Synaptic plasticity and signaling in rett syndrome

Developmental Neurobiology

Volumn 74, Issue 2, 2014, Pages 178-196

  Della Sala, Grazia ^a   Pizzorusso, Tommaso ^a,b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b CNR   (Italy)

Author keywords

CDKL5; Dendritic spine; DNA methylation; MeCP2; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR FOXG1; MAMMALIAN TARGET OF RAPAMYCIN; METHYL CPG BINDING PROTEIN 2; PROTEIN; PROTEIN CDKL 5; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ARTICLE; BRAIN DEVELOPMENT; BREATHING DISORDER; CELL TYPE; CENTRAL NERVOUS SYSTEM FUNCTION; DENDRITIC CELL; FACE VALIDITY; GLIA; GLIA CELL; HAND MOVEMENT; HUMAN; INTRACELLULAR SIGNALING; MORPHOLOGY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RETT SYNDROME; SEIZURE; SYNAPTIC TRANSMISSION;

CDKL5; DENDRITIC SPINE; DNA METHYLATION; MECP2; SYNAPTIC PLASTICITY;

ANIMALS; HUMANS; METHYL-CPG-BINDING PROTEIN 2; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; RETT SYNDROME; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84891903668     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22114     Document Type: Article

References (171)

1. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188.
2. Archer HL, Whatley SD, Evans JC, Ravine D, Huppke P, Kerr A, Bunyan D, et al. 2006. Gross rearrangements of the MECP2 gene are found in both classical and atypical Rett syndrome patients. J Med Genet 43:451-456.
3. Ariani F, Hayek G, Rondinella D, Artuso R, Mencarelli MA, Spanhol-Rosseto A, Pollazzon M, et al. 2008. FOXG1 is responsible for the congenital variant of Rett syndrome. Am J Hum Genet 83:89-93.
4. Armstrong DD. 2002. Neuropathology of Rett syndrome. Ment Retard Dev Disabil Res Rev 8:72-76.
5. Armstrong DD, Dunn K, Antalffy B. 1998. Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol 57:1013-1017.
6. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM. 2006. Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21:217-227.
7. Ballas N, Lioy DT, Grunseich C, Mandel G. 2009. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12:311-317.
8. Belichenko NP, Belichenko PV, Mobley WC. 2009a. Evidence for both neuronal cell autonomous and nonautonomous effects of methyl-CpG-binding protein 2 in the cerebral cortex of female mice with Mecp2 mutation. Neurobiol Dis 34:71-77.
9. Belichenko PV, Kleschevnikov AM, Masliah E, Wu C, Takimoto-Kimura R, Salehi A, Mobley WC. 2009b. Excitatory-inhibitory relationship in the fascia dentata in the Ts65Dn mouse model of Down syndrome. J Comp Neurol 512:453-466.
10. Belichenko PV, Kleschevnikov AM, Salehi A, Epstein CJ, Mobley WC. 2007. Synaptic and cognitive abnormalities in mouse models of Down syndrome: Exploring genotype-phenotype relationships. J Comp Neurol 504:329-345.
11. Belichenko PV, Wright EE, Belichenko NP, Masliah E, Li HH, Mobley WC, Francke U. 2009c. Widespread changes in dendritic and axonal morphology in Mecp2-mutant mouse models of Rett syndrome: Evidence for disruption of neuronal networks. J Comp Neurol 514:240-258.
12. Benitez-Bribiesca L, De la Rosa-Alvarez I, Mansilla-Olivares A. 1999. Dendritic spine pathology in infants with severe protein-calorie malnutrition. Pediatrics 104:e21.
13. Bhatt DH, Zhang S, Gan WB. 2009. Dendritic spine dynamics. Annu Rev Physiol 71:261-282.
14. Blackman MP, Djukic B, Nelson SB, Turrigiano GG. 2012. A critical and cell-autonomous role for MeCP2 in synaptic scaling up. J Neurosci 32:13529-13536.
15. Boggio EM, Lonetti G, Pizzorusso T, Giustetto M. 2010. Synaptic determinants of rett syndrome. Front Synaptic Neurosci 2:28.
16. Calfa G, Hablitz JJ, Pozzo-Miller L. 2011. Network hyperexcitability in hippocampal slices from Mecp2 mutant mice revealed by voltage-sensitive dye imaging. J Neurophysiol 105:1768-1784.
17. Campos M Jr, Pestana CP, dos Santos AV, Ponchel F, Churchman S, Abdalla-Carvalho CB, dos Santos JM, et al. 2011. A MECP2 missense mutation within the MBD domain in a Brazilian male with autistic disorder. Brain Dev 33:807-809.
18. Carney RM, Wolpert CM, Ravan SA, Shahbazian M, Ashley-Koch A, Cuccaro ML, Vance JM, et al. 2003. Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatr Neurol 28:205-211.
19. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY. 2008. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320:1224-1229.
20. 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 49:341-348.
21. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, et al. 2010. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468:263-269.
22. Chao HT, Zoghbi HY, Rosenmund C. 2007. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56:58-65.
23. Chapleau CA, Boggio EM, Calfa G, Percy AK, Giustetto M, Pozzo-Miller L. 2012. Hippocampal CA1 pyramidal neurons of Mecp2 mutant mice show a dendritic spine phenotype only in the presymptomatic stage. Neural Plast 2012:976164.
24. Chapleau CA, Larimore JL, Theibert A, Pozzo-Miller L. 2009. Modulation of dendritic spine development and plasticity by BDNF and vesicular trafficking: Fundamental roles in neurodevelopmental disorders associated with mental retardation and autism. J Neurodev Disord 1:185-196.
25. Chen C, Regehr WG. 2000. Developmental remodeling of the retinogeniculate synapse. Neuron 28:955-966.
26. Chen JL, Villa KL, Cha JW, So PT, Kubota Y, Nedivi E. 2012. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74:361-373.
27. Chen RZ, Akbarian S, Tudor M, Jaenisch R. 2001. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27:327-331.
28. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC, Jaenisch R, et al. 2003. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302:885-889.
29. Chen Y, Dube CM, Rice CJ, Baram TZ. 2008. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J Neurosci 28:2903-2911.
30. Cheval H, Guy J, Merusi C, De Sousa D, Selfridge J, Bird A. 2012. Postnatal inactivation reveals enhanced requirement for MeCP2 at distinct age windows. Hum Mol Genet 21:3806-3814.
31. Cobb S, Guy J, Bird A. 2010. Reversibility of functional deficits in experimental models of Rett syndrome. Biochem Soc Trans 38:498-506.
32. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70:271-288.
33. Cohen DR, Matarazzo V, Palmer AM, Tu Y, Jeon OH, Pevsner J, Ronnett GV. 2003. Expression of MeCP2 in olfactory receptor neurons is developmentally regulated and occurs before synaptogenesis. Mol Cell Neurosci 22:417-429.
34. Cohen S, Gabel HW, Hemberg M, Hutchinson AN, Sadacca LA, Ebert DH, Harmin DA, et al. 2011. Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function. Neuron 72:72-85.
35. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, David Sweatt J, et al. 2004. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 13:2679-2689.
36. Coutinho AM, Oliveira G, Katz C, Feng J, Yan J, Yang C, Marques C, et al. 2007. MECP2 coding sequence and 3'UTR variation in 172 unrelated autistic patients. Am J Med Genet B Neuropsychiatr Genet 144:475-483.
37. Cruz-Martin A, Crespo M, Portera-Cailliau C. 2010. Delayed stabilization of dendritic spines in fragile X mice. J Neurosci 30:7793-7803.
38. Danesin C, Peres JN, Johansson M, Snowden V, Cording A, Papalopulu N, Houart C. 2009. Integration of telencephalic Wnt and hedgehog signaling center activities by Foxg1. Dev Cell 16:576-587.
39. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. 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.
40. Dastidar SG, Bardai FH, Ma C, Price V, Rawat V, Verma P, Narayanan V, et al. 2012. Isoform-specific toxicity of Mecp2 in postmitotic neurons: Suppression of neurotoxicity by FoxG1. J Neurosci 32:2846-2855.
41. Dastidar SG, Landrieu PM, D'Mello SR. 2011. FoxG1 promotes the survival of postmitotic neurons. J Neurosci 31:402-413.
42. De Filippis B, Fabbri A, Simone D, Canese R, Ricceri L, Malchiodi-Albedi F, Laviola G, et al. 2012. Modulation of RhoGTPases improves the behavioral phenotype and reverses astrocytic deficits in a mouse model of Rett syndrome. Neuropsychopharmacology 37:1152-1163.
43. Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248:73-76.
44. Deogracias R, Yazdani M, Dekkers MP, Guy J, Ionescu MC, Vogt KE, Barde YA. 2012. Fingolimod, a sphingosine-1 phosphate receptor modulator, increases BDNF levels and improves symptoms of a mouse model of Rett syndrome. Proc Natl Acad Sci USA 109:14230-14235.
45. Derecki NC, Cronk JC, Kipnis J. 2013. The role of microglia in brain maintenance: implications for Rett syndrome. Trends Immunol 34:144-150.
46. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SB, Guyenet PG, Kipnis J. 2012. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484:105-109.
47. Durand S, Patrizi A, Quast KB, Hachigian L, Pavlyuk R, Saxena A, Carninci P, et al. 2012. NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76:1078-1090.
48. Ebert DH, Gabel HW, Robinson ND, Kastan NR, Hu LS, Cohen S, Navarro AJ, et al. 2013. Activity-dependent phosphorylation of MECP2 threonine 308 regulates interaction with NcoR. Nature, 499:341-345.
49. Fehr S, Wilson M, Downs J, Williams S, Murgia A, Sartori S, Vecchi M, et al. 2013. The CDKL5 disorder is an independent clinical entity associated with early-onset encephalopathy. Eur J Hum Genet 21:266-273.
50. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, et al. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
51. Ferrer I, Gullotta F. 1990. Down's syndrome and Alzheimer's disease: dendritic spine counts in the hippocampus. Acta Neuropathol 79:680-685.
52. Fischer M, Reuter J, Gerich FJ, Hildebrandt B, Hagele S, Katschinski D, Muller M. 2009. Enhanced hypoxia susceptibility in hippocampal slices from a mouse model of rett syndrome. J Neurophysiol 101:1016-1032.
53. Florian C, Bahi-Buisson N, Bienvenu T. 2012. FOXG1-related disorders: From clinical description to molecular genetics. Mol Syndromol 2:153-163.
54. 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.
55. Gambino F, Khelfaoui M, Poulain B, Bienvenu T, Chelly J, Humeau Y. 2010. Synaptic maturation at cortical projections to the lateral amygdala in a mouse model of Rett syndrome. PLoS One 5:e11399.
56. Giacometti E, Luikenhuis S, Beard C, Jaenisch R. 2007. Partial rescue of MeCP2 deficiency by postnatal activation of MeCP2. Proc Natl Acad Sci USA 104:1931-1936.
57. Godement P, Salaun J, Imbert M. 1984. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230:552-575.
58. Goffin D, Allen M, Zhang L, Amorim M, Wang IT, Reyes AR, Mercado-Berton A, et al. 2011. Rett syndrome mutation MeCP2 T158A disrupts DNA binding, protein stability and ERP responses. Nat Neurosci 15:274-283.
59. Gonzales ML, Adams S, Dunaway KW, LaSalle JM. 2012. Phosphorylation of distinct sites in MeCP2 modifies cofactor associations and the dynamics of transcriptional regulation. Mol Cell Biol 32:2894-2903.
60. Greenberg ME, Xu B, Lu B, Hempstead BL. 2009. New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29:12764-12767.
61. Guerrini R, Parrini E. 2012. Epilepsy in Rett syndrome, and CDKL5- and FOXG1-gene-related encephalopathies. Epilepsia 53:2067-2078.
62. Guy J, Cheval H, Selfridge J, Bird A. 2011. The role of MeCP2 in the brain. Annu Rev Cell Dev Biol 27:631-652.
63. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326.
64. Hagberg B. 1985. Rett's syndrome: prevalence and impact on progressive severe mental retardation in girls. Acta Paediatr Scand 74:405-408.
65. Han K, Kim E. 2008. Synaptic adhesion molecules and PSD-95. Prog Neurobiol 84:263-283.
66. Hanashima C, Fernandes M, Hebert JM, Fishell G. 2007. The role of Foxg1 and dorsal midline signaling in the generation of Cajal-Retzius subtypes. J Neurosci 27:11103-11111.
67. Hanashima C, Li SC, Shen L, Lai E, Fishell G. 2004. Foxg1 suppresses early cortical cell fate. Science 303:56-59.
68. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
69. Hering H, Sheng M. 2001. Dendritic spines: Structure, dynamics and regulation. Nat Rev Neurosci 2:880-888.
70. Holtmaat A, Svoboda K. 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647-658.
71. Hooks BM, Chen C. 2006. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52:281-291.
72. Hooks BM, Chen C. 2008. Vision triggers an experience-dependent sensitive period at the retinogeniculate synapse. J Neurosci 28:4807-4817.
73. Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W. 2005. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 22:661-676.
74. Johnson RA, Lam M, Punzo AM, Li H, Lin BR, Ye K, Mitchell GS, et al. 2012. 7, 8-dihydroxyflavone exhibits therapeutic efficacy in a mouse model of Rett syndrome. J Appl Physiol 112:704-710.
75. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, et al. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187-191.
76. Kano M, Hashimoto K. 2009. Synapse elimination in the central nervous system. Curr Opin Neurobiol 19:154-161.
77. Katz DM, Berger-Sweeney JE, Eubanks JH, Justice MJ, Neul JL, Pozzo-Miller L, Blue ME, et al. 2012. Preclinical research in Rett syndrome: setting the foundation for translational success. Dis Models Mechanisms 5:733-745.
78. Kim KY, Hysolli E, Park IH. 2011. Neuronal maturation defect in induced pluripotent stem cells from patients with Rett syndrome. Proc Natl Acad Sci USA 108:14169-14174.
79. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, et al. 2006. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9:1294-1301.
80. Kishi N, Macklis JD. 2004. MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions. Mol Cell Neurosci 27:306-321.
81. Kline DD, Ogier M, Kunze DL, Katz DM. 2010. Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice. J Neurosci 30:5303-5310.
82. Kokura K, Kaul SC, Wadhwa R, Nomura T, Khan MM, Shinagawa T, Yasukawa T, et al. 2001. The Ski protein family is required for MeCP2-mediated transcriptional repression. J Biol Chem 276:34115-34121.
83. Kondo M, Gray LJ, Pelka GJ, Christodoulou J, Tam PP, Hannan AJ. 2008. Environmental enrichment ameliorates a motor coordination deficit in a mouse model of Rett syndrome-Mecp2 gene dosage effects and BDNF expression. Eur J Neurosci 27:3342-3350.
84. Kron M, Howell CJ, Adams IT, Ransbottom M, Christian D, Ogier M, Katz DM. 2012. Brain activity mapping in Mecp2 mutant mice reveals functional deficits in forebrain circuits, including key nodes in the default mode network, that are reversed with ketamine treatment. J Neurosci 32:13860-13872.
85. Kron M, Zimmermann JL, Dutschmann M, Funke F, Muller M. 2011. Altered responses of MeCP2-deficient mouse brain stem to severe hypoxia. J Neurophysiol 105:3067-3079.
86. Kurt MA, Davies DC, Kidd M, Dierssen M, Florez J. 2000. Synaptic deficit in the temporal cortex of partial trisomy 16 (Ts65Dn) mice. Brain Res 858:191-197.
87. Ladeby R, Wirenfeldt M, Garcia-Ovejero D, Fenger C, Dissing-Olesen L, Dalmau I, Finsen B. 2005. Microglial cell population dynamics in the injured adult central nervous system. Brain Res Brain Res Rev 48:196-206.
88. Landi S, Putignano E, Boggio EM, Giustetto M, Pizzorusso T, Ratto GM. 2011. The short-time structural plasticity of dendritic spines is altered in a model of Rett syndrome. Sci Rep 1:45.
89. Lang M, Wither RG, Brotchie JM, Wu C, Zhang L, Eubanks JH 2013. Selective preservation of MeCP2 in catecholaminergic cells is sufficient to improve the behavioral phenotype of male and female Mecp2-deficient mice. Hum Mol Genet, 15;22(2):358-371.
90. Levy SE, Mandell DS, Schultz RT. 2009. Autism. Lancet 374:1627-1638.
91. Li H, Zhong X, Chau KF, Williams EC, Chang Q. 2011. Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP and spatial memory. Nat Neurosci 14:1001-1008.
92. Lin C, Franco B, Rosner MR. 2005. CDKL5/Stk9 kinase inactivation is associated with neuronal developmental disorders. Hum Mol Genet 14:3775-3786.
93. Lintas C, Sacco R, Persico AM. 2012. Genome-wide expression studies in autism spectrum disorder, Rett syndrome, and Down syndrome. Neurobiol Dis 45:57-68.
94. Lioy DT, Garg SK, Monaghan CE, Raber J, Foust KD, Kaspar BK, Hirrlinger PG, et al. 2011. A role for glia in the progression of Rett's syndrome. Nature 475:497-500.
95. Lonetti G, Angelucci A, Morando L, Boggio EM, Giustetto M, Pizzorusso T. 2010. Early environmental enrichment moderates the behavioral and synaptic phenotype of MeCP2 null mice. Biol Psychiatry 67:657-665.
96. Lyst MJ, Ekiert R, Ebert DH, Merusi C, Nowak J, Selfridge J, Guy J, et al. 2013. Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor. Nat Neurosci, 16:898-902.
97. Maezawa I, Jin LW. 2010. Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30:5346-5356.
98. Maezawa I, Swanberg S, Harvey D, LaSalle JM, Jin LW. 2009. Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions. J Neurosci 29:5051-5061.
99. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, et al. 2010. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143:527-539.
100. Mari F, Azimonti S, Bertani I, Bolognese F, Colombo E, Caselli R, Scala E, et al. 2005. CDKL5 belongs to the same molecular pathway of MeCP2 and it is responsible for the early-onset seizure variant of Rett syndrome. Hum Mol Genet 14:1935-1946.
101. Marin-Padilla M. 1976. Pyramidal cell abnormalities in the motor cortex of a child with Down's syndrome. A Golgi study. J Comp Neurol 167:63-81.
102. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, et al. 2003. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302:890-893.
103. Matijevic T, Knezevic J, Slavica M, Pavelic J. 2009. Rett syndrome: from the gene to the disease. Eur Neurol 61:3-10.
104. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290:754-758.
105. McGraw CM, Samaco RC, Zoghbi HY. 2011. Adult neural function requires MeCP2. Science 333:186.
106. Medrihan L, Tantalaki E, Aramuni G, Sargsyan V, Dudanova I, Missler M, Zhang W. 2008. Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J Neurophysiol 99:112-121.
107. Miyoshi G, Fishell G. 2012. Dynamic FoxG1 expression coordinates the integration of multipolar pyramidal neuron precursors into the cortical plate. Neuron 74:1045-1058.
108. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, et al. 2006. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26:319-327.
109. Mullaney BC, Johnston MV, Blue ME. 2004. Developmental expression of methyl-CpG binding protein 2 is dynamically regulated in the rodent brain. Neuroscience 123:939-949.
110. Na ES, Nelson ED, Adachi M, Autry AE, Mahgoub MA, Kavalali ET, Monteggia LM. 2012. A mouse model for MeCP2 duplication syndrome: MeCP2 overexpression impairs learning and memory and synaptic transmission. J Neurosci 32:3109-3117.
111. Na ES, Nelson ED, Kavalali ET, Monteggia LM. 2013. The impact of MeCP2 loss- or gain-of-function on synaptic plasticity. Neuropsychopharmacology 38:212-219.
112. Nag N, Moriuchi JM, Peitzman CG, Ward BC, Kolodny NH, Berger-Sweeney JE. 2009. Environmental enrichment alters locomotor behaviour and ventricular volume in Mecp2 1lox mice. Behav Brain Res 196:44-48.
113. Nagarajan RP, Hogart AR, Gwye Y, Martin MR, LaSalle JM. 2006. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics 1:e1-11.
114. Nagarajan RP, Patzel KA, Martin M, Yasui DH, Swanberg SE, Hertz-Picciotto I, Hansen RL, Van de Water J, et al. 2008. MECP2 promoter methylation and X chromosome inactivation in autism. Autism Res 1:169-178.
115. Nan X, Campoy FJ, Bird A. 1997. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471-481.
116. Nan X, Meehan RR, Bird A. 1993. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res 21:4886-4892.
117. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389.
118. Nan X, Tate P, Li E, Bird A. 1996. DNA methylation specifies chromosomal localization of MeCP2. Mol Cell Biol 16:414-421.
119. Nelson ED, Bal M, Kavalali ET, Monteggia LM. 2011. Selective impact of MeCP2 and associated histone deacetylases on the dynamics of evoked excitatory neurotransmission. J Neurophysiol 106:193-201.
120. Neul JL, Fang P, Barrish J, Lane J, Caeg EB, Smith EO, Zoghbi H, et al. 2008. Specific mutations in methyl-CpG-binding protein 2 confer different severity in Rett syndrome. Neurology 70:1313-1321.
121. Neul JL, Kaufmann WE, Glaze DG, Christodoulou J, Clarke AJ, Bahi-Buisson N, Leonard H, et al. 2010. Rett syndrome: revised diagnostic criteria and nomenclature. Ann Neurol 68:944-950.
122. Noutel J, Hong YK, Leu B, Kang E, Chen C. 2011. Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron 70:35-42.
123. Palmer A, Qayumi J, Ronnett G. 2008. MeCP2 mutation causes distinguishable phases of acute and chronic defects in synaptogenesis and maintenance, respectively. Mol Cell Neurosci 37:794-807.
124. Pan F, Aldridge GM, Greenough WT, Gan WB. 2010. Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome. Proc Natl Acad Sci USA 107:17768-17773.
125. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, et al. 2011. Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458.
126. Pelka GJ, Watson CM, Radziewic T, Hayward M, Lahooti H, Christodoulou J, Tam PP. 2006. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129:887-898.
127. Philippe C, Villard L, De Roux N, Raynaud M, Bonnefond JP, Pasquier L, Lesca G, et al. 2006. Spectrum and distribution of MECP2 mutations in 424 Rett syndrome patients: a molecular update. Eur J Med Genet 49:9-18.
128. Purpura DP. 1974. Dendritic spine "dysgenesis" and mental retardation. Science 186:1126-1128.
129. Qiu Z, Sylwestrak EL, Lieberman DN, Zhang Y, Liu XY, Ghosh A. 2012. The Rett syndrome protein MeCP2 regulates synaptic scaling. J Neurosci 32:989-994.
130. Rett A. 1966. [On a unusual brain atrophy syndrome in hyperammonemia in childhood]. Wien Med Wochenschr 116:723-726.
131. Ricciardi S, Boggio EM, Grosso S, Lonetti G, Forlani G, Stefanelli G, Calcagno E, et al. 2011. Reduced AKT/mTOR signaling and protein synthesis dysregulation in a Rett syndrome animal model. Hum Mol Genet 20:1182-1196.
132. Ricciardi S, Kilstrup-Nielsen C, Bienvenu T, Jacquette A, Landsberger N, Broccoli V. 2009. CDKL5 influences RNA splicing activity by its association to the nuclear speckle molecular machinery. Hum Mol Genet 18:4590-4602.
133. Ricciardi S, Ungaro F, Hambrock M, Rademacher N, Stefanelli G, Brambilla D, Sessa A, et al. 2012. CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons. Nat Cell Biol 14:911-923.
134. Robinson L, Guy J, McKay L, Brockett E, Spike RC, Selfridge J, De Sousa D, et al. 2012. Morphological and functional reversal of phenotypes in a mouse model of Rett syndrome. Brain 135:2699-2710.
135. Robinson TE, Gorny G, Mitton E, Kolb B. 2001. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39:257-266.
136. Rusconi L, Salvatoni L, Giudici L, Bertani I, Kilstrup-Nielsen C, Broccoli V, Landsberger N. 2008. CDKL5 expression is modulated during neuronal development and its subcellular distribution is tightly regulated by the C-terminal tail. J Biol Chem 283:30101-30111.
137. Samaco RC, Mandel-Brehm C, Chao HT, Ward CS, Fyffe-Maricich SL, Ren J, et al. 2009. Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc Natl Acad Sci USA 106:21966-21971.
138. Samaco RC, Mandel-Brehm C, McGraw CM, Shaw CA, McGill BE, Zoghbi HY. 2012. Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nat Genet 44:206-211.
139. Samaco RC, Nagarajan RP, Braunschweig D, LaSalle JM. 2004. Multiple pathways regulate MeCP2 expression in normal brain development and exhibit defects in autism-spectrum disorders. Hum Mol Genet 13:629-639.
140. Schmid DA, Yang T, Ogier M, Adams I, Mirakhur Y, Wang Q, Massa SM, et al. 2012. A TrkB small molecule partial agonist rescues TrkB phosphorylation deficits and improves respiratory function in a mouse model of Rett syndrome. J Neurosci 32:1803-1810.
141. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, et al. 2002. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35:243-254.
142. Shahbazian MD, Antalffy B, Armstrong DL, Zoghbi HY. 2002. Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum Mol Genet 11:115-124.
143. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, et al. 2006. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743-751.
144. Shibayama A, Cook EH Jr, Feng J, Glanzmann C, Yan J, Craddock N, Jones IR, et al. 2004. MECP2 structural and 3′-UTR variants in schizophrenia, autism and other psychiatric diseases: A possible association with autism. Am J Med Genet B Neuropsychiatr Genet 128:50-53.
145. Shors TJ, Chua C, Falduto J. 2001. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292-6297.
146. Skene PJ, Illingworth RS, Webb S, Kerr AR, James KD, Turner DJ, Andrews R, et al. 2010. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol Cell 37:457-468.
147. Smrt RD, Eaves-Egenes J, Barkho BZ, Santistevan NJ, Zhao C, Aimone JB, Gage FH, et al. 2007. Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol Dis 27:77-89.
148. Stettner GM, Huppke P, Brendel C, Richter DW, Gartner J, Dutschmann M. 2007. Breathing dysfunctions associated with impaired control of postinspiratory activity in Mecp2-/y knockout mice. J Physiol 579:863-876.
149. Swanberg SE, Nagarajan RP, Peddada S, Yasui DH, LaSalle JM. 2009. Reciprocal co-regulation of EGR2 and MECP2 is disrupted in Rett syndrome and autism. Hum Mol Genet 18:525-534.
150. Takashima S, Becker LE, Armstrong DL, Chan F. 1981. Abnormal neuronal development in the visual cortex of the human fetus and infant with down's syndrome. A quantitative and qualitative Golgi study. Brain Res 225:1-21.
151. Takashima S, Iida K, Mito T, Arima M. 1994. Dendritic and histochemical development and ageing in patients with Down's syndrome. J Intellect Disabil Res 38 (Part 3):265-273.
152. Taneja P, Ogier M, Brooks-Harris G, Schmid DA, Katz DM, Nelson SB. 2009. Pathophysiology of locus ceruleus neurons in a mouse model of Rett syndrome. J Neurosci 29:12187-12195.
153. Tao J, Hu K, Chang Q, Wu H, Sherman NE, Martinowich K, Klose RJ, et al. 2009. Phosphorylation of MeCP2 at Serine 80 regulates its chromatin association and neurological function. Proc Natl Acad Sci USA 106:4882-4887.
154. Theer P, Hasan MT, Denk W. 2003. Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier. Opt Lett 28:1022-1024.
155. Tian C, Gong Y, Yang Y, Shen W, Wang K, Liu J, Xu B, et al. 2012. Foxg1 has an essential role in postnatal development of the dentate gyrus. J Neurosci 32:2931-2949.
156. Tropea D, Giacometti E, Wilson NR, Beard C, McCurry C, Fu DD, Flannery R, et al. 2009. Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Proc Natl Acad Sci USA 106:2029-2034.
157. Tsankova N, Renthal W, Kumar A, Nestler EJ. 2007. Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8:355-367.
158. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
159. Vacca M, Filippini F, Budillon A, Rossi V, Della Ragione F, De Bonis ML, Mercadante G, et al. 2001. MECP2 gene mutation analysis in the British and Italian Rett Syndrome patients: Hot spot map of the most recurrent mutations and bioinformatic analysis of a new MECP2 conserved region. Brain Dev 23 (Suppl 1):S246-S250.
160. van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, Sommeijer JP, De Zeeuw CI, et al. 2012. Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74:374-383.
161. Wang IT, Allen M, Goffin D, Zhu X, Fairless AH, Brodkin ES, Siegel SJ, et al. 2012. Loss of CDKL5 disrupts kinome profile and event-related potentials leading to autistic-like phenotypes in mice. Proc Natl Acad Sci USA 109:21516-21521.
162. Woo J, Kwon SK, Kim E. 2009. The NGL family of leucine-rich repeat-containing synaptic adhesion molecules. Mol Cell Neurosci 42:1-10.
163. Wood L, Gray NW, Zhou Z, Greenberg ME, Shepherd GM. 2009. Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in an RNA interference model of methyl-CpG-binding protein 2 deficiency. J Neurosci 29:12440-12448.
164. Yazdani M, Deogracias R, Guy J, Poot RA, Bird A, Barde YA. 2012. Disease modeling using embryonic stem cells: MeCP2 regulates nuclear size and rna synthesis in neurons. Stem Cells 30:2128-2139.
165. Young JI, Hong EP, Castle JC, Crespo-Barreto J, Bowman AB, Rose MF, Kang D, et al. 2005. Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc Natl Acad Sci USA 102:17551-17558.
166. Zachariah RM, Rastegar M. 2012. Linking epigenetics to human disease and Rett syndrome: the emerging novel and challenging concepts in MeCP2 research. Neural Plast 2012:415825.
167. Zappella M, Meloni I, Longo I, Hayek G, Renieri A. 2001. Preserved speech variants of the Rett syndrome: molecular and clinical analysis. Am J Med Genet 104:14-22.
168. Zhang L, He J, Jugloff DG, Eubanks JH. 2008. The MeCP2-null mouse hippocampus displays altered basal inhibitory rhythms and is prone to hyperexcitability. Hippocampus 18:294-309.
169. Zhong X, Li H, Chang Q. 2012. MeCP2 Phosphorylation Is Required for Modulating Synaptic Scaling through mGluR5. J Neurosci 32:12841-12847.
170. Zhou Z, Hong EJ, Cohen S, Zhao WN, Ho HY, Schmidt L, Chen WG, et al. 2006. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52:255-269.
171. Zocchi L, Sassone-Corsi P. 2012. SIRT1-mediated deacetylation of MeCP2 contributes to BDNF expression. Epigenetics 7:695-700.