Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome (original) (raw)

• Abrahams, B.S. & Geschwind, D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 9, 341–355 (2008).
  Article CAS Google Scholar
• Bassell, G.J. & Warren, S.T. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60, 201–214 (2008).
  Article CAS Google Scholar
• Berry-Kravis, E. Epilepsy in fragile X syndrome. Dev. Med. Child Neurol. 44, 724–728 (2002).
  Article Google Scholar
• Hagerman, R. The physical and behavioral phenotype. in Fragile X Syndrome: Diagnosis, Treatment, and Research (eds. Hagerman, R. & Hagerman, P.) 3–109 (Johns Hopkins Univ. Press, Baltimore, 2002).
• Lüscher, C. & Huber, K.M. Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65, 445–459 (2010).
  Article 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).
  Article CAS Google Scholar
• Dölen, G. et al. Correction of fragile X syndrome in mice. Neuron 56, 955–962 (2007).
  Article Google Scholar
• Dölen, G., Carpenter, R.L., Ocain, T.D. & Bear, M.F. Mechanism-based approaches to treating fragile X. Pharmacol. Ther. 127, 78–93 (2010).
  Article Google Scholar
• Jacquemont, S. et al. Epigenetic modification of the FMR1 gene in fragile X syndrome is associated with differential response to the mGluR5 antagonist AFQ056. Sci. Transl. Med. 3, 64ra61 (2011).
  Article Google Scholar
• Giuffrida, R. et al. A reduced number of metabotropic glutamate subtype 5 receptors are associated with constitutive homer proteins in a mouse model of fragile X syndrome. J. Neurosci. 25, 8908–8916 (2005).
  Article CAS Google Scholar
• Shiraishi-Yamaguchi, Y. & Furuichi, T. The Homer family proteins. Genome Biol. 8, 206 (2007).
  Article Google Scholar
• Park, S. et al. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59, 70–83 (2008).
  Article CAS Google Scholar
• Ango, F. et al. Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer. Nature 411, 962–965 (2001).
  Article CAS Google Scholar
• Tu, J.C. et al. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21, 717–726 (1998).
  Article CAS Google Scholar
• Xiao, B. et al. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707–716 (1998).
  Article CAS Google Scholar
• Mao, L. et al. The scaffold protein Homer1b/c links metabotropic glutamate receptor 5 to extracellular signal-regulated protein kinase cascades in neurons. J. Neurosci. 25, 2741–2752 (2005).
  Article CAS Google Scholar
• Ronesi, J.A. & Huber, K.M. Metabotropic glutamate receptors and fragile X mental retardation protein: partners in translational regulation at the synapse. Sci. Signal. 1, pe6 (2008).
  Article Google Scholar
• Ronesi, J.A. & Huber, K.M. Homer interactions are necessary for metabotropic glutamate receptor-induced long-term depression and translational activation. J. Neurosci. 28, 543–547 (2008).
  Article CAS Google Scholar
• Sharma, A. et al. Dysregulation of mTOR signaling in fragile X syndrome. J. Neurosci. 30, 694–702 (2010).
  Article CAS Google Scholar
• Osterweil, E.K., Krueger, D.D., Reinhold, K. & Bear, M.F. Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome. J. Neurosci. 30, 15616–15627 (2010).
  Article CAS Google Scholar
• Hu, J.H. et al. Homeostatic scaling requires group I mGluR activation mediated by Homer1a. Neuron 68, 1128–1142 (2010).
  Article CAS Google Scholar
• Gross, C. et al. Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome. J. Neurosci. 30, 10624–10638 (2010).
  Article CAS Google Scholar
• Proud, C.G. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 403, 217–234 (2007).
  Article CAS Google Scholar
• Banko, J.L., Hou, L., Poulin, F., Sonenberg, N. & Klann, E. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26, 2167–2173 (2006).
  Article CAS Google Scholar
• Herbert, T.P., Tee, A.R. & Proud, C.G. The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E–BP1 at multiple sites. J. Biol. Chem. 277, 11591–11596 (2002).
  Article CAS Google Scholar
• Kelleher, R.J. III, Govindarajan, A., Jung, H.Y., Kang, H. & Tonegawa, S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467–479 (2004).
  Article CAS Google Scholar
• Waung, M.W., Pfeiffer, B.E., Nosyreva, E.D., Ronesi, J.A. & Huber, K.M. Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59, 84–97 (2008).
  Article CAS 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. Cell 112, 317–327 (2003).
  Article CAS Google Scholar
• Muddashetty, R.S. et al. Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42, 673–688 (2011).
  Article CAS Google Scholar
• Gibson, J.R., Bartley, A.F., Hays, S.A. & Huber, K.M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 100, 2615–2626 (2008).
  Article Google Scholar
• Hays, S.A., Huber, K.M. & Gibson, J.R. Altered neocortical rhythmic activity states in Fmr1 KO mice are due to enhanced mGluR5 signaling and involve changes in excitatory circuitry. J. Neurosci. 31, 14223–14234 (2011).
  Article CAS Google Scholar
• Sanchez-Vives, M.V. & McCormick, D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).
  Article CAS Google Scholar
• Haider, B. & McCormick, D.A. Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62, 171–189 (2009).
  Article CAS Google Scholar
• Liu, Z.H. & Smith, C.B. Dissociation of social and nonsocial anxiety in a mouse model of fragile X syndrome. Neurosci. Lett. 454, 62–66 (2009).
  Article CAS Google Scholar
• Scheetz, A.J., Nairn, A.C. & Constantine-Paton, M. NMDA receptor-mediated control of protein synthesis at developing synapses. Nat. Neurosci. 3, 211–216 (2000).
  Article CAS Google Scholar
• Waung, M.W. & Huber, K.M. Protein translation in synaptic plasticity: mGluR-LTD, Fragile X. Curr. Opin. Neurobiol. 19, 319–326 (2009).
  Article CAS Google Scholar
• Rubenstein, J.L. & Merzenich, M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255–267 (2003).
  Article CAS Google Scholar
• Uhlhaas, P.J. & Singer, W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155–168 (2006).
  Article CAS Google Scholar
• Mackiewicz, M., Paigen, B., Naidoo, N. & Pack, A.I. Analysis of the QTL for sleep homeostasis in mice: Homer1a is a likely candidate. Physiol. Genomics 33, 91–99 (2008).
  Article CAS Google Scholar
• Brown, M.R. et al. Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat. Neurosci. 13, 819–821 (2010).
  Article CAS Google Scholar
• Thomas, A.M. et al. Genetic reduction of group 1 metabotropic glutamate receptors alters select behaviors in a mouse model for fragile X syndrome. Behav. Brain Res. 223, 310–321 (2011).
  Article CAS Google Scholar
• Thomas, A.M., Bui, N., Perkins, J.R., Yuva-Paylor, L.A. & Paylor, R. Group I metabotropic glutamate receptor antagonists alter select behaviors in a mouse model for fragile X syndrome. Psychopharmacology (Berl.) 219, 47–58 (2012).
  Article CAS Google Scholar
• Darnell, J.C. et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247–261 (2011).
  Article CAS Google Scholar
• Mizutani, A., Kuroda, Y., Futatsugi, A., Furuichi, T. & Mikoshiba, K. Phosphorylation of Homer3 by calcium/calmodulin-dependent kinase II regulates a coupling state of its target molecules in Purkinje cells. J. Neurosci. 28, 5369–5382 (2008).
  Article CAS Google Scholar
• Huang, G.N. et al. NFAT binding and regulation of T cell activation by the cytoplasmic scaffolding Homer proteins. Science 319, 476–481 (2008).
  Article CAS Google Scholar
• Orlando, L.R. et al. Phosphorylation of the homer-binding domain of group I metabotropic glutamate receptors by cyclin-dependent kinase 5. J. Neurochem. 110, 557–569 (2009).
  Article CAS Google Scholar
• Bangash, M.A. et al. Enhanced polyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. Cell 145, 758–772 (2011).
  Article CAS Google Scholar
• Billuart, P. et al. Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392, 923–926 (1998).
  Article CAS Google Scholar
• The Dutch-Belgian Fragile X Consortium. Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78, 23–33 (1994).
• Potschka, H. et al. Kindling-induced overexpression of Homer 1A and its functional implications for epileptogenesis. Eur. J. Neurosci. 16, 2157–2165 (2002).
  Article CAS Google Scholar