Rett syndrome mutation MeCP2 T158A disrupts DNA binding, protein stability and ERP responses

Nature Neuroscience

Volumn 15, Issue 2, 2012, Pages 274-283

  Goffin, Darren ^a   Allen, Megan ^a   Zhang, Le ^a   Amorim, Maria ^a   Wang, I Ting Judy ^a   Reyes, Arith Ruth S ^a   Mercado Berton, Amy ^a   Ong, Caroline ^b   Cohen, Sonia ^b   Hu, Linda ^b   Blendy, Julie A ^a   Carlson, Gregory C ^a   Siegel, Steve J ^a   Greenberg, Michael E ^b   Zhou, Zhaolan ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; METHIONINE; METHYL CPG BINDING PROTEIN 2;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DNA BINDING; DNA METHYLATION; EVENT RELATED POTENTIAL; GENE MUTATION; LEARNING DISORDER; MOTOR DYSFUNCTION; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STABILITY; RETT SYNDROME;

ACOUSTIC STIMULATION; AGE FACTORS; ALANINE; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; CHROMATIN IMMUNOPRECIPITATION; CONDITIONING (PSYCHOLOGY); DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; ELECTROENCEPHALOGRAPHY; EMBRYO, MAMMALIAN; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; EXPLORATORY BEHAVIOR; FEAR; GENE EXPRESSION REGULATION; HUMANS; MAZE LEARNING; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; NEURONS; SPECTRUM ANALYSIS; THREONINE;

EID: 84856270235     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2997     Document Type: Article

References (49)

1. Amir, R.E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23, 185-188 (1999). (Pubitemid 29455390)
2. Bienvenu, T. & Chelly, J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7, 415-426 (2006). (Pubitemid 43780485)
3. Chahrour, M. & Zoghbi, H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422-437 (2007). (Pubitemid 350026269)
4. Chen, R.Z., Akbarian, S., Tudor, M. & Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27, 327-331 (2001). (Pubitemid 32201857)
5. Guy, J., Hendrich, B., Holmes, M., Martin, J.E. & Bird, A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27, 322-326 (2001). (Pubitemid 32201856)
6. Shahbazian, M. et al. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35, 243-254 (2002). (Pubitemid 34876728)
7. Collins, A.L. et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 13, 2679-2689 (2004). (Pubitemid 39485416)
8. Pelka, G.J. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129, 887-898 (2006).
9. Kerr, B., Alvarez-Saavedra, M., Sáez, M.A., Saona, A. & Young, J.I. Defective body-weight regulation, motor control and abnormal social interactions in Mecp2 hypomorphic mice. Hum. Mol. Genet. 17, 1707-1717 (2008). (Pubitemid 351791497)
10. Samaco, R.C. et al. A partial loss of function allele of methyl-CpG-binding protein 2 predicts a human neurodevelopmental syndrome. Hum. Mol. Genet. 17, 1718-1727 (2008). (Pubitemid 351791498)
11. Jentarra, G.M. et al. Abnormalities of cell packing density and dendritic complexity in the MeCP2 A140V mouse model of Rett syndrome/X-linked mental retardation. BMC Neurosci. 11, 19 (2010).
12. Guy, J., Gan, J., Selfridge, J., Cobb, S. & Bird, A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143-1147 (2007). (Pubitemid 46328028)
13. Lioy, D.T. et al. A role for glia in the progression of Rett's syndrome. Nature 475, 497-500 (2011).
14. Ho, K.L. et al. MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol. Cell 29, 525-531 (2008). (Pubitemid 351282541)
15. Dani, V.S. et al. 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 (2005). (Pubitemid 41266398)
16. Dani, V.S. & Nelson, S.B. Intact long-term potentiation but reduced connectivity between neocortical layer 5 pyramidal neurons in a mouse model of Rett syndrome. J. Neurosci. 29, 11263-11270 (2009).
17. Wood, L., Gray, N.W., Zhou, Z., Greenberg, M.E. & Shepherd, G.M.G. 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 (2009).
18. Uhlhaas, P.J. & Singer, W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11, 100-113 (2010).
19. Gandal, M.J., Edgar, J.C., Klook, K. & Siegel, S.J. Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology (2011).
20. Roberts, T.P.L. et al. MEG detection of delayed auditory evoked responses in autism spectrum disorders: towards an imaging biomarker for autism. Autism Res. 3, 8-18 (2010).
21. Gandal, M.J. et al. Validating γ oscillations and delayed auditory responses as translational biomarkers of autism. Biol. Psychiatry 68, 1100-1106 (2010).
22. Chao, H.-T. et al. Dysfunction in GABA signaling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263-269 (2010).
23. D'Cruz, J.A. et al. Alterations of cortical and hippocampal EEG activity in MeCP2-deficient mice. Neurobiol. Dis. 38, 8-16 (2010).
24. Bader, G.G., Witt-Engerström, I. & Hagberg, B. Neurophysiological findings in the Rett syndrome. II. Visual and auditory brainstem, middle and late evoked responses. Brain Dev. 11, 110-114 (1989). (Pubitemid 19106473)
25. Stauder, J.E.A., Smeets, E.E.J., van Mil, S.G.M. & Curfs, L.G.M. The development of visual-and auditory processing in Rett syndrome: an ERP study. Brain Dev. 28, 487-494 (2006). (Pubitemid 44051823)
26. Vacca, M. et al. 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 (2001).
27. Schanen, C. et al. Phenotypic manifestations of MECP2 mutations in classical and atypical Rett syndrome. Am. J. Med. Genet. A. 126A, 129-140 (2004). (Pubitemid 38445468)
28. Armstrong, D.D. Neuropathology of Rett syndrome. J. Child Neurol. 20, 747-753 (2005). (Pubitemid 41498709)
29. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).
30. Shahbazian, M.D., Antalffy, B., Armstrong, D.L. & Zoghbi, H.Y. Insight into Rett syndrome: MeCP2 levels display tissue-and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 11, 115-124 (2002). (Pubitemid 34157003)
31. Skene, P.J. et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457-468 (2010).
32. Chahrour, M. et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229 (2008). (Pubitemid 351929512)
33. Nan, X., Tate, P., Li, E. & Bird, A. DNA methylation specifies chromosomal localization of MeCP2. Mol. Cell. Biol. 16, 414-421 (1996). (Pubitemid 126506989)
34. Nuber, U.A. et al. Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum. Mol. Genet. 14, 2247-2256 (2005). (Pubitemid 41418024)
35. Jones, P.L. et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187-191 (1998). (Pubitemid 28248804)
36. Nan, X. et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389 (1998). (Pubitemid 28269714)
37. Uhlhaas, P.J., Pipa, G., Neuenschwander, S., Wibral, M. & Singer, W. A new look at gamma? High-(60 Hz) γ-band activity in cortical networks: function, mechanisms and impairment. Prog. Biophys. Mol. Biol. 105, 14-28 (2011).
38. Tallon-Baudry, C. & Bertrand, O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3, 151-162 (1999). (Pubitemid 29155465)
39. Buzsáki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926-1929 (2004).
40. Winterer, G. et al. Schizophrenia: reduced signal-to-noise ratio and impaired phase-locking during information processing. Clin. Neurophysiol. 111, 837-849 (2000). (Pubitemid 30236430)
41. Foster, B.A., Coffey, H.A., Morin, M.J. & Rastinejad, F. Pharmacological rescue of mutant p53 conformation and function. Science 286, 2507-2510 (1999).
42. Kishi, N. & Macklis, J.D. 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 (2004). (Pubitemid 39433843)
43. Uhlhaas, P.J. & Singer, W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155-168 (2006). (Pubitemid 44466360)
44. Ben-Ari, Y. Developing networks play a similar melody. Trends Neurosci. 24, 353-360 (2001). (Pubitemid 32455437)
45. Goffin, D. et al. Dopamine-dependent tuning of striatal inhibitory synaptogenesis. J. Neurosci. 30, 2935-2950 (2010).
46. Zhou, Z. et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269 (2006). (Pubitemid 44548348)
47. Liao, W.-L. et al. Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc. Natl. Acad. Sci. USA 105, 6765-6770 (2008). (Pubitemid 351754581)
48. Canolty, R.T. et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626-1628 (2006). (Pubitemid 44414034)
49. Hardisty-Hughes, R.E., Parker, A. & Brown, S.D.M. A hearing and vestibular phenotyping pipeline to identify mouse mutants with hearing impairment. Nat. Protoc. 5, 177-190 (2010).