The mGluR theory of fragile X mental retardation

Trends in Neurosciences

Volumn 27, Issue 7, 2004, Pages 370-377

  Bear, Mark F ^a   Huber, Kimberly M ^b   Warren, Stephen T ^c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 6 PHENYLETHYNYLPYRIDINE; CALMODULIN; FRAGILE X MENTAL RETARDATION PROTEIN; GLUTAMATE RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; PYRIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANXIETY; ATAXIA; AUTISM; CIRCADIAN RHYTHM; COGNITIVE DEFECT; EPILEPSY; FRAGILE X SYNDROME; GENE MUTATION; HYPERALGESIA; INNERVATION; INTESTINE MOTILITY; KNOCKOUT MOUSE; LEARNING DISORDER; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY DISORDER; MENTAL DEFICIENCY; MOTOR COORDINATION; NERVE CELL PLASTICITY; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; PATHOPHYSIOLOGY; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PURKINJE CELL; REVIEW; RNA BINDING; RNA INTERFERENCE; RNA TRANSLATION; SYNAPSE; TRANSLATION REGULATION; VALIDATION PROCESS;

EID: 3042647610     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2004.04.009     Document Type: Article

References (95)

1. O'Donnell W.T., Warren S.T. A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 25:2002;315-338
2. Hagerman R.J. The physical and behavioral phenotype. Hagerman R.J., Hagerman P. Fragile X Syndrome: Diagnosis, Treatment, and Research. 2002;3-109 The Johns Hopkins University Press
3. Bakker C.E., Oostra B.A. Understanding fragile X syndrome: insights from animal models. Cytogenet. Genome Res. 100:2003;111-123
4. Rudelli R.D., et al. Adult fragile X syndrome. Clinico-neuropathologic findings. Acta Neuropathol. (Berl.). 67:1985;289-295
5. Hinton V.J., et al. Analysis of neocortex in three males with the fragile X syndrome. Am. J. Med. Genet. 41:1991;289-294
6. 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. 98:2001;161-167
7. Purpura D.P. Dendritic spine 'dysgenesis' and mental retardation. Science. 186:1974;1126-1128
8. Kaufmann W.E., Moser H.W. Dendritic anomalies in disorders associated with mental retardation. Cereb. Cortex. 10:2000;981-991
9. Bakker C.E., et al. Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian fragile X consortium. Cell. 78:1994;23-33
10. Kooy R.F. Of mice and the fragile X syndrome. Trends Genet. 19:2003;148-154
11. Nimchinsky E.A., et al. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21:2001;5139-5146
12. Irwin S.A., et al. Dendritic spine and dendritic field characteristics of layer V pyramidal neurons in the visual cortex of fragile-X knockout mice. Am. J. Med. Genet. 111:2002;140-146
13. Huber K.M., et al. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. U. S. A. 99:2002;7746-7750
14. Bear M.F. The role of LTD and LTP in development and learning. Carew T.J., et al. Mechanistic Relationships between Development and Learning. 1998;205-225 Wiley
15. Ito M., et al. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. 324:1982;113-134
16. Ito M. Long term depression. Cowan M.W., et al. Annual Review of Neuroscience. Vol. 12:1989;85-102 Annual Reviews
17. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. U. S. A. 89:1992;4363-4367
18. Aiba A., et al. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell. 79:1994;377-388
19. Shigemoto R., et al. Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron. 12:1994;1245-1255
20. Oliet S.H., et al. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron. 18:1997;969-982
21. Lee H.K., et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 112:2003;631-643
22. Kemp N., Bashir Z.I. Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors. Neuropharmacology. 38:1999;495-504
23. Carroll R.C., et al. Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat. Neurosci. 2:1999;454-460
24. Snyder E.M., et al. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci. 4:2001;1079-1085
25. Huber K.M., et al. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science. 288:2000;1254-1257
26. Manahan-Vaughan D., et al. Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J. Neurosci. 20:2000;8572-8576
27. Sajikumar S., Frey J.U. Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro. Neurosci. Lett. 338:2003;147-150
28. Huber K.M., et al. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 86:2001;321-325
29. Kleppisch T., et al. G(alpha)q-deficient mice lack metabotropic glutamate receptor-dependent long-term depression but show normal long-term potentiation in the hippocampal CA1 region. J. Neurosci. 21:2001;4943-4948
30. Huber, K.M., et al. (2001) Evidence for a novel signal transduction pathway in hippocampal mGluR-dependent LTD. Program number 388.7. In Abstract Viewer/Itinerary Planner, Society for Neuroscience Online.
31. Antar L.N., et al. Metabotropic glutamate receptor activation regulates fragile X mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 24:2004;2648-2655
32. Weiler I.J., et al. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl. Acad. Sci. U. S. A. 94:1997;5395-5400
33. Godfraind J.M., et al. Long-term potentiation in the hippocampus of fragile X knockout mice. Am. J. Med. Genet. 64:1996;246-251
34. Paradee W., et al. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience. 94:1999;185-192
35. Chiurazzi P., et al. Understanding the biological underpinnings of fragile X syndrome. Curr. Opin. Pediatr. 15:2003;559-566
36. Jin P., Warren S.T. New insights into fragile X syndrome: from molecules to neurobehaviors. Trends Biochem. Sci. 28:2003;152-158
37. Antar L.N., Bassell G.J. Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface. Neuron. 37:2003;555-558
38. Feng Y., et al. Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17:1997;1539-1547
39. Feng Y., et al. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell. 1:1997;109-118
40. Brown V., et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell. 107:2001;477-487
41. Darnell J.C., et al. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell. 107:2001;489-499
42. Miyashiro K.Y., et al. RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron. 37:2003;417-431
43. Chen L., et al. The fragile X mental retardation protein binds and regulates a novel class of mRNAs containing U rich target sequences. Neuroscience. 120:2003;1005-1017
44. Zalfa F., et al. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell. 112:2003;317-327
45. Wang H., et al. Dendritic BC1 RNA: functional role in regulation of translation initiation. J. Neurosci. 22:2002;10232-10241
46. Jin P., et al. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat. Neurosci. 7:2004;113-117
47. Caudy A.A., et al. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16:2002;2491-2496
48. Ishizuka A., et al. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16:2002;2497-2508
49. Zhang Y.Q., et al. Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell. 107:2001;591-603
50. Laggerbauer B., et al. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10:2001;329-338
51. Li Z., et al. The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 29:2001;2276-2283
52. Todd P.K., et al. 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. 100:2003;14374-14378
53. Steward O., Schuman E.M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24:2001;299-325
54. Steward O., Schuman E.M. Compartmentalized synthesis and degradation of proteins in neurons. Neuron. 40:2003;347-359
55. Weiler I.J., Greenough W.T. Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 90:1993;7168-7171
56. Job C., Eberwine J. Identification of sites for exponential translation in living dendrites. Proc. Natl. Acad. Sci. U. S. A. 98:2001;13037-13042
57. Merlin L.R., et al. Requirement of protein synthesis for group 1 mGluR-mediated induction of eplileptiform discharges. J. Neurophysiol. 80:1998;989-993
58. Lee A.C., et al. Role of synaptic metabotropic glutamate receptors in epileptiform discharges in hippocampal slices. J. Neurophysiol. 88:2002;1625-1633
59. Stoop R., et al. Activation of metabotropic glutamate 5 and NMDA receptors underlies the induction of persistent bursting and associated long-lasting changes in CA3 recurrent connections. J. Neurosci. 23:2003;5634-5644
60. Cohen A.S., Abraham W.C. Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors. J. Neurophysiol. 76:1996;953-962
61. Bashir Z.I., Collingridge G.L. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp. Brain Res. 100:1994;437-443
62. Palmer M.J., et al. The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology. 36:1997;1517-1532
63. Raymond C.R., et al. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong LTP. J. Neurosci. 20:2000;969-976
64. Zho W.M., et al. The group I metabotropic glutamate receptor agonist (S)-3, 5-dihydroxyphenylglycine induces a novel form of depotentiation in the CA1 region of the hippocampus. J. Neurosci. 22:2002;8838-8849
65. Xiao M.Y., et al. Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology. 41:2001;664-671
66. Zakharenko S.S., et al. Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron. 35:2002;1099-1110
67. 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. U. S. A. 99:2002;1639-1644
68. Harris K.M., Stevens J.K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9:1989;2982-2997
69. Nusser Z., et al. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:1998;545-559
70. Schikorski T., Stevens C.F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17:1997;5858-5867
71. Karachot L., et al. Induction of long-term depression in cerebellar Purkinje cells requires a rapidly turned over protein. J. Neurophysiol. 86:2001;280-289
72. Rodrigues S.M., et al. The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. J. Neurosci. 22:2002;5219-5229
73. Tatarczynska E., et al. Potential anxiolytic- and antidepressant-like effects of MPEP, a potent, selective and systemically active mGlu5 receptor antagonist. Br. J. Pharmacol. 132:2001;1423-1430
74. Graybiel A.M. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70:1998;119-136
75. Gubellini P., et al. Corticostriatal LTP requires combined mGluR1 and mGluR5 activation. Neuropharmacology. 44:2003;8-16
76. Chapman A.G., et al. Anticonvulsant activity of two metabotropic glutamate group I antagonists selective for the mGlu5 receptor: 2-methyl-6-(phenylethynyl)-pyridine (MPEP), and (E)-6-methyl-2-styryl-pyridine (SIB 1893). Neuropharmacology. 39:2000;1567-1574
77. Chen L., Toth M. Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience. 103:2001;1043-1050
78. Sourdet V., et al. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J. Neurosci. 23:2003;10238-10248
79. Castren M., et al. Augmentation of auditory N1 in children with fragile X syndrome. Brain Topogr. 15:2003;165-171
80. Brody S.A., et al. Disruption of prepulse inhibition in mice lacking mGluR1. Eur. J. Neurosci. 18:2003;3361-3366
81. Nielsen D.M., et al. Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res. 927:2002;8-17
82. Tachibana T., et al. Immunohistochemical expressions of mGluR5, P2Y2 receptor, PLC-beta1, and IP3R-I and -II in Merkel cells in rat sinus hair follicles. Histochem. Cell Biol. 120:2003;13-21
83. Walker K., et al. mGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurones mediate inflammatory hyperalgesia. Neuropharmacology. 40:2001;10-19
84. Neugebauer V., et al. Role of metabotropic glutamate receptor subtype mGluR1 in brief nociception and central sensitization of primate STT cells. J. Neurophysiol. 82:1999;272-282
85. Hu H.Z., et al. Functional group I metabotropic glutamate receptors in submucous plexus of guinea-pig ileum. Br. J. Pharmacol. 128:1999;1631-1635
86. Liu M., Kirchgessner A.L. Agonist- and reflex-evoked internalization of metabotropic glutamate receptor 5 in enteric neurons. J. Neurosci. 20:2000;3200-3205
87. Park D., et al. Translation of clock rhythmicity into neural firing in suprachiasmatic nucleus requires mGluR-PLCbeta4 signaling. Nat. Neurosci. 6:2003;337-338
88. Morales J., et al. Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron. 34:2002;961-972
89. Dockendorff T.C., et al. Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron. 34:2002;973-984
90. Inoue S., et al. A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 12:2002;1331-1335
91. Bear M.F., Cooper L.N. From molecules to mental states. Daedalus. 127:1998;131-144
92. Yan, Q., et al. (2003) Audiogenic seizures and effects of mGluR5 antagonist MPEP in the fMR1-tm1cgr Fragile X mouse. Program number 634.5. In Abstract Viewer/Itinerary Planner, Society for Neuroscience Online.
93. Lu Y.M., et al. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17:1997;5196-5205
94. Spooren W.P., et al. Novel allosteric antagonists shed light on mglu(5) receptors and CNS disorders. Trends Pharmacol. Sci. 22:2001;331-337
95. Migaud M., et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439