X-linked mental retardation: Focus on synaptic function and plasticity

Journal of Neurochemistry

Volumn 109, Issue 1, 2009, Pages 1-14

  Humeau, Yann ^a   Gambino, Frédéric ^a   Chelly, Jamel ^b   Vitale, Nicolas ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT COCHIN   (France)

Author keywords

LTP; Mental disorder; Receptor recycling; Synapse; Synaptic plasticity

Indexed keywords

P21 ACTIVATED KINASE 3;

BRAIN FUNCTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE MUTATION; HUMAN; NERVE CELL PLASTICITY; PRIORITY JOURNAL; REVIEW; SYNAPSE; X LINKED MENTAL RETARDATION;

ANIMALS; DENDRITIC SPINES; HUMANS; MENTAL RETARDATION, X-LINKED; MUTATION; NEURONAL PLASTICITY; PHENOTYPE; SYNAPSES;

EID: 61849104129     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05881.x     Document Type: Review

References (130)

1. Adesnik H. Nicoll R. A. (2007) Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598 4602.
2. Allen K. M., Gleeson J. G., Bagrodia S., Partington M. W., MacMillan J. C., Cerione R. A., Mulley J. C. Walsh C. A. (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20, 25 30.
3. Alvarez V. A. Sabatini B. L. (2007) Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 30, 79 97.
4. Antar L. N. Bassell G. J. (2003) Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface. Neuron. 37, 555 558.
5. Antar L. N., Afroz R., Dictenberg J. B., Carroll R. C. Bassell G. J. (2004) 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.
6. Asaka Y., Jugloff D. G., Zhang L., Eubanks J. H. Fitzsimonds R. M. (2006) Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis. 21, 217 227.
7. Bader M. F., Doussau F., Chasserot-Golaz S., Vitale N. Gasman S. (2004) Coupling actin and membrane dynamics during calcium-regulated exocytosis: a role for Rho and ARF GTPases. Biochim. Biophys. Acta 1742, 37 49.
8. Bagni C. Greenough W. T. (2005) From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat Rev Neurosci. 6, 376 387.
9. Bahi N., Friocourt G., Carrié A., Graham M. E., Weiss J. L., Chafey P., Fauchereau F., Burgoyne R. D. Chelly J. (2003) IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with Neuronal Calcium Sensor-1 and regulates exocytosis. Hum. Mol. Genet. 12, 1415 1425.
10. de Barry J., Janoshazi A., Dupont J. L., Procksch O., Chasserot-Golaz S., Jeromin A. Vitale N. (2006) Functional implication of neuronal calcium sensor-1 and phosphoinositol 4-kinase-beta interaction in regulated exocytosis of PC12 cells. J. Biol. Chem. 281, 18098 18111.
11. Bats C., Groc L. Choquet D. (2007) The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53, 719 734.
12. Béïque J. C. Andrade R. (2003) PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 546, 859 867.
13. Bellone C., Lüscher C. Mameli M. (2008) Mechanisms of synaptic depression triggered by metabotropic glutamate receptors. Cell Mol Life Sci. 65, 2913 2923.
14. Bienenstock E. L., Cooper L. N. Munro P. W. (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32 48.
15. Bienvenu T., des Portes V., Saint Martin A. et al. (1998) Non-specific X-linked semidominant mental retardation by mutations in a Rab GDP-dissociation inhibitor. Hum. Mol. Genet. 7, 1311 1315.
16. Bienvenu T., des Portes V., McDonell N. et al. (2000) Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am. J. Med. Genet. 93, 294 298.
17. Billuart P. Chelly J. (2003) From fragile X mental retardation protein to Rac1 GTPase: new insights from Fly CYFIP. Neuron. 38, 843 845.
18. Bliss T. V. Lomo T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331 356.
19. Boda B., Alberi S., Nikonenko I., Node-Langlois R., Jourdain P., Moosmayer M., Parisi-Jourdain L. Muller D. (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24, 10816 10825.
20. Bonhoeffer T. Yuste R. (2002) Spine motility. Phenomenology, mechanisms, and function. Neuron. 35, 1019 1027.
21. Born T. L., Smith D. E., Garka K. E., Renshaw B. R., Bertles J. S. Sims J. E. (2000) Identification and characterization of two members of a novel class of the interleukin-1 receptor (IL-1R) family. Delineation of a new class of IL-1R-related proteins based on signaling. J. Biol. Chem. 275, 29946 29954.
22. Carrié A., Jun L., Bienvenu T. et al. (1999) A new member of the IL-1 receptor family highly expressed in hippocampus and involved in X-linked mental retardation. Nat. Genet. 23, 25 31.
23. Carroll R. C., Beattie E. C., Xia H., Lüscher C., Altschuler Y., Nicoll R. A., Malenka R. C. von Zastrow M. (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc. Natl Acad. Sci. USA 96, 14112 14117.
24. Castro-Alamancos M. A. Calcagnotto M. E. (1999) Presynaptic long-term potentiation in cortico-thalamic synapses. J. Neurosci. 19, 9090 9097.
25. Chahrour M. Zoghbi H. Y. (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron. 56, 422 437.
26. Chang Q., Khare G., Dani V., Nelson S. Jaenisch R. (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron. 49, 321 323.
27. Chao H. T., Zoghbi H. Y. Rosenmund C. (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron. 56, 58 65.
28. Chechlacz M. Gleeson J. G. (2003) Is mental retardation a defect of synapse structure and function? Pediatr. Neurol. 29, 11 17.
29. Chelly J., Khelfaoui M., Francis F., Chérif B. Bienvenu T. (2006) Genetics and pathophysiology of mental retardation. Eur. J. Hum. Genet. 14, 701 713.
30. Chen L., Chetkovich D. M., Petralia R. S., Sweeney N. T., Kawasaki Y., Wenthold R. J., Bredt D. S. Nicoll R. A. (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936 943.
31. Collins A. L., Levenson J. M., Vilaythong A. P., Richman R., Armstrong D. L., Noebels J. L., David Sweatt J. Zoghbi H. Y. (2004) Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 13, 2679 2689.
32. Comery T. A., Harris J. B., Willems P. J., Oostra B. A., Irwin S. A., Weiler I. J. Greenough W. T. (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl Acad. Sci. USA 94, 5401 5404.
33. Cooper S. J. Donald O. (2005) Hebb's synapse and learning rule: a history and commentary. Neurosci. Biobehav. Rev. 28, 851 874.
34. D'Adamo P., Menegon A., Lo Nigro C. et al. (1998) Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nat. Genet. 19, 134 139.
35. D'Adamo P., Welzl H., Papadimitriou S. et al. (2002) Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice. Hum. Mol. Genet. 11, 2567 2580.
36. Dani V. S., Chang Q., Maffei A., Turrigiano G. G., Jaenisch R. Nelson S. B. (2005) Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl Acad. Sci. USA 102, 12560 12565.
37. Desai N. S., Casimiro T. M., Gruber S. M. Vanderklish P. W. (2006) Early postnatal plasticity in neocortex of Fmr1 knockout mice. J. Neurophysiol. 96, 1734 1745.
38. Doussau F., Clabecq A., Henry J. P., Darchen F. Poulain B. (1998) Calcium-dependent regulation of rab3 in short-term plasticity. J. Neurosci. 18, 3147 3157.
39. Fisher T. L. Blenis J. (1996) Evidence for two catalytically active kinase domains in pp90rsk. Mol. Cell. Biol. 16, 1212 1219.
40. Fourcaudot E., Gambino F., Humeau Y., Casassus G., Shaban H., Poulain B. Lüthi A. (2008) cAMP/PKA signaling and RIM1alpha mediate presynaptic LTP in the lateral amygdala. Proc. Natl Acad. Sci. USA 105, 15130 15135.
41. Frints S. G., Froyen G., Marynen P. Fryns J. P. (2002) X-linked mental retardation: vanishing boundaries between non-specific (MRX) and syndromic (MRXS) forms. Clin. Genet. 62, 423 432.
42. Fukuda T., Itoh M., Ichikawa T., Washiyama K. Goto Y. (2005) Delayed maturation of neuronal architecture and synaptogenesis in cerebral cortex of Mecp2-deficient mice. J. Neuropathol. Exp. Neurol. 64, 537 544.
43. 2+-channel and neurite elongation. Proc. Natl Acad. Sci. USA 104, 9063 9068.
44. Gao X., Xi G., Niu Y. et al. (2008) A study on the correlation between IL1RAPL1 and human cognitive ability. Neurosci. Lett. 438, 163 167.
45. Godfraind J., Reyniers E., De Boulle K., D'Hooge R., De Deyn P., Bakker C., Oostra B., Kooy R. Willems P. (1996) Long-term potentiation in the hippocampus of fragile X knockout mice. Am. J. Med. Genet. 64, 246 251.
46. Govek E. E., Newey S. E., Akerman C. J., Cross J. R., Van der Veken L. Van Aelst L. (2004) The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat. Neurosci. 7, 364 372.
47. Gu Y., McIlwain K. L., Weeber E. J. et al. (2002) Impaired conditioned fear and enhanced long-term potentiation in Fmr2 knock-out mice. J. Neurosci. 22, 2753 2763.
48. Guy J., Gan J., Selfridge J., Cobb S. Bird A. (2007) Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143 1147.
49. Hammond S. M., Jenco J. M., Nakashima S., Cadwallader K., Gu Q., Cook S., Nozawa Y., Prestwich G. D., Frohman M. A. Morris A. J. (1997) Characterization of two alternately spliced forms of phospholipase D1. Activation of the purified enzymes by phosphatidylinositol 4,5-bisphosphate, ADP-ribosylation factor, and Rho family monomeric GTP-binding proteins and protein kinase C-alpha. J. Biol. Chem. 272, 3860 3868.
50. Hayashi M. L., Choi S. Y., Rao B. S., Jung H. Y., Lee H. K., Zhang D., Chattarji S., Kirkwood A. Tonegawa S. (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice. Neuron. 42, 773 787.
51. Heine M., Groc L., Frischknecht R., Béïque J. C., Lounis B., Rumbaugh G., Huganir R. L., Cognet L. Choquet D. (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201 205.
52. Huber K. M., Gallagher S. M., Warren S. T. Bear M. F. (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl Acad. Sci. USA 99, 7746 7750.
53. Humeau Y., Vitale N., Chasserot-Golaz S., Dupont J. L., Du G., Frohman M. A., Bader M. F. Poulain B. (2001) A role for phospholipase D1 in neurotransmitter release. Proc. Natl Acad. Sci. USA 98, 15300 15305.
54. Humeau Y., Popoff M. R., Kojima H., Doussau F. Poulain B. (2002) Rac GTPase plays an essential role in exocytosis by controlling the fusion competence of release sites. J. Neurosci. 22, 7968 7981.
55. Humeau Y., Herry C., Kemp N., Shaban H., Fourcaudot E., Bissière S. Lüthi A. (2005) Dendritic spine heterogeneity determines afferent-specific Hebbian plasticity in the amygdala. Neuron. 45, 119 131.
56. Humeau Y., Doussau F., Popoff M. R., Benfenati F. Poulain B. (2007) Fast changes in the functional status of release sites during short-term plasticity: involvement of a frequency-dependent bypass of Rac at Aplysia synapses. J. Physiol. 583, 983 1004.
57. Inlow J. K. Restifo L. L. (2004) Molecular and comparative genetics of mental retardation. Genetics 166, 835 881.
58. Isaac J. T., Ashby M. McBain C. J. (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron. 54, 859 871.
59. Ishizaki H., Miyoshi J., Kamiya H., Togawa A., Tanaka M., Sasaki T., Endo K., Mizoguchi A., Ozawa S. Takai Y. (2000) Role of rab GDP dissociation inhibitor alpha in regulating plasticity of hippocampal neurotransmission. Proc. Natl Acad. Sci. USA 97, 11587 11592.
60. Kaufmann W. E. Moser H. W. (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb. Cortex 10, 981 991.
61. Khelfaoui M., Denis C., van Galen E. et al. (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J. Neurosci. 27, 9439 9450.
62. Koekkoek S. K., Yamaguchi K., Milojkovic B. A. et al. (2005) Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron. 47, 339 352.
63. Kreis P., Rousseau V., Thévenot E., Combeau G. Barnier J. V. (2008) The four mammalian splice variants encoded by the p21-activated kinase 3 gene have different biological properties. J. Neurochem. 106, 1184 1197.
64. Krueger S. Fitzsimonds R. M. (2006) Remodeling the plasticity debate: the presynaptic locus revisited. Physiology 21, 346 351.
65. Larson J., Jessen R., Kim D., Fine A. du Hoffmann J. (2005) Age-dependent and selective impairment of long-term potentiation in the anterior piriform cortex of mice lacking the fragile X mental retardation protein. J. Neurosci. 25, 9460 9469.
66. Laumonnier F., Cuthbert P. C. Grant S. G. (2007) The role of neuronal complexes in human X-linked brain diseases. Am. J. Hum. Genet. 80, 205 220.
67. Lauterborn J. C., Rex C. S., Kramár E., Chen L. Y., Pandyarajan V., Lynch G. Gall C. M. (2007) Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J. Neurosci. 27, 10685 10694.
68. Leprêtre F., Delannoy V., Froguel P., Vasseur F. Montpellier C. (2003) Dissection of an inverted X(p21.3q27.1) chromosome associated with mental retardation. Cytogenet Genome Res. 101, 124 129.
69. Li J., Pelletier M. R., Perez Velazquez J. L. Carlen P. L. (2002) Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Mol. Cell. Neurosci. 19, 138 151.
70. Lledo P. M., Zhang X., Südhof T. C., Malenka R. C. Nicoll R. A. (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279, 399 403.
71. Lopez de Armentia M. Sah P. (2007) Bidirectional synaptic plasticity at nociceptive afferents in the rat central amygdala. J. Physiol. 581, 961 970.
72. Malinow R. Malenka R. C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103 126.
73. Mandel J. L. Chelly J. (2004) Monogenic X-linked mental retardation: is it as frequent as currently estimated? The paradox of the ARX (Aristaless X) mutations. Eur. J. Hum. Genet. 12, 689 693.
74. Matsuzaki M., Honkura N., Ellis-Davies G. C. Kasai H. (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761 766.
75. Matus A. (2000) Actin-based plasticity in dendritic spines. Science 290, 754 758.
76. McMullan R., Hiley E., Morrison P. Nurrish S. J. (2006) Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. Genes Dev. 20, 65 76.
77. Menegon A., Bonanomi D., Albertinazzi C., Lotti F., Ferrari G., Kao H. T., Benfenati F., Baldelli P. Valtorta F. (2006) Protein kinase A-mediated synapsin I phosphorylation is a central modulator of Ca2 + -dependent synaptic activity. J. Neurosci. 26, 11670 11681.
78. Meng J., Meng Y., Hanna A., Janus C. Jia Z. (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J. Neurosci. 25, 6641 6650.
79. Moretti P., Levenson J. M., Battaglia F., Atkinson R., Teague R., Antalffy B., Armstrong D., Arancio O., Sweatt J. D. Zoghbi H. Y. (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 26, 319 327.
80. Nadif Kasri N. Van Aelst L. (2008) Rho-linked genes and neurological disorders. Pflugers Arch. 455, 787 797.
81. Nägerl U. V., Eberhorn N., Cambridge S. B. Bonhoeffer T. (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron. 44, 759 767.
82. Nakamoto M., Nalavadi V., Epstein M. P., Narayanan U., Bassell G. J. Warren S. T. (2007) Fragile X mental retardation protein deficiency leads to excessive mGluR5-dependent internalization of AMPA receptors. Proc. Natl Acad. Sci. USA 104, 15537 15542.
83. Nevian T. Sakmann B. (2006) Spine Ca2 + signaling in spike-timing- dependent plasticity. J. Neurosci. 26, 11001 11013.
84. Newey S. E., Velamoor V., Govek E. E. Van Aelst L. (2005) Rho GTPases, dendritic structure, and mental retardation. J. Neurobiol. 64, 58 74.
85. Nicoll R. A. Schmitz D. (2005) Synaptic plasticity at hippocampal mossy fiber synapses. Nat Rev Neurosci 6, 863 876.
86. Nimchinsky E. A., Oberlander A. M. Svoboda K. (2001) Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21, 5139 5146.
87. Nodé-Langlois R., Muller D. Boda B. (2006) Sequential implication of the mental retardation proteins ARHGEF6 and PAK3 in spine morphogenesis. J Cell Sci. 119, 4986 4993.
88. Paradee W., Melikian H. E., Rasmussen D. L., Kenneson A., Conn P. J. Warren S. T. (1999) Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 94, 185 192.
89. Pinheiro P. S. Mulle C. (2008) Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci. 9, 423 436.
90. Piton A., Michaud J. L., Peng H. et al. S2D team (2008) Mutations in the calcium-related gene IL1RAPL1 are associated with autism. Hum Mol Genet. 17, 3965 3974.
91. Poirier K., Lacombe D., Gilbert-Dussardier B. et al. (2006) Screening of ARX in mental retardation families: Consequences for the strategy of molecular diagnosis. Neurogenetics. 7, 39 46.
92. Poirier R., Jacquot S., Vaillend C. et al. (2007) Deletion of the Coffin-Lowry syndrome gene Rsk2 in mice is associated with impaired spatial learning and reduced control of exploratory behavior. Behav. Genet. 37, 31 50.
93. Purpura D. P. (1974) Dendritic spine "dysgenesis" and mental retardation. Science 186, 1126 1128.
94. Rizo J. Rosenmund C. (2008) Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665 674.
95. Ropers H. H. Hamel B. C. J. (2005) X-linked mental retardation. Nat Rev Genet 6, 42 57.
96. Sabatini B. L., Oertner T. G. Svoboda K. (2002) The life cycle of Ca(2 +) ions in dendritic spines. Neuron. 33, 439 452.
97. Sah P., Westbrook R. F. Lüthi A. (2008) Fear conditioning and long-term potentiation in the amygdala: what really is the connection? Ann. NY Acad. Sci. 1129, 88 95.
98. Salin P. A., Malenka R. C. Nicoll R. A. (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16, 797 803.
99. Saneyoshi T., Wayman G., Fortin D., Davare M., Hoshi N., Nozaki N., Natsume T. Soderling T. R. (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57, 94 107.
100. Sasaki R., Inamo Y., Saitoh K., Hasegawa T., Kinoshita E. Ogata T. (2003) Mental retardation in a boy with congenital adrenal hypoplasia: a clue to contiguous gene syndrome involving DAX1 and IL1RAPL. Endocr. J. 50, 303 307.
101. Schenck A., Bardoni B., Langmann C., Harden N., Mandel J. L. Giangrande A. (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38, 887 898.
102. Schlüter O. M., Basu J., Südhof T. C. Rosenmund C. (2006) Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J. Neurosci. 26, 1239 1246.
103. Schoch S. Gundelfinger E. D. (2006) Molecular organization of the presynaptic active zone. Cell Tissue Res. 326, 379 391.
104. Sdrulla A. D. Linden D. J. (2007) Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Nat. Neurosci. 10, 546 548.
105. Sjöström P. J. Nelson S. B. (2002) Spike timing, calcium signals and synaptic plasticity. Curr. Opin. Neurobiol. 12, 305 314.
106. Sjöström P. J., Turrigiano G. G. Nelson S. B. (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149 1164.
107. Sudhof T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509 547.
108. Tabolacci E., Pomponi M. G., Pietrobono R., Terracciano A., Chiurazzi P. Neri G. (2006) A truncating mutation in the IL1RAPL1 gene is responsible for X-linked mental retardation in the MRX21 family. Am J Med Genet A. 140 (5 482 487.
109. Tabuchi K., Blundell J., Etherton M. R., Hammer R. E., Liu X., Powell C. M. Südhof T. C. (2007) A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318, 71 76.
110. Tada T. Sheng M. (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 16, 95 101.
111. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G. C. Kasai H. (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319, 1627 1628.
112. Tashiro A. Yuste R. (2004) Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol. Cell. Neurosci. 26, 429 440.
113. The Dutch-Belgian Fragile X Consortium (1994) FMR1 knockout mice: a model to study fragile X mental retardation. Cell 78, 23 33.
114. Thomas G. M., Rumbaugh G. R., Harrar D. B. Huganir R. L. (2005a) Ribosomal S6 kinase 2 interacts with and phosphorylates PDZ domain-containing proteins and regulates AMPA receptor transmission. Proc. Natl Acad. Sci. USA 102, 15006 15011.
115. Thomas G. M., Rumbaugh G. R., Harrar D. B. Huganir R. L. (2005b) Ribosomal S6 kinase 2 interacts with and phosphorylates PDZ domain-containing proteins and regulates AMPA receptor transmission. Proc. Natl Acad. Sci. USA 102, 15006 15011.
116. Trivier E., De Cesare D., Jacquot S., Pannetier S., Zackai E., Young I., Mandel J. L., Sassone-Corsi P. Hanauer A. (1996) Mutations in the kinase Rsk-2 associated with Coffin-Lowry syndrome. Nature 384, 567 570.
117. Turrigiano G. G. (2000) AMPA receptors unbound: membrane cycling and synaptic plasticity. Neuron 26, 5 8.
118. Turrigiano G. G., Leslie K. R., Desai N. S., Rutherford L. C. Nelson S. B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892 896.
119. Vaillend C., Poirier R. Laroche S. (2008) Genes, plasticity and mental retardation. Behav. Brain Res. 192, 88 105.
120. Verkerk A. J., Pieretti M., Sutcliffe J. S. et al. (1991) Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65, 905 914.
121. 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. (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl Acad. Sci. USA 94, 5395 5400.
122. Weiss J. L. Burgoyne R. D. (2002) Sense and sensibility in the regulation of voltage-gated Ca(2 +) channels. Trends Neurosci. 25, 489 491.
123. Wheway J. M., Yau S. C., Nihalani V., Ellis D., Irving M., Splitt M. Roberts R. G. (2003) A complex deletion-inversion-deletion event results in a chimeric IL1RAPL1-dystrophin transcript and a contiguous gene deletion syndrome. J. Med. Genet. 40, 127 131.
124. Wilson B. M. Cox C. L. (2007) Absence of metabotropic glutamate receptor-mediated plasticity in the neocortex of fragile X mice. Proc. Natl Acad. Sci. USA 104, 2454 2459.
125. Yasuda R., Sabatini B. L. Svoboda K. (2003) Plasticity of calcium channels in dendritic spines. Nat. Neurosci. 6, 948 955.
126. Zeniou-Meyer M., Zabari N., Ashery U. et al. (2007) Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J. Biol. Chem. 282, 21746 21757.
127. Zeniou-Meyer M., Liu Y., Béglé A., Olanish M., Hanauer A., Becherer U., Rettig J., Bader M. F. Vitale N. (2008) The Coffin-Lowry syndrome-associated protein RSK2 is implicated in calcium-regulated exocytosis through the regulation of PLD1. Proc. Natl Acad. Sci. USA 105, 8434 8439.
128. Zhang H., Webb D. J., Asmussen H., Niu S. Horwitz A. F. (2005) A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 25, 3379 3388.
129. Zhao M., Toyoda H., Ko S., Ding H., Wu L. Zhuo M. (2005) Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J. Neurosci. 25, 7385 7392.
130. Zhou Q., Homma K. J. Poo M. M. (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749 757.