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 371(6500): 762-767.
167. Tsokas P, Ma T, Iyengar R, Landau EM, Blitzer RD. (2007) Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J Neurosci 27(22): 5885-5894.
168. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, et al. (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99(1): 467-472.
169. Shobe J. (2002) The role of PKA, CaMKII, and PKC in avoidance conditioning: Permissive or instructive? Neurobiol Learn Mem 77(3): 291-312.
170. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, et al. (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24(3): 715-726.
171. Yu TP, McKinney S, Lester HA, Davidson N. (2001) Gamma-aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses. Proc Natl Acad Sci U S A 98(9): 5264-5269.
172. Yanow SK, Manseau F, Hislop J, Castellucci VF, Sossin WS. (1998) Biochemical pathways by which serotonin regulates translation in the nervous system of aplysia. J Neurochem 70(2): 572-583.
173. Ling DS, Benardo LS, Serrano PA, Blace N, Kelly MT, et al. (2002) Protein kinase mzeta is necessary and sufficient for LTP maintenance. Nat Neurosci 5(4): 295-296.
174. Hernandez AI, Blace N, Crary JF, Serrano PA, Leitges M, et al. (2003) Protein kinase M zeta synthesis from a brain mRNA encoding an independent protein kinase C zeta catalytic domain. implications for the molecular mechanism of memory. J Biol Chem 278(41): 40305-40316.
175. Pollak DD, Herkner K, Hoeger H, Lubec G. (2005) Behavioral testing upregulates pCaMKII, BDNF, PSD-95 and egr-1 in hippocampus of FVB/N mice. Behav Brain Res 163(1): 128-135.
176. Davis S, Bozon B, Laroche S. (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 142(1-2): 17-30.
177. Taha S, Stryker MP. (2002) Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis. Neuron 34(3): 425-436.
178. Wells DG, Dong X, Quinlan EM, Huang YS, Bear MF, et al. (2001) A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J Neurosci 21(24): 9541-9548.
179. Atkins CM, Nozaki N, Shigeri Y, Soderling TR. (2004) Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J Neurosci 24(22): 5193-5201.
180. Hu Y, Zhang Y, Venkitaramani DV, Lombroso PJ. (2007) Translation of striatal-enriched protein tyrosine phosphatase (STEP) after beta1-adrenergic receptor stimulation. J Neurochem 103(2): 531-541.
181. Gelinas JN, Banko JL, Hou L, Sonenberg N, Weeber EJ, et al. (2007) ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J Biol Chem 282(37): 27527-27535.
182. Kelleher RJ,3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S. (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116(3): 467-479.
183. Gong R, Tang SJ. (2006) Mitogen-activated protein kinase signaling is essential for activity-dependent dendritic protein synthesis. Neuroreport 17(15): 1575-1578.
184. Kim SH, Markham JA, Weiler IJ, Greenough WT. (2008) Aberrant early-phase ERK inactivation impedes neuronal function in fragile X syndrome. Proc Natl Acad Sci U S A 105(11): 4429-4434.
185. Meng J, Meng Y, Hanna A, Janus C, Jia Z. (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J Neurosci 25(28): 6641-6650.
186. Barco A, Alarcon JM, Kandel ER. (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108(5): 689-703.
187. Costa-Mattioli M, Gobert D, Harding H, Herdy B, Azzi M, et al. (2005) Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436(7054): 1166-1173.
188. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6(5): 1099-1108.
189. Chotiner JK, Khorasani H, Nairn AC, O'Dell TJ, Watson JB. (2003) Adenylyl cyclase-dependent form of chemical long-term potentiation triggers translational regulation at the elongation step. Neuroscience 116(3): 743-752.
190. Hoeffer CA, Klann E. (2007) Switching gears: Translational mastery of transcription during memory formation. Neuron 54(2): 186-189.
191. Todd PK, Malter JS. (2002) Fragile X mental retardation protein in plasticity and disease. J Neurosci Res 70(5): 623-630.
192. Grossman AW, Aldridge GM, Weiler IJ, Greenough WT. (2006) Local protein synthesis and spine morphogenesis: Fragile X syndrome and beyond. J Neurosci 26(27): 7151-7155.
193. Hagerman RJ, Hagerman PJ. (2002) Physical and behavioral phenotype. Baltimore: John Hopkins University Press.: 3-109 p.
194. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, et al. (1997) Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits. Proc Natl Acad Sci U S A 94(10): 5401-5404.
195. Nimchinsky EA, Oberlander AM, Svoboda K. (2001) Abnormal development of dendritic spines in FMR1 knock-out mice. J Neurosci 21(14): 5139-5146.
196. Hinton VJ, Brown WT, Wisniewski K, Rudelli RD. (1991) Analysis of neocortex in three males with the fragile X syndrome. Am J Med Genet 41(3): 289-294.
197. Rudelli RD, Brown WT, Wisniewski K, Jenkins EC, Laure-Kamionowska M, et al. (1985) Adult fragile X syndrome. clinico-neuropathologic findings. Acta Neuropathol 67(3-4): 289-295.
198. Wisniewski KE, Segan SM, Miezejeski CM, Sersen EA, Rudelli RD. (1991) The fra(X) syndrome: Neurological, electrophysiological, and neuropathological abnormalities. Am J Med Genet 38(2-3): 476-480.
199. [Anonymous]. (1994) Fmr1 knockout mice: A model to study fragile X mental retardation. the dutch-belgian fragile X consortium. Cell 78(1): 23-33.
200. Irwin SA, Galvez R, Greenough WT. (2000) Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex 10(10): 1038-1044.
201. McKinney BC, Grossman AW, Elisseou NM, Greenough WT. (2005) Dendritic spine abnormalities in the occipital cortex of C57BL/6 Fmr1 knockout mice. Am J Med Genet B Neuropsychiatr Genet
202. Vanderklish PW, Edelman GM. (2002) Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci U S A 99(3): 1639-1644.
203. Huber KM, Roder JC, Bear MF. (2001) Chemical induction of mGluR5-and protein synthesis--dependent long-term depression in hippocampal area CA1. J Neurophysiol 86(1): 321-325.
204. Snyder EM, Philpot BD, Huber KM, Dong X, Fallon JR, et al. (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat Neurosci 4(11): 1079-1085.
205. Xiao MY, Zhou Q, Nicoll RA. (2001) Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology 41(6): 664-671.
206. Huber KM, Gallagher SM, Warren ST, Bear MF. (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci U S A 99(11): 7746-7750.
207. Nosyreva ED, Huber KM. (2006) Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J Neurophysiol 95(5): 3291-3295.
208. Hou L, Antion MD, Hu D, Spencer CM, Paylor R, et al. (2006) Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51(4): 441-454.
209. Godfraind JM, Reyniers E, De Boulle K, D'Hooge R, De Deyn PP, et al. (1996) Long-term potentiation in the hippocampus of fragile X knockout mice. Am J Med Genet 64(2): 246-251.
210. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, et al. (1999) Fragile X mouse: Strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 94(1): 185-192.
211. Shigematsu K, McGeer PL, McGeer EG. (1992) Localization of amyloid precursor protein in selective postsynaptic densities of rat cortical neurons. Brain Res 592(1-2): 353-357.
212. Torroja L, Packard M, Gorczyca M, White K, Budnik V. (1999) The drosophila beta-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J Neurosci 19(18): 7793-7803.
213. Yang G, Gong YD, Gong K, Jiang WL, Kwon E, et al. (2005) Reduced synaptic vesicle density and active zone size in mice lacking amyloid precursor protein (APP) and APP-like protein 2. Neurosci Lett 384(1-2): 66-71.
214. Akaaboune M, Allinquant B, Farza H, Roy K, Magoul R, et al. (2000) Developmental regulation of amyloid precursor protein at the neuromuscular junction in mouse skeletal muscle. Mol Cell Neurosci 15(4): 355-367.
215. Loffler J, Huber G. (1992) Beta-amyloid precursor protein isoforms in various rat brain regions and during brain development. J Neurochem 59(4): 1316-1324.
216. Moya KL, Benowitz LI, Schneider GE, Allinquant B. (1994) The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol 161(2): 597-603.
217. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, et al. (2003) APP processing and synaptic function. Neuron 37(6): 925-937.
218. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, et al. (2004) Synaptic targeting by alzheimer's-related amyloid beta oligomers. J Neurosci 24(45): 10191-10200.
219. Sokol DK, Chen D, Farlow MR, Dunn DW, Maloney B, et al. (2006) High levels of alzheimer beta-amyloid precursor protein (APP) in children with severely autistic behavior and aggression. J Child Neurol 21(6): 444-449.
220. Beyreuther K, Pollwein P, Multhaup G, Monning U, Konig G, et al. (1993) Regulation and expression of the alzheimer's beta/A4 amyloid protein precursor in health, disease, and down's syndrome. Ann N Y Acad Sci 695: 91-102.
221. Wisniewski KE, Wisniewski HM, Wen GY. (1985) Occurrence of neuropathological changes and dementia of alzheimer's disease in down's syndrome. Ann Neurol 17(3): 278-282.
222. Denman R, Potempska A, Wolfe G, Ramakrishna N, Miller DL. (1991) Distribution and activity of alternatively spliced alzheimer amyloid peptide precursor and scrapie PrP mRNAs on rat brain polysomes. Arch Biochem Biophys 288(1): 29-38.
223. Schuman EM, Dynes JL, Steward O. (2006) Synaptic regulation of translation of dendritic mRNAs. J Neurosci 26(27): 7143-7146.
224. Rogers JT, Leiter LM, McPhee J, Cahill CM, Zhan SS, et al. (1999) Translation of the alzheimer amyloid precursor protein mRNA is up-regulated by interleukin-1 through 5'-untranslated region sequences. J Biol Chem 274(10): 6421-6431.
225. Todd PK, Malter JS, Mack KJ. (2003) Whisker stimulation-dependent translation of FMRP in the barrel cortex requires activation of type I metabotropic glutamate receptors. Brain Res Mol Brain Res 110(2): 267-278.
226. Ceman S, O'Donnell WT, Reed M, Patton S, Pohl J, et al. (2003) Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum Mol Genet 12(24): 3295-3305.
227. Darnell JC, Fraser CE, Mostovetsky O, Stefani G, Jones TA, et al. (2005) Kissing complex RNAs mediate interaction between the fragile-X mental retardation protein KH2 domain and brain polyribosomes. Genes Dev 19(8): 903-918.
228. Chen L, Yun SW, Seto J, Liu W, Toth M. (2003) The fragile X mental retardation protein binds and regulates a novel class of mRNAs containing U rich target sequences. Neuroscience 120(4): 1005-1017.
229. Dolzhanskaya N, Sung YJ, Conti J, Currie JR, Denman RB. (2003) The fragile X mental retardation protein interacts with U-rich RNAs in a yeast three-hybrid system. Biochem Biophys Res Commun 305(2): 434-441.
230. Singh K, Gaur P, Prasad S. (2006) Fragile x mental retardation (fmr-1) gene expression is down regulated in brain of mice during aging. Mol Biol Rep
231. Nalbantoglu J, Tirado-Santiago G, Lahsaini A, Poirier J, Goncalves O, et al. (1997) Impaired learning and LTP in mice expressing the carboxy terminus of the alzheimer amyloid precursor protein. Nature 387(6632): 500-505.
232. Murphree LJ, Rundhaugen LM, Kelly KM. (2007) Animal models of geriatric epilepsy. Int Rev Neurobiol 81: 29-40.
233. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, et al. (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of alzheimer's disease. Neuron 55(5): 697-711.
234. Hauser WA, Morris ML, Heston LL, Anderson VE. (1986) Seizures and myoclonus in patients with alzheimer's disease. Neurology 36(9): 1226-1230.
235. Hesdorffer DC, Hauser WA, Annegers JF, Kokmen E, Rocca WA. (1996) Dementia and adult-onset unprovoked seizures. Neurology 46(3): 727-730.
236. Amatniek JC, Hauser WA, DelCastillo-Castaneda C, Jacobs DM, Marder K, et al. (2006) Incidence and predictors of seizures in patients with alzheimer's disease. Epilepsia 47(5): 867-872.
237. Mendez M, Lim G. (2003) Seizures in elderly patients with dementia: Epidemiology and management. Drugs Aging 20(11): 791-803.
238. Hauser WA, Annegers JF, Kurland LT. (1993) Incidence of epilepsy and unprovoked seizures in rochester, minnesota: 1935-1984. Epilepsia 34(3): 453-468.
239. Chen L, Toth M. (2001) Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 103(4): 1043-1050.
240. Westmark CJ, Westmar PR, Beard AM, Hildebrandt SM, Malter JS. (2007) Seizure susceptibility and mortality in mice that over-express amyloid precursor protein. IJCEP 1(2): 157.
241. Westmark CJ, Westmark PR, Malter JS. (2008) Manuscript in preparation.