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Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation
Open accessAbstract
Local translation of proteins in distal dendrites is thought to support synaptic structural plasticity. We have previously shown that metabotropic glutamate receptor (mGluR1) stimulation initiates a phosphorylation cascade, triggering rapid association of some mRNAs with translation machinery near synapses, and leading to protein synthesis. To determine the identity of these mRNAs, a cDNA library produced from distal nerve processes was used to screen synaptic polyribosome-associated mRNA. We identified mRNA for the fragile X mental retardation protein (FMRP) in these processes by use of synaptic subcellular fractions, termed synaptoneurosomes. We found that this mRNA associates with translational complexes in synaptoneurosomes within 1-2 min after mGluR1 stimulation of this preparation, and we observed increased expression of FMRP after mGluR1 stimulation. In addition, we found that FMRP is associated with polyribosomal complexes in these fractions. In vivo, we observed FMRP immunoreactivity in spines, dendrites, and somata of the developing rat brain, but not in nuclei or axons. We suggest that rapid production of FMRP near synapses in response to activation may be important for normal maturation of synaptic connections.
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“In fact, in both assays there was more FMRP immunoprecipitated from the DHPG-treated WT SNs, which is in agreement with previous reports that DHPG stimulates the dendritic translation of FMRP [22,39].”
From FMRP Mediates mGluR5-Dependent Translation of Amyloid Precursor Protein (2007) · cites this paper as [39]
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“The mRNA for FMRP is found in dendrites, and the synthesis of FMRP protein in dendrites can be modulated by pharmacological agent”
BackgroundSelf-citationMolecular Insights into mRNA Transport and Local Translation in the Mammalian Nervous System
Kiebler, M. A., & DesGroseillers, L. (2000) · Neuron · doi:10.1016/s0896-6273(00)80868-5 · Cited by 202
Lessons from Fragile X Regarding Neurobiology, Autism, and Neurodegeneration
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“With stimulation of the metabotropic glutamate system, FMRP organizes the translation of messages important for synaptic structural changes or synaptic plasticity.(22,26,27) The FMR1 mutation no only affects the gene product, FMRP, but many other genes.”
MethodVanderklish, P. W., & Edelman, G. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.032681099 · Cited by 200
Costa, E., Davis, J. M., Grayson, D. R., Guidotti, A., Pappas, G. D., & Pesold, C. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0436 · Cited by 197
Meredith, R. M., Holmgren, C. D., Weidum, M., Burnashev, N., & Mansvelder, H. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.028 · Cited by 190
The Drosophila Fragile X Gene Negatively Regulates Neuronal Elaboration and Synaptic Differentiation
Pan, L., Zhang, Y., Woodruff, E. A., & Broadie, K. S. (2004) · Current Biology · doi:10.1016/j.cub.2004.09.085 · Cited by 197
Spatially restricting gene expression by local translation at synapses
Wang, D. O., Martin, K. C., & Zukin, R. S. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.005 · Cited by 196
“FMRP mRNA is translated near synapses in response to neurotransmitter activation [78]; moreover, different models of experience-dependent plasticity such as whisker stimulation [79,80], visual experience [81], and exposure to enriched environment [82] also promote FMRP translation.”
Local translational control in dendrites and its role in long‐term synaptic plasticity
Sutton, M. A., & Schuman, E. M. (2005) · Journal of Neurobiology · doi:10.1002/neu.20152 · Cited by 195
“Another target of mGluR-activated translation, interestingly, is FMRP. DHPG-treated synaptoneurosomes demonstrate increased FMR1 mRNA associated with polysomes and increased levels of FMRP protein assayed by Western blotting (Weiler et al., 1997).”
BackgroundChuang, S.-C., Zhao, W., Bauchwitz, R., Yan, Q., Bianchi, R., & Wong, R. K. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1777-05.2005 · Cited by 190
“FMRP may be coupled to group I mGluR activities (Weiler et al., 1997) and may mediate synaptic plasticity via its action on mRNA translation.”
BackgroundRole of HuD and other RNA‐binding proteins in neural development and plasticity
Perrone‐Bizzozero, N. I., & Bolognani, F. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10175 · Cited by 186
“FMRP is mainly cytoplasmic associated with polyribosomes, but it is also present in the nucleus, in the nuclear pore, and in dendrites, suggesting a role in mRNA translation and transport (Feng et al., 1997; Weiler et al., 1997).”
BackgroundArendt, T. (2003) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2003.09.007 · Cited by 189
The role of Rho GTPases in disease development
Boettner, B., & Van Aelst, L. (2002) · Gene · doi:10.1016/s0378-1119(02)00426-2 · Cited by 229
Pfeiffer, B. E., & Huber, K. M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0054-07.2007 · Cited by 189
“Although transfected FMRP levels are greater than endogenous FMRP levels in unstimulated WT neurons, these levels are within the physiological range of FMRP induced by experience or neuronal activity (Weiler et al., 1997; Todd and Mack, 2000; Hou et al., 2006).”
BackgroundReduced FMR1 mRNA translation efficiency in Fragile X patients with premutations
Primerano, B., Tassone, F., Hagerman, R. J., Hagerman, P. J., Amaldi, F., & Bagni, C. (2002) · RNA · doi:10.1017/s1355838202020642 · Cited by 182
Blanpied, T. A., & Ehlers, M. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.006 · Cited by 187
Khandjian, E. W., Huot, M.-E., Tremblay, S., Davidovic, L., Mazroui, R., & Bardoni, B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405398101 · Cited by 178
Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions
Sigrist, S. J., Thiel, P. R., Reiff, D. F., Lachance, P. E. D., Lasko, P. F., & Schuster, C. (2000) · Nature · doi:10.1038/35016598 · Cited by 179
“These findings are consistent with the hypothesis that synaptic activity can control synaptic translatio”
ResultDendritic spine dysgenesis in autism related disorders
Phillips, M. L., & Pozzo‐Miller, L. D. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.011 · Cited by 188
Local Protein Synthesis and Spine Morphogenesis: Fragile X Syndrome and Beyond
Grossman, A. W., Aldridge, G. M., Weiler, I. J., & Greenough, W. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1790-06.2006 · Cited by 177
“In addition to being synthesized at synapses, FMRP binds mRNA and ribosomes and seems to regulate mRNA transport and synaptic protein synthesis (Weiler et al., 1997; Khandjian et al., 2004).”
BackgroundRodríguez, M. Á., Pesold, C., Liu, W. S., Kriho, V., Guidotti, A., Pappas, G. D., & Costa, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050589797 · Cited by 178
ADHD symptoms in children with FXS
Sullivan, K., Hatton, D., Hammer, J., Sideris, J., Hooper, S., Ornstein, P., & Bailey, D. (2006) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.31388 · Cited by 174
“Perhaps because FMRP has been found to be involved in synaptic functioning [Weiler et al., 1997], as well as theorized to alter structures in the brain [Reiss et al., 1995; Eliez et al., 2001; Hessl et al., 2004], FXS probably affects cognitive function, including attention, in an ongoing dynamic…”
BackgroundProtein translation in synaptic plasticity: mGluR-LTD, Fragile X
Waung, M. W., & Huber, K. M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.03.011 · Cited by 174
“FMRP associates with dendritic mRNAs and RNA granules, as well as translating polyribosomes, while Fmr1 mRNA is itself present in dendrites and translated in response to mGluR activation [10] (reviewed in [9]).”
BackgroundLing, S., Fahrner, P. S., Greenough, W. T., & Gelfand, V. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408114101 · Cited by 169
Current advances in local protein synthesis and synaptic plasticity
Pfeiffer, B. E., & Huber, K. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1797-06.2006 · Cited by 168
“Interestingly, the mRNA for FMRP is present in dendrites, and FMRP is synthesized in response to mGluR activation (Weiler et al., 1997; Antar et al., 2004).”
Emerging role of microRNAs in major depressive disorder: diagnosis and therapeutic implications
Dwivedi, Y. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.1/ydwivedi · Cited by 169
Gantois, I., Vandesompele, J., Speleman, F., Reyniers, E., D’Hooge, R., Severijnen, L.-A. W. F. M., Willemsen, R., Tassone, F., & Kooy, R. F. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.07.017 · Cited by 166
Dendritic mRNAs encode diversified functionalities in hippocampal pyramidal neurons
Zhong, J. W., Zhang, T., & Bloch, L. M. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-17 · Cited by 162
“Local translation of dendritic mRNAs is modulated by synaptic activities [2-8].”
Functional and Selective RNA Interference in Developing Axons and Growth Cones
Hengst, U., Cox, L. J., Macosko, E. Z., & Jaffrey, S. R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5229-05.2006 · Cited by 170
“FMRP has previously been found in dendrites (Weiler et al., 1997), but its localization in developing axons has not been addressed.”
BackgroundVolk, L. J., Pfeiffer, B. E., Gibson, J. R., & Huber, K. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2266-07.2007 · Cited by 166
“6) (Weiler et al., 1997, 2004; Huber et al., 2002; Koekkoek et al., 2005; Hou et al., 2006).”
BackgroundOostra, B. A., & Willemsen, R. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.02.007 · Cited by 163
“Weiler et al showed that FMRP is synthesized in response to mGluR activation using glutamate [15].”
BackgroundMethodFmr1 knockout mouse has a distinctive strain-specific learning impairment
Dobkin, C., Rabe, A., Dumas, R., El Idrissi, A., Haubenstock, H., & Ted Brown, W. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00292-x · Cited by 179
Berry-Kravis, E., Krause, S. E., Block, S. S., Guter, S., Wuu, J., Leurgans, S., Decle, P., Potanos, K., Cook, E., Salt, J., et al. (2006) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2006.16.525 · Cited by 155
“14 years has demonstrated dendritic ribosomes (Jin and Warren 2003; Willem-son et al. 2004) and that FMRP expression increases after type I metabotropic glutamate receptor (mGluR1) activation (Weiler identified and named Fragile X Mental Retarda-tion-1 ( FMR1 ; Verkerk et al. 1991).”
Schütt, J., Falley, K., Richter, D., Kreienkamp, H., & Kindler, S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.042663 · Cited by 158
Fragile X targeted pharmacotherapy: lessons learned and future directions
Erickson, C. A., Davenport, M. H., Schaefer, T. L., Wink, L. K., Pedapati, E. V., Sweeney, J. A., Fitzpatrick, S. E., Brown, W. T., Budimirovic, D. B., Hagerman, R. J., et al. (2017) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-017-9186-9 · Cited by 157
“of mGluRs [16], FMRP deficit leads to increased downstream effects of mGluR signaling [26, 54], and many of these downstream effects are dependent on mRNA translation at the synapse [55–58].”
BackgroundShin, C. Y., Kundel, M., & Wells, D. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2457-04.2004 · Cited by 151
FMRP Involvement in Formation of Synapses among Cultured Hippocampal Neurons
Braun, K. A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1045 · Cited by 149
“FMRP is synthesized at the synapse, in a synaptoneurosome preparation (Weiler et al., 1997), in response to glutamate, KCl and class I metabotropic glutamate receptor agonists.”
BackgroundTransport of Fragile X Mental Retardation Protein via Granules in Neurites of PC12 Cells
de Diego‐Otero, Y., Severijnen, L.-A. W. F. M., van Cappellen, G. W. A., Schrier, M., Oostra, B. A., & Willemsen, R. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.23.8332-8341.2002 · Cited by 149
“In synaptoneurosome preparations from rat cortex, both Fmr1 mRNA and Fmrp could be detected, and after mGluR1 stimulation a moderate increase of Fmrp expression within translational complexes was observed (42).”
BackgroundPresence and phosphorylation of transcription factors in developing dendrites
Crino, P. B., Khodakhah, K., Becker, K. G., Ginsberg, S. D., Hemby, S. E., & Eberwine, J. H. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.5.2313 · Cited by 149
Aschrafi, A., Cunningham, B. A., Edelman, G. M., & Vanderklish, P. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409803102 · Cited by 148
Local translation of classes of mRNAs that are targeted to neuronal dendrites
Eberwine, J. H., Miyashiro, K., Kacharmina, J. E., & Job, C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.121146698 · Cited by 148
Min, W. W., Yuskaitis, C. J., Yan, Q., Sikorski, C., Chen, S., Jope, R. S., & Bauchwitz, R. P. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.09.017 · Cited by 146
“* p < 0.05; *** p < 0.001 compared with mice not given a GSK3 inhibitor, inwhich 100% of mice displayed AGS. protein translation in neurons (Bear et al., 2007; Grossman et al., 2006; Miyashiro et al., 2003; Weiler et al., 1997).”
BackgroundInfluentialTranscription, translation and fragile X syndrome
Garber, K. B., Smith, K. T., Reines, D., & Warren, S. T. (2006) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2006.04.010 · Cited by 148
“Treatment of primary neurons with KCl rapidly induces localization of both FMR1 mRNA and FMRP to dendrites [38].”
BackgroundKao, D.-I., Aldridge, G. M., Weiler, I. J., & Greenough, W. T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010564107 · Cited by 143
“Activity-dependent local translation is a fundamental mechanism underlying synaptic plasticity (5, 6).”
BackgroundTessier, C. R., & Broadie, K. S. (2008) · Development · doi:10.1242/dev.015867 · Cited by 147
“Neural activity from sensory experience and metabotropic glutamate receptor signaling increases FMRP expression and function (Gabel et al., 2004; Hou et al., 2006; Irwin et al., 2005; Irwin et al., 2000; Restivo et al., 2005; Todd and Mack, 2000; Todd et al., 2003; Valentine et al., 2000; Weiler et al., 1997).”
BackgroundInfluentialMichel, C. I., Kraft, R., & Restifo, L. L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1102-04.2004 · Cited by 145
“Moreover, FMRP expression is neuronal activity-dependent in several systems (Weiler et al., 1997; Irwin et al., 2000; Todd and Mack, 2000).”
BackgroundKwon, H., Menon, V., D, S. E. M., Warsofsky, I. S., White, C. D., Dyer-Friedman, J., Taylor, A. K., Glover, G. H., & Reiss, A. L. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.7.1040 · Cited by 144
“These studies point to the function of FMRP as an RNA-binding protein, possibly involved in the transport and/or stabilization of RNA from the nucleus to the dendrites (53, 54).”
BackgroundEarly developmental alterations in GABAergic protein expression in fragile X knockout mice
Adusei, D. C., Pacey, L. K. K., Chen, D., & Hampson, D. R. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.05.002 · Cited by 139
“12 The activation of group I mGluRs triggers the rapid translation of certain mRNAs at synapses, including FMRP (Weiler and Greenough, 1993; Weiler et al., 1997).”
Buckley, P. T., Lee, M. T., Sul, J., Miyashiro, K., Bell, T. J., Fisher, S. A., Kim, J., & Eberwine, J. H. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.028 · Cited by 143
“Further, we observed that FMRP localization is directly affected by the disruption of endogenous ID element-mediated FMR1i1 targeting, suggesting that CIRTs may be critically important in the presumptive role of FMRP in modulation of local dendritic protein synthesis (Huber et al., 2002; Weiler et al., 1997).”
Emerging role of CaMKII in neuropsychiatric disease
Robison, A. J. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.07.001 · Cited by 150
Barnea‐Goraly, N., D, S. E. M., Hedeus, M., Menon, V., White, C. D., Moseley, M. E., & Reiss, A. L. (2003) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.10035 · Cited by 140
mRNPs, polysomes or granules: FMRP in neuronal protein synthesis
Zalfa, F., Achsel, T., & Bagni, C. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.05.010 · Cited by 138
“The finding that mGluR (metabotropic glutamate receptor) activation actually increases FMRP levels [61] implies that FMRP itself is involved in”
BackgroundGiuffrida, R., Musumeci, S., D'Antoni, S., Bonaccorso, C. M., Giuffrida-Stella, A. M., Oostra, B. A., & Catania, M. V. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0932-05.2005 · Cited by 141
Glutamatergic synapses in neurodevelopmental disorders
Moretto, E., Murru, L., Martano, G., Sassone, J., & Passafaro, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.09.014 · Cited by 146
“This form of plasticity was shown to induce the translation of FMRP in synaptoneurosomes (Weiler et al., 1997).”
BackgroundLarson, J., Jessen, R. E., Kim, D., Fine, A.-K. S., & du Hoffmann, J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2638-05.2005 · Cited by 135
“Activation of metabotropic glutamate receptors (mGluRs) in cellular fractions enriched in dendritic spines triggers protein synthetic activity most likely via translation of dendritic resident mRNA associated with polyribosomes (Weiler et al., 1997).”
BackgroundOf mice and the fragile X syndrome
Kooy, R. F. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00017-9 · Cited by 138
Davidovic, L., Jaglin, X. H., Lepagnol-Bestel, A.-M., Tremblay, S., Simonneau, M., Bardoni, B., & Khandjian, E. W. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm263 · Cited by 134
Tucker, B., Richards, R. I., & Lardelli, M. T. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl422 · Cited by 133
“This receptor alters FMRP levels at the synapse and is associated with a protein-synthesis-dependent lengthening of dendritic spines (16,17).”
Backgroundde Diego-Otero, Y., Romero-Zerbo, Y., Bekay, R. E., Decara, J., Sanchez, L., Fonseca, F. R.-D., & Arco-Herrera, I. D. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.152 · Cited by 133
Nalavadi, V. C., Muddashetty, R. S., Gross, C., & Bassell, G. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5057-11.2012 · Cited by 128
“, 2004) and FMRP synthesis at synapses (Weiler et al., 1997).”
BackgroundMolecular and cognitive predictors of the continuum of autistic behaviours in fragile X
Loesch, D. Z., Bui, M., Dissanayake, C., Clifford, S. M., Gould, E. L., Bulhak‐Paterson, D., Tassone, F., Taylor, A. K., Hessl, D. R., Hagerman, R. J., et al. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.09.007 · Cited by 136
“FMRP is involved in synaptogenesis, especially in the cerebral cortex, cerebellum, and hippocampus, and more specifically, in synaptic pruning (Comery et al., 1997; Weiler et al., 1997; Weiler & Greenough, 1999).”
BackgroundCosta, L., Spatuzza, M., D’Antoni, S., Bonaccorso, C. M., Trovato, C., Musumeci, S. A., Leopoldo, M., Lacivita, E., Catania, M. V., & Ciranna, L. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.008 · Cited by 134
Bardoni, B., & Mandel, J. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00300-3 · Cited by 129
Hicks, S. D., Ignacio, C., Gentile, K. L., & Middleton, F. A. (2016) · BMC Pediatrics · doi:10.1186/s12887-016-0586-x · Cited by 128
“Levels of miR-23a also fluctuate in response to CNS injuries such as cerebral ischemia [23] or temporal epilepsy [24], both of which can be associated with ASD [18].”
BackgroundA fragile balance: FMR1 expression levels
Oostra, B. A., & Willemsen, R. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg298 · Cited by 130
“The synthesis of FMRP in the synaptoneurosomes increases after stimulation with the neurotransmitter glutamate, suggesting that synthesis of this protein in synaptoneurosomes is triggered by a class I glutamate receptor (73).”
BackgroundAltered Hippocampal Synaptic Plasticity in the Fmr1 Gene Family Knockout Mouse Models
Zhang, J., Hou, L., Klann, E., & Nelson, D. L. (2009) · Journal of Neurophysiology · doi:10.1152/jn.90558.2008 · Cited by 126
Fragile X syndrome: from molecular genetics to therapy
D’Hulst, C., & Kooy, R. F. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2008.064667 · Cited by 128
“KO mice. Rather than a deficit, however, they found that mGluR-LTD was augmented in the absence of FMRP. This finding is consistent with the discovery that FMRP normally functions as a negative regulator of translation. Based on the evidence that FMRP is normally synthesised following stimulation of Gp1 mGluRs,”
ResultMechanism-based approaches to treating fragile X
Dölen, G., Carpenter, R. L., Ocain, T. D., & Bear, M. F. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.02.008 · Cited by 129
“Furthermore, recall that synaptic mGluR5 activation induces protein synthesis (Weiler & Greenough, 1993; Weiler et al., 1997; Job & Eberwine, 2001; Todd et al., 2003; Davidkova & Carroll, 2007; Mameli et al., 2007; Muddashetty et al., 2007;Westmark &Malter, 2007; Park et al., 2008; Waung et al.,…”
BackgroundIdentification of sites for exponential translation in living dendrites
Job, C., & Eberwine, J. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.231485698 · Cited by 135
AFQ056, a new mGluR5 antagonist for treatment of fragile X syndrome
Levenga, J., Hayashi, S., de Vrij, F. M. S., Koekkoek, S. K. E., van der Linde, H. C., Nieuwenhuizen, I. M., Song, C., Buijsen, R. A. M., Pop, A. S., Gomez‐Mancilla, B., et al. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.01.022 · Cited by 122
“Moreover, at the synapse FMRP has shown to be important for translational regulation of target mRNAs in synaptosomes after mGluR5 stimulation (Greenough et al., 2001; Muddashetty et al., 2007; Weiler et al., 1997, 2004).”
BackgroundFerrari, F., Mercaldo, V., Piccoli, G., Sala, C., Cannata, S. M., Achsel, T., & Bagni, C. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.11.015 · Cited by 125
“, 1993) and demonstrated a dendritic localization of FMRP in mouse brain sections (Feng et al., 1997; Weiler et al., 1997) and in primary hippocampal neurons (Ohashi et al.”
BackgroundOf Men and Mice: Modeling the Fragile X Syndrome
Dahlhaus, R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00041 · Cited by 133
“Here, FMRP is primarily located in the cytosol and the nucleus (Feng et al., 1997), but it has also been found along dendrites, axons and at synaptic sites (Weiler et al., 1997; Greenough et al., 2001; Antar et al., 2006; Akins et al., 2017).”
BackgroundLoesch, D. Z., Bui, M., Grigsby, J., Butler, E., Epstein, J., Huggins, R., Taylor, A. K., & Hagerman, R. J. (2003) · Neuropsychology · doi:10.1037/0894-4105.17.4.646 · Cited by 119
Absence of metabotropic glutamate receptor-mediated plasticity in the neocortex of fragile X mice
Wilson, B. M., & Cox, C. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610875104 · Cited by 121
Quantification and real-time tracking of RNA in live cells using Sticky-flares
Briley, W. E., Bondy, M. H., Randeria, P. S., Dupper, T. J., & Mirkin, C. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1510581112 · Cited by 121
“For instance, synaptic potentiation, the basis of learning and memory, relies on the local translation of specific mRNAs in pre- and postsynaptic compartments (2).”
BackgroundBC1 Regulation of Metabotropic Glutamate Receptor-Mediated Neuronal Excitability
Zhong, J. W., Chuang, S.-C., Bianchi, R., Zhao, W., Lee, H., Fenton, A. A., Wong, R. K. S., & Tiedge, H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3893-08.2009 · Cited by 120
“We focused on PSD-95 and FMRP because synthesis of these synaptic proteins has been shown previously to be stimulated by group I mGluR activation (Weiler et al., 1997; Todd et al., 2003).”
BackgroundAbnormal mGlu 5 Receptor/Endocannabinoid Coupling in Mice Lacking FMRP and BC1 RNA
Maccarrone, M., Rossi, S., Bari, M., Chiara, V. D., Rapino, C., Musella, A., Bernardi, G., Bagni, C., & Centonze, D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.19 · Cited by 120
“Accordingly, stimulation of mGluRs by DHPG has been shown to induce FMRP translation (Weiler et al, 1997) and translocation at dendritic spines (Ferrari et al, 2007), raising the possibility that FMRP mediates some of the synaptic effects of mGluR activation.”
BackgroundTheDrosophilaFragile X Mental Retardation Gene Regulates Sleep Need
Bushey, D., Tononi, G., & Cirelli, C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4830-08.2009 · Cited by 120
“, 2005) and glutamatergic stimulation (Weiler et al., 1997), this is the first indication that dFmr1 expression in adult Drosophila increases with prolonged activity, and is consistent with the fact that sensory deprivation decreases dFmr1 mRNA and protein levels (Tessier and Broadie, 2008).”
BackgroundSantini, E., Huynh, T. N., & Klann, E. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00005-2 · Cited by 120
Galvez, R., Gopal, A. R., & Greenough, W. T. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02363-1 · Cited by 118
Wang, H. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddh009 · Cited by 117
“In the adult brain, FMRP is detected in the somatodendritic compartments of neurons including dendritic spines, with negligible expression in glia (10,13,21).”
BackgroundFisch, G. S., Simensen, R. J., & Schroer, R. J. (2002) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1014888505185 · Cited by 115
“, 1997) found dendritic abnormalities in brain that may be implicated in neurotransmitter activation (Weiler et al., 1997).”
BackgroundNovel isoforms of the fragile X related protein FXR1P are expressed during myogenesis
Khandjian, E. W. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.13.2121 · Cited by 114
Regulation and function of local protein synthesis in neuronal dendrites
Jiang, C., & Schuman, E. M. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02190-4 · Cited by 113
“For example, activation of group I mGluRs in synaptosomes leads to the synthesis of fragile X mental retardation protein (FMRP) [ 53 ], a RNA-binding protein that regulates translation in both cell body and dendrites [54,55].”
MethodSynaptic Plasticity and Translation InitiationPreprint
Klann, E., Antion, M. D., Banko, J. L., & Hou, L. (2004) · Learning & Memory · doi:10.1101/lm.79004 · Cited by 112
“2002), and stimulation of group I mGluRs was shown to increase the synthesis of the fragile X mental retardation protein (Weiler et al. 1997).”
BackgroundInfluentialHelmeke, C. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.8.717 · Cited by 106
“, 1999), and some psychopathological syndromes in humans are associated with increased spine and decreased shaft synapses in prefrontal cortical regions (Aganova and Uranova, 1990; Comery et al., 1997; Weiler et al., 1997).”
BackgroundFragile X-associated disorders: a clinical overview
Gallagher, A. T., & Hallahan, B. P. (2011) · Journal of Neurology · doi:10.1007/s00415-011-6161-3 · Cited by 116
“Other amino acids, including glutamate (Glu) and Nacetyl aspartate (NAA) have also been implicated in the aetiology of FraX [109–112], with recent animal research particularly focusing on metabotrophic glutamate receptors (mGluR).”
BackgroundMolecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment
Wells, D. G., Richter, J. D., & Fallon, J. R. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00050-1 · Cited by 108
The fragile X syndrome: From molecular genetics to neurobiology
Willemsen, R., Oostra, B. A., Bassell, G. J., & Dictenberg, J. B. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20010 · Cited by 106
Aberrant early-phase ERK inactivation impedes neuronal function in fragile X syndrome
Kim, S. H., Markham, J. A., Weiler, I. J., & Greenough, W. T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800257105 · Cited by 97
“In normal mice, FMRP is translated near synapses in response to group I mGluR activation (7, 28).”
BackgroundMetabotropic glutamate receptor 5 as drug target for Fragile X syndrome
Scharf, S. H., Jaeschke, G., Wettstein, J. G., & Lindemann, L. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2014.11.004 · Cited by 106
Therapeutic Strategies in Fragile X Syndrome: Dysregulated mGluR Signaling and Beyond
Groß, C., Berry‐Kravis, E., & Bassell, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.137 · Cited by 109
“…only a multifaceted regulator of numerous target mRNAs, but is also itself activity-regulated at multiple steps, such as FMRP synthesis at synapses (Weiler et al, 1997), protein and mRNA localization in dendrites and at synapses (Antar et al, 2004), and posttranslational modifications and protein…”
BackgroundFragile X Syndrome and Targeted Treatment Trials
Hagerman, R. J., Lauterborn, J. C., Au, J., & Berry‐Kravis, E. (2011) · Results and problems in cell differentiation · doi:10.1007/978-3-642-21649-7_17 · Cited by 111
“…Synthesis: FMRP binds to mRNAs (including its own) and regulates their translation within dendrites and spines in response to neural activation (Weiler et al. 1997, 2004) and, in particular, occurs in response to activation by either group I mGluR, (Huber et al. 2002; Antar et al. 2004;…”
Cell-Type-Specific Translation Profiling Reveals a Novel Strategy for Treating Fragile X Syndrome
Thomson, S. R., Seo, S. S., Barnes, S. A., Louros, S. R., Muscas, M., Dando, O., Kirby, C., Wyllie, D. J. A., Hardingham, G. E., Kind, P. C., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.013 · Cited by 100
“Publi This is an open access article under the CC BY license (http://creative FMRP is synthesized at synapses by activation of group I metabotropic glutamate receptors (mGlu1/5), where it acts as a negative regulator of the mRNA translation supporting long-term synaptic depression (LTD) (Bear et al., 2004; Weiler et a…”
BackgroundTargeted treatments for fragile X syndrome
Berry‐Kravis, E., Knox, A. T., & Hervey, C. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9074-7 · Cited by 108
“1997) or non-translating ribonucleoprotein (RNP) particles known as processing bodies (PB; Ceman et al. 1999; Zalfa et al. 2003; Blackwell et al. 2010; Weiler et al. 1997).”
BackgroundGabel, L. A., Won, S., Kawai, H. D., McKinney, M., Tartakoff, A. M., & Fallon, J. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2185-04.2004 · Cited by 103
“Activation of metabotropic glutamate receptors (mGluR) in isolated synaptoneurosomes has been reported to increase both Fmr1 mRNA association with polyribosomes and FMRP expression (Weiler et al., 1997).”
BackgroundPastori, C., Peschansky, V. J., Barbouth, D., Mehta, A., Silva, J., & Wahlestedt, C. (2013) · Human Genetics · doi:10.1007/s00439-013-1356-6 · Cited by 102
“The protein encoded by FMR1, FMRP, is an RNA-binding protein involved in translational repression, synaptic maturation, dendritic mRNA localization and nucleoplasmic shuttling of mRNA (Antar et al. 2005; Brown et al. 1998; Weiler et al. 1997) lending support to the idea that its aberrant expression contributes to the…”
Background
Metadata
- Authors
- Weiler, I. J., Irwin, S. A., Klintsova, A. Y., Spencer, C. M., Brazelton, A. D., Miyashiro, K., Comery, T. A., Patel, B., Eberwine, J., & Greenough, W. T.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1997-05-13
- Volume
- 94
- Issue
- 10
- Pages
- 5395-5400
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC24689
- OpenAlex
- W2002760096
- Cited by
- 644
- References
- 58
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 8 · 2023: 11 · 2022: 11 · 2021: 12 · 2020: 8 · 2019: 14 · 2018: 13 · 2017: 19 · 2016: 15 · 2015: 23 · 2014: 24 · 2013: 27 · 2012: 29
- FWCI
- 12.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- FRAXA Research Foundation (MH35321)
- John D. and Catherine T. MacArthur Foundation
- National Institutes of Health
- U.S. Public Health Service
- National Institute on Aging (AG10154, R01AG010154)
- National Institute of Mental Health (MH-35321, R01MH035321, R37MH035321)
- National Center for Research Resources (RR 04050, P41RR004050)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- FMRP, local protein synthesis, metabotropic glutamate receptor 1, polysomes, synaptoneurosomes, dendritic mRNA, synapse maturation, synaptic plasticity, dendritic translation
- MeSH terms
- Amino Acid Sequence, Animals, Antibodies, Brain, Dendrites, Glycine, Humans, Kinetics, Molecular Sequence Data, Nerve Tissue Proteins, Neurons, Organ Specificity, Polyribosomes, Resorcinols, RNA, Messenger, Synapses, Protein Biosynthesis, Oligonucleotide Probes, Gene Library, Antisense Elements (Genetics), RNA-Binding Proteins, Sequence Homology, Amino Acid, DNA, Complementary, Receptors, Metabotropic Glutamate, Neurotransmitter Agents, Excitatory Amino Acid Antagonists, Rats, Fragile X Mental Retardation Protein, Fragile X Messenger Ribonucleoprotein 1
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