From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome (original) (raw)
Oberle, I. et al. Instability of a 550-base pair DNA segment and abnormal methylation in fragile X syndrome. Science252, 1097–1102 (1991). CASPubMed Google Scholar
Hagerman, P. J. & Hagerman, R. J. Fragile X-associated tremor/ataxia syndrome (FXTAS). Ment. Retard. Dev. Disabil. Res. Rev.10, 25–30 (2004). PubMed Google Scholar
Hinton, V. J., Brown, W. T., Wisniewski, K. & Rudelli, R. D. Analysis of neocortex in three males with the fragile X syndrome. Am. J. Med. Genet.41, 289–294 (1991). CASPubMed Google Scholar
Comery, T. A. et al. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl Acad. Sci. USA94, 5401–5404 (1997). CASPubMedPubMed Central Google Scholar
Irwin, S. A. et al. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am. J. Med. Genet.98, 161–167 (2001). Provides the most thorough and the only quantitative description of the human fragile X cortical neuronal morphological phenotype. CASPubMed Google Scholar
Nimchinsky, E. A., Oberlander, A. M. & Svoboda, K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci.21, 5139–5146 (2001). CASPubMedPubMed Central Google Scholar
Greenough, W. T. et al. Synaptic regulation of protein synthesis and the fragile X protein. Proc. Natl Acad. Sci. USA98, 7101–7106 (2001). CASPubMedPubMed Central Google Scholar
Coss, R. G. & Perkel, D. H. The function of dendritic spines: a review of theoretical issues. Behav. Neural Biol.44, 151–185 (1985). CASPubMed Google Scholar
Nimchinsky, E. A., Sabatini, B. L. & Svoboda, K. Structure and function of dendritic spines. Annu. Rev. Physiol.64, 313–353 (2002). CASPubMed Google Scholar
Campbell, D. S. & Holt, C. E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron32, 1013–1026 (2001). CASPubMed Google Scholar
Steward, O. & Schuman, E. M. Compartmentalized synthesis and degradation of proteins in neurons. Neuron40, 347–359 (2003). CASPubMed Google Scholar
Van de Bor, V. & Davis, I. mRNA localisation gets more complex. Curr. Opin. Cell Biol.16, 300–307 (2004). CASPubMed Google Scholar
Farina, K. L. & Singer, R. H. The nuclear connection in RNA transport and localization. Trends Cell Biol.12, 466–472 (2002). CASPubMed Google Scholar
Gu, W., Pan, F., Zhang, H., Bassell, G. J. & Singer, R. H. A predominantly nuclear protein affecting cytoplasmic localization of β-actin mRNA in fibroblasts and neurons. J. Cell Biol.156, 41–51 (2002). CASPubMedPubMed Central Google Scholar
Ainger, K. et al. Transport and localization elements in myelin basic protein mRNA. J. Cell Biol.138, 1077–1087 (1997). CASPubMedPubMed Central Google Scholar
Shan, J., Munro, T. P., Barbarese, E., Carson, J. H. & Smith, R. A molecular mechanism for mRNA trafficking in neuronal dendrites. J. Neurosci.23, 8859–8866 (2003). CASPubMedPubMed Central Google Scholar
Deshler, J. O., Highett, M. I. & Schnapp, B. J. Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science276, 1128–1131 (1997). CASPubMed Google Scholar
Ross, A. F., Oleynikov, Y., Kislauskis, E. H., Taneja, K. L. & Singer, R. H. Characterization of a β-actin mRNA zipcode-binding protein. Mol. Cell Biol.17, 2158–2165 (1997). CASPubMedPubMed Central Google Scholar
Tiruchinapalli, D. M. et al. Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and β-actin mRNA in dendrites and spines of hippocampal neurons. J. Neurosci.23, 3251–3261 (2003). CASPubMedPubMed Central Google Scholar
Kislauskis, E. H., Zhu, X. & Singer, R. H. Sequences responsible for intracellular localization of β-actin messenger RNA also affect cell phenotype. J. Cell Biol.127, 441–451 (1994). CASPubMed Google Scholar
Palacios, I. M., Gatfield, D., St Johnston, D. & Izaurralde, E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature427, 753–757 (2004). Shows that the translation-initiation factor eIF4AIII is a component of the oskar mRNP localization complex inD. melanogaster. Moreover, the same factor is also involved in nonsense-mediated mRNA decay in mammals. CASPubMed Google Scholar
Singh, G. & Lykke-Andersen, J. New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem. Sci.28, 464–466 (2003). CASPubMed Google Scholar
Holbrook, J. A., Neu-Yilik, G., Hentze, M. W. & Kulozik, A. E. Nonsense-mediated decay approaches the clinic. Nature Genet.36, 801–808 (2004). CASPubMed Google Scholar
Weiler, I. J. et al. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl Acad. Sci. USA94, 5395–5400 (1997). Initial description of neurotransmitter activation of FMRP synthesis at the synapse (see also reference 25). CASPubMedPubMed Central Google Scholar
Weiler, I. J. et al. From the cover: fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses. Proc. Natl Acad. Sci. USA101, 17504–17509 (2004). CASPubMedPubMed Central Google Scholar
Verheij, C. et al. Characterization and localization of the FMR-1 gene product associated with fragile X syndrome. Nature363, 722–724 (1993). CASPubMed Google Scholar
Eberhart, D. E., Malter, H. E., Feng, Y. & Warren, S. T. The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum. Mol. Genet.5, 1083–1091 (1996). An initial, detailed characterization of FMRP. CASPubMed Google Scholar
Feng, Y. et al. Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci.17, 1539–1547 (1997). CASPubMedPubMed Central Google Scholar
Khandjian, E. W. et al. Novel isoforms of the fragile X related protein FXR1P are expressed during myogenesis. Hum. Mol. Genet.7, 2121–2128 (1998). CASPubMed Google Scholar
Ceman, S., Brown, V. & Warren, S. T. 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, 7925–7932 (1999). CASPubMedPubMed Central Google Scholar
Bardoni, B. et al. NUFIP1 (nuclear FMRP interacting protein 1) is a nucleocytoplasmic shuttling protein associated with active synaptoneurosomes. Exp. Cell Res.289, 95–107 (2003). CASPubMed Google Scholar
Ceman, S., Nelson, R. & Warren, S. T. Identification of mouse YB1/p50 as a component of the FMRP-associated mRNP particle. Biochem. Biophys. Res. Commun.279, 904–908 (2000). CASPubMed Google Scholar
Stickeler, E. et al. The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J.20, 3821–3830 (2001). CASPubMedPubMed Central Google Scholar
Nekrasov, M. P. et al. The mRNA-binding protein YB-1 (p50) prevents association of the eukaryotic initiation factor eIF4G with mRNA and inhibits protein synthesis at the initiation stage. J. Biol. Chem.278, 13936–13943 (2003). CASPubMed Google Scholar
Sittler, A., Devys, D., Weber, C. & Mandel, J. L. Alternative splicing of exon 14 determines nuclear or cytoplasmic localisation of fmr1 protein isoforms. Hum. Mol. Genet.5, 95–102 (1996). CASPubMed Google Scholar
De Boulle, K. et al. A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nature Genet.3, 31–35 (1993). CASPubMed Google Scholar
Tamanini, F. et al. Different targets for the fragile X-related proteins revealed by their distinct nuclear localizations. Hum. Mol. Genet.8, 863–869 (1999). CASPubMed Google Scholar
Nakamura, M. et al. When overexpressed, a novel centrosomal protein, RanBPM, causes ectopic microtubule nucleation similar to γ-tubulin. J. Cell Biol.143, 1041–1052 (1998). CASPubMedPubMed Central Google Scholar
Menon, R. P., Gibson, T. J. & Pastore, A. The C terminus of fragile X mental retardation protein interacts with the multi-domain Ran-binding protein in the microtubule-organising centre. J. Mol. Biol.343, 43–53 (2004). CASPubMed Google Scholar
Hoelz, A. & Blobel, G. Cell biology: popping out of the nucleus. Nature432, 815–816 (2004). CASPubMed Google Scholar
Greenbaum, L., Katcoff, D. J., Dou, H., Gozlan, Y. & Malik, Z. A porphobilinogen deaminase (PBGD) Ran-binding protein interaction is implicated in nuclear trafficking of PBGD in differentiating glioma cells. Oncogene22, 5221–5228 (2003). CASPubMed Google Scholar
Ashley, C. T. et al. Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG-repeat. Nature Genet.4, 244–251 (1993). CASPubMed Google Scholar
Zalfa, F. et al. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell112, 317–327 (2003). This work reveals an intriguing mechanism by which FMRP regulates the translation of some neuronal mRNAs at synapses through the small non-coding RNA BC1. This RNA functions as an 'adaptor molecule' between FMRP and its mRNA targets. The FMRP–mRNA target interaction can be inhibited using a chemically synthesized oligo against BC1 RNA. CASPubMed Google Scholar
Jin, P. et al. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neurosci.7, 113–117 (2004). CASPubMed Google Scholar
He, L. & Hannon, G. J. MicroRNAs: small RNAs with a big role in gene regulation. Nature Rev. Genet.5, 522–531 (2004). CASPubMed Google Scholar
Jenuwein, T. Molecular biology. An RNA-guided pathway for the epigenome. Science297, 2215–2218 (2002). CASPubMed Google Scholar
Bao, N., Lye, K. W. & Barton, M. K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell7, 653–662 (2004). CASPubMed Google Scholar
Matzke, M. A. & Birchler, J. A. RNAi-mediated pathways in the nucleus. Nature Rev. Genet.6, 24–35 (2005). CASPubMed Google Scholar
Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C. & Bassell, G. J. Metabotropic glutamate receptor activation regulates fragile X mental retardation protein and Fmr1 mRNA localization differentially in dendrites and at synapses. J. Neurosci.24, 2648–2655 (2004). Shows clearly, for the first time, evidence of activity-dependent regulation of FMRP andFMR1mRNA trafficking in dendrites and synapses. In particular, the authors show that synaptic activation through the mGluR5 receptor regulates the localization of FMRP andFMR1mRNA in dendrites. CASPubMedPubMed Central Google Scholar
Miyashiro, K. Y. et al. RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron37, 417–431 (2003). CASPubMed Google Scholar
Steward, O., Bakker, C. E., Willems, P. J. & Oostra, B. A. No evidence for disruption of normal patterns of mRNA localization in dendrites or dendritic transport of recently synthesized mRNA in FMR1 knockout mice, a model for human fragile-X mental retardation syndrome. Neuroreport9, 477–481 (1998). CASPubMed Google Scholar
Kanai, Y., Dohmae, N. & Hirokawa, N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron43, 513–525 (2004). A thorough description and functional assessment of the composition of granules that contain FMRP and transport its mRNAs (see also references 49,60). They identified more than 40 proteins including Staufen, FMRP and other factors involved in protein synthesis. In addition, they showed the presence of α-CaMKII and ARC mRNAs in these granules. CASPubMed Google Scholar
Rackham, O. & Brown, C. M. Visualization of RNA–protein interactions in living cells: FMRP and IMP1 interact on mRNAs. EMBO J.23, 3346–3355 (2004). CASPubMedPubMed Central Google Scholar
Ling, S. C., Fahrner, P. S., Greenough, W. T. & Gelfand, V. I. Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc. Natl Acad. Sci. USA101, 17428–17433 (2004). CASPubMedPubMed Central Google Scholar
Schrier, M. et al. Transport kinetics of FMRP containing the I304N mutation of severe fragile X syndrome in neurites of living rat PC12 cells. Exp. Neurol.189, 343–353 (2004). CASPubMed Google Scholar
Clarke, N. F., Mowat, D., Kooy, R. F., Reyniers, E. & Willemsen, R. Fragile X syndrome phenotype with normal FMR1 gene studies. Am. J. Med. Genet. A.129, 326–328 (2004). Google Scholar
Zhang, Y. et al. The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J.14, 5358–5366 (1995). CASPubMedPubMed Central Google Scholar
Schenck, A., Bardoni, B., Moro, A., Bagni, C. & Mandel, J. L. A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc. Natl Acad. Sci. USA98, 8844–8849 (2001). The authors characterized two cytoplasmic FMRP-interacting proteins, both of which are also present at synapses.This work represents one of the first links between FMRP and the cytoskeleton (see also reference 68). CASPubMedPubMed Central Google Scholar
Bardoni, B. & Mandel, J. L. Advances in understanding of fragile X pathogenesis and FMRP function, and in identification of X linked mental retardation genes. Curr. Opin. Genet. Dev.12, 284–293 (2002). CASPubMed Google Scholar
Ohashi, S. et al. Identification of mRNA/protein (mRNP) complexes containing Purα, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem.277, 37804–37810 (2002). Shows that a possible molecular machinery containing PURα, Staufen, myosin VA and FMRP might be involved in the regulatation of dendritic transport. CASPubMed Google Scholar
Villace, P., Marion, R. M. & Ortin, J. The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res.32, 2411–2420 (2004). CASPubMedPubMed Central Google Scholar
Siomi, M. C., Zhang, Y., Siomi, H. & Dreyfuss, G. 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, 3825–3832 (1996). CASPubMedPubMed Central Google Scholar
Adinolfi, S. et al. The N-terminus of the fragile X mental retardation protein contains a novel domain involved in dimerization and RNA binding. Biochemistry42, 10437–10444 (2003). CASPubMed Google Scholar
Agulhon, C. et al. Expression of FMR1, FXR1, and FXR2 genes in human prenatal tissues. J. Neuropathol. Exp. Neurol.58, 867–880 (1999). CASPubMed Google Scholar
Sreeram, N., Wren, C., Bhate, M., Robertson, P. & Hunter, S. Cardiac abnormalities in the fragile X syndrome. Br. Heart J.61, 289–291 (1989). CASPubMedPubMed Central Google Scholar
Mientjes, E. J. et al. Fxr1 knockout mice show a striated muscle phenotype: implications for Fxr1p function in vivo. Hum. Mol. Genet.13, 1291–1302 (2004). CASPubMed Google Scholar
Kobayashi, K. et al. p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J. Biol. Chem.273, 291–295 (1998). CASPubMed Google Scholar
Schenck, A. et al. CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron38, 887–898 (2003). CASPubMed Google Scholar
Bardoni, B. et al. 82-FIP, a novel FMRP (fragile X mental retardation protein) interacting protein, shows a cell cycle-dependent intracellular localization. Hum. Mol. Genet.12, 1689–1698 (2003). CASPubMed Google Scholar
Kohrmann, M. et al. Microtubule-dependent recruitment of Staufen–green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell10, 2945–2953 (1999). CASPubMedPubMed Central Google Scholar
Li, Y. et al. Pur α protein implicated in dendritic RNA transport interacts with ribosomes in neuronal cytoplasm. Biol. Pharm. Bull.24, 231–235 (2001). CASPubMed Google Scholar
Duchaine, T. F. et al. Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. J. Cell Sci.115, 3285–3295 (2002). CASPubMed Google Scholar
Ohashi, S. et al. The single-stranded DNA- and RNA-binding proteins pur α and pur β link BC1 RNA to microtubules through binding to the dendrite-targeting RNA motifs. J. Neurochem.75, 1781–1790 (2000). CASPubMed Google Scholar
Mallardo, M. et al. Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl Acad. Sci. USA100, 2100–2105 (2003). CASPubMedPubMed Central Google Scholar
Pastural, E. et al. Two genes are responsible for Griscelli syndrome at the same 15q21 locus. Genomics63, 299–306 (2000). CASPubMed Google Scholar
Siomi, M. C. et al. FXR1, an autosomal homolog of the fragile X mental retardation gene. EMBO J.14, 2401–2408 (1995). CASPubMedPubMed Central Google Scholar
Adinolfi, S. et al. Dissecting FMR1, the protein responsible for fragile X syndrome, in its structural and functional domains. RNA5, 1248–1258 (1999). CASPubMedPubMed Central Google Scholar
Brown, V. et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell107, 477–487 (2001). CASPubMed Google Scholar
Darnell, J. C. et al. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell107, 489–499 (2001). Describes an approach to identifying mRNA 'cargoes' of FMRP (see also references 50,78,80). CASPubMed Google Scholar
Chen, L., Yun, S. W., Seto, J., Liu, W. & Toth, M. The fragile X mental retardation protein binds and regulates a novel class of mRNAs containing U rich target sequences. Neuroscience120, 1005–1017 (2003). CASPubMed Google Scholar
Zhang, Y. Q. et al. Drosophila fragile X-related gene regulates the MAP1B homolog futsch to control synaptic structure and function. Cell107, 591–603 (2001). CASPubMed Google Scholar
Schaeffer, C. et al. The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J.20, 4803–4813 (2001). CASPubMedPubMed Central Google Scholar
Hessl, D., Rivera, S. M. & Reiss, A. L. The neuroanatomy and neuroendocrinology of fragile X syndrome. Ment. Retard. Dev. Disabil. Res. Rev.10, 17–24 (2004). PubMed Google Scholar
Ramos, A., Hollingworth, D. & Pastore, A. G-quartet-dependent recognition between the FMRP RGG box and RNA. RNA9, 1198–1207 (2003). CASPubMedPubMed Central Google Scholar
Rozhdestvensky, T. S., Kopylov, A. M., Brosius, J. & Huttenhofer, A. Neuronal BC1 RNA structure: evolutionary conversion of a tRNA(Ala) domain into an extended stem-loop structure. RNA7, 722–730 (2001). CASPubMedPubMed Central Google Scholar
Gabus, C., Mazroui, R., Tremblay, S., Khandjian, E. W. & Darlix, J. L. The fragile X mental retardation protein has nucleic acid chaperone properties. Nucleic Acids Res.32, 2129–2137 (2004). CASPubMedPubMed Central Google Scholar
Caudy, A. A., Myers, M., Hannon, G. J. & Hammond, S. M. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev.16, 2491–2496 (2002). This study provides the first evidence that theD. melanogasterFMRP is part of the RNAi-related machinery (see also reference 88). CASPubMedPubMed Central Google Scholar
Ishizuka, A., Siomi, M. C. & Siomi, H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev.16, 2497–2508 (2002). The authors of this study suggest a model in which the RNAi pathway andD. melanogasterFMRP-mediated translational control intersect with each other (see also reference 86). CASPubMedPubMed Central Google Scholar
Gebauer, F. & Hentze, M. W. Molecular mechanisms of translational control. Nature Rev. Mol. Cell Biol.5, 827–835 (2004). CAS Google Scholar
Chapman, R. E. & Walter, P. Translational attenuation mediated by an mRNA intron. Curr. Biol.7, 850–859 (1997). CASPubMed Google Scholar
Kedersha, N. & Anderson, P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans.30, 963–969 (2002). CASPubMed Google Scholar
Krichevsky, A. M. & Kosik, K. S. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron32, 683–696 (2001). CASPubMed Google Scholar
Antic, D. & Keene, J. D. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J. Cell Sci.111, 183–197 (1998). CASPubMed Google Scholar
Khandjian, E. W., Corbin, F., Woerly, S. & Rousseau, F. The fragile X mental retardation protein is associated with ribosomes. Nature Genet.12, 91–93 (1996). CASPubMed Google Scholar
Stefani, G., Fraser, C. E., Darnell, J. C. & Darnell R. B. Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J. Neurosci.24, 7272–7276 (2004). CASPubMedPubMed Central Google Scholar
Ceman, S. et al. Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum. Mol. Genet.12, 3295–3305 (2003). CASPubMed Google Scholar
Aschrafi, A., Cunningham, B. A., Edelman, G. M. & Vanderklish, P. W. The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain. Proc. Natl Acad. Sci. USA102, 2180–2185 (2005). CASPubMedPubMed Central Google Scholar
Purpura, D. P. Dendritic spine 'dysgenesis' and mental retardation. Science186, 1126–1128 (1974). CASPubMed Google Scholar
Marin-Padilla, M. Structural abnormalities of the cerebral cortex in human chromosomal aberrations: a Golgi study. Brain Res.44, 625–629 (1972). CASPubMed Google Scholar
Wisniewski, K. E. et al. Fragile X syndrome: associated neurological abnormalities and developmental disabilities. Ann. Neurol.18, 665–669 (1985). CASPubMed Google Scholar
Rudelli, R. D. et al. Adult fragile X syndrome. Clinico-neuropathologic findings. Acta Neuropathol. (Berl.)67, 289–295 (1985). CAS Google Scholar
McKinney, B. C., Grossman, A. W., Elisseou, N. M. & Greenough, W. T. Dendritic spine abnormalities in the occipital cortex of C57BL/6 Fmr1 knockout mice. Am. J. Med. Genet. (in the press).
Bakker, C. E. et al. Fmr1 knockout mice: a model to study fragile X mental retardation. Cell78, 23–33 (1994). Google Scholar
Braun, K. & Segal, M. FMRP involvement in formation of synapses among cultured hippocampal neurons. Cereb. Cortex10, 1045–1052 (2000). CASPubMed Google Scholar
Galvez, R. & Greenough, W. T. Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am. J. Med. Genet. (in the press).
Greenough, W. T. & Chang, F. L. Dendritic pattern formation involves both oriented regression and oriented growth in the barrels of mouse somatosensory cortex. Brain Res.471, 148–152 (1988). CASPubMed Google Scholar
Huttenlocher, P. R. & Dabholkar, A. S. Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol.387, 167–178 (1997). CASPubMed Google Scholar
Galvez, R., Gopal, A. R. & Greenough, W. T. Somatosensory cortical barrel dendritic abnormalities in a mouse model of the fragile X mental retardation syndrome. Brain Res.971, 83–89 (2003). Evidence that synaptic pruning deficiencies give rise to the neuronal phenotype of fragile X syndrome. CASPubMed Google Scholar
Volkmar, F. R. & Greenough, W. T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science176, 1145–1147 (1972). Google Scholar
van Praag, H., Kempermann, G. & Gage, F. H. Neural consequences of environmental enrichment. Nature Rev. Neurosci.1, 191–198 (2000). CAS Google Scholar
Benaroya-Milshtein, N. et al. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur. J. Neurosci.20, 1341–1347 (2004). CASPubMed Google Scholar
Schrijver, N. C., Bahr, N. I., Weiss, I. C. & Wurbel, H. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol. Biochem. Behav.73, 209–224 (2002). CASPubMed Google Scholar
Moser, M. B., Trommald, M., Egeland, T. & Andersen, P. Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. J. Comp. Neurol.380, 373–381 (1997). CASPubMed Google Scholar
Lee, E. H., Hsu, W. L., Ma, Y. L., Lee, P. J. & Chao, C. C. Enrichment enhances the expression of sgk, a glucocorticoid-induced gene, and facilitates spatial learning through glutamate AMPA receptor mediation. Eur. J. Neurosci.18, 2842–2852 (2003). PubMed Google Scholar
Greenough, W. T., Yuwiler, A. & Dollinger, M. Effects of posttrial eserine administration on learning in 'enriched'- and 'impoverished'-reared rats. Behav. Biol.8, 261–272 (1973). CASPubMed Google Scholar
Diamond, M. C. & Connor, J. R. Jr. Plasticity of the aging cerebral cortex. Exp. Brain Res.5 (suppl.), 36–44 (1982). PubMed Google Scholar
Turner, A. M. & Greenough, W. T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res.329, 195–203 (1985). CASPubMed Google Scholar
Irwin, S. A. et al. Evidence for altered Fragile-X mental retardation protein expression in response to behavioral stimulation. Neurobiol. Learn. Mem.74, 87–93 (2000). CASPubMed Google Scholar
Todd, P. K. & Mack, K. J. Sensory stimulation increases cortical expression of the fragile X mental retardation protein in vivo. Brain Res. Mol. Brain Res.80, 17–25 (2000). CASPubMed Google Scholar
Ostroff, L. E., Fiala, J. C., Allwardt, B. & Harris, K. M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron35, 535–545 (2002). A landmark study on how dendritic protein synthesis might stabilize the growth of the postsynaptic density, including an increase in the number of ribosomes, after the induction of LTP by tetanic stimulation. CASPubMed Google Scholar
Chang, F. L. & Greenough, W. T. Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res.309, 35–46 (1984). CASPubMed Google Scholar
Greenough, W. T., Hwang, H. M. & Gorman, C. Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc. Natl Acad. Sci. USA82, 4549–4552 (1985). CASPubMedPubMed Central Google Scholar
Huber, K. M., Gallagher, S. M., Warren, S. T. & Bear, M. F. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl Acad. Sci. USA99, 7746–7750 (2002). CASPubMedPubMed Central Google Scholar
Li, J., Pelletier, M. R., Perez Velazquez, J. L. & Carlen, P. L. Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Mol. Cell Neurosci.19, 138–151 (2002). PubMed Google Scholar
Snyder, E. M. et al. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nature Neurosci.4, 1079–1085 (2001). CASPubMed Google Scholar
Vanderklish, P. W. & Edelman, G. M. Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc. Natl Acad. Sci. USA99, 1639–1644 (2002). CASPubMedPubMed Central Google Scholar
Bear, M. F., Huber, K. M. & Warren, S. T. The mGluR theory of fragile X mental retardation. Trends Neurosci.27, 370–377 (2004). CASPubMed Google Scholar
Godfraind, J. M. et al. Long-term potentiation in the hippocampus of fragile X knockout mice. Am. J. Med. Genet.64, 246–251 (1996). Initial evidence for a direct effect ofFMR1knockout on a widely studied model of learning and memory (see also reference 122). CASPubMed Google Scholar
Siomi, H., Siomi, M. C., Nussbaum, R. L. & Dreyfuss, G. The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell74, 291–298 (1993). CASPubMed Google Scholar
Adinolfi, S. et al. Novel RNA-binding motif: the KH module. Biopolymers51, 153–164 (1999). CASPubMed Google Scholar
Gibson, T. J., Thompson, J. D. & Heringa, J. The KH domain occurs in a diverse set of RNA-binding proteins that include the antiterminator NusA and is probably involved in binding to nucleic acid. FEBS Lett.324, 361–366 (1993). CASPubMed Google Scholar
Lewis, H. A. et al. Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell100, 323–332 (2000). CASPubMed Google Scholar
Duncan, R. et al. A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNA-binding motif. Genes Dev.8, 465–480 (1994). CASPubMed Google Scholar
Michelotti, E. F., Michelotti, G. A., Aronsohn, A. I. & Levens, D. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell Biol.16, 2350–2360 (1996). CASPubMedPubMed Central Google Scholar
Kiledjian, M. & Dreyfuss, G. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J.11, 2655–2664 (1992). CASPubMedPubMed Central Google Scholar
Zhang, S. & Grosse, F. Domain structure of human nuclear DNA helicase II (RNA helicase A). J. Biol. Chem.272, 11487–11494 (1997). CASPubMed Google Scholar
Sandri-Goldin, R. M. ICP27 mediates HSV RNA export by shuttling through a leucine-rich nuclear export signal and binding viral intronless RNAs through an RGG motif. Genes Dev.12, 868–879 (1998). CASPubMedPubMed Central Google Scholar
Ghisolfi, L., Kharrat, A., Joseph, G., Amalric, F. & Erard, M. Concerted activities of the RNA recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with pre-ribosomal RNA. Eur. J. Biochem.209, 541–548 (1992). CASPubMed Google Scholar
Fouraux, M. A., Bouvet, P., Verkaart, S., van Venrooij, W. J. & Pruijn, G. J. Nucleolin associates with a subset of the human Ro ribonucleoprotein complexes. J. Mol. Biol.320, 475–488 (2002). CASPubMed Google Scholar
Lapeyre, B. et al. Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease. Mol. Cell Biol.10, 430–434 (1990). CASPubMedPubMed Central Google Scholar
Bagni, C. & Lapeyre, B. Gar1p binds to the small nucleolar RNAs snR10 and snR30 in vitro through a nontypical RNA binding element. J. Biol. Chem.273, 10868–10873 (1998). CASPubMed Google Scholar
Lee, W. C., Xue, Z. X. & Melese, T. The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs. J. Cell Biol.113, 1–12 (1991). CASPubMed Google Scholar
Nichols, R. C. et al. The RGG domain in hnRNP A2 affects subcellular localization. Exp. Cell Res.256, 522–532 (2000). CASPubMed Google Scholar
Maurer-Stroh, S. et al. The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci.28, 69–74 (2003). CASPubMed Google Scholar
Siomi, H., Choi, M., Siomi, M. C., Nussbaum, R. L. & Dreyfuss, G. Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell77, 33–39 (1994). CASPubMed Google Scholar
Feng, Y. et al. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell1, 109–118 (1997). CASPubMed Google Scholar
Brown, V. et al. Purified recombinant Fmrp exhibits selective RNA binding as an intrinsic property of the fragile X mental retardation protein. J. Biol. Chem.273, 15521–15527 (1998). CASPubMed Google Scholar
Laggerbauer, B., Ostareck, D., Keidel, E. M., Ostareck-Lederer, A. & Fischer, U. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet.10, 329–338 (2001). CASPubMed Google Scholar
Li, Z. et al. The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res.29, 2276–2283 (2001). CASPubMedPubMed Central Google Scholar
Hollmann, M. & Heinemann, S. Cloned glutamate receptors. Annu. Rev. Neurosci.17, 31–108 (1994). CASPubMed Google Scholar
Bardoni, B., Schenck, A. & Mandel, J. L. A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum. Mol. Genet.8, 2557–2566 (1999). CASPubMed Google Scholar