Brain-Specific Phosphorylation of MeCP2 Regulates Activity-Dependent Bdnf Transcription, Dendritic Growth, and Spine Maturation

Neuron

Volumn 52, Issue 2, 2006, Pages 255-269

  Zhou, Zhaolan ^a,b   Hong, Elizabeth J ^a,b   Cohen, Sonia ^a,b   Zhao, Wen ning ^b   Ho, Hsin yi Henry ^a,b   Schmidt, Lauren ^a   Chen, Wen G ^a,b   Lin, Yingxi ^a,b   Savner, Erin ^a   Griffith, Eric C ^a,b   Hu, Linda ^a   Steen, Judith A J ^a   Weitz, Charles J ^b   Greenberg, Michael E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

DEVBIO; HUMDISEASE; MOLNEURO

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; METHYL CPG BINDING PROTEIN 2; SERINE;

ARTICLE; BRAIN DEPTH STIMULATION; CALCIUM TRANSPORT; CELL ACTIVITY; DENDRITE; DENDRITIC SPINE; GENE EXPRESSION REGULATION; GENE MUTATION; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NEUROBIOLOGY; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETT SYNDROME; STATISTICAL SIGNIFICANCE; TRANSCRIPTION REGULATION;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CELL DIFFERENTIATION; DENDRITIC SPINES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; METHYL-CPG-BINDING PROTEIN 2; NEURAL PATHWAYS; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; ORGAN SPECIFICITY; PHOSPHORYLATION; RATS; RETT SYNDROME; SERINE; SYNAPTIC TRANSMISSION;

EID: 33749590330     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.09.037     Document Type: Article

References (54)

1. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., and Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23 (1999) 185-188
2. Ariani F., Mari F., Pescucci C., Longo I., Bruttini M., Meloni I., Hayek G., Rocchi R., Zappella M., and Renieri A. Real-time quantitative PCR as a routine method for screening large rearrangements in Rett syndrome: report of one case of MECP2 deletion and one case of MECP2 duplication. Hum. Mutat. 24 (2004) 172-177
3. Asaka Y., Jugloff D.G., Zhang L., Eubanks J.H., and Fitzsimonds R.M. Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol. Dis. 21 (2006) 217-227
4. Ballas N., Grunseich C., Lu D.D., Speh J.C., and Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121 (2005) 645-657
5. Bienvenu T., and Chelly J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7 (2006) 415-426
6. Chandler S.P., Guschin D., Landsberger N., and Wolffe A.P. The methyl-CpG binding transcriptional repressor MeCP2 stably associates with nucleosomal DNA. Biochemistry 38 (1999) 7008-7018
7. Chang B.H., Mukherji S., and Soderling T.R. Characterization of a calmodulin kinase II inhibitor protein in brain. Proc. Natl. Acad. Sci. USA 95 (1998) 10890-10895
8. Chang Q., Khare G., Dani V., Nelson S., and Jaenisch R. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49 (2006) 341-348
9. Chen R.Z., Akbarian S., Tudor M., and Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27 (2001) 327-331
10. Chen W.G., Chang Q., Lin Y., Meissner A., West A.E., Griffith E.C., Jaenisch R., and Greenberg M.E. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302 (2003) 885-889
11. Collins A.L., Levenson J.M., Vilaythong A.P., Richman R., Armstrong D.L., Noebels J.L., David Sweatt J., and Zoghbi H.Y. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 13 (2004) 2679-2689
12. Dani V.S., Chang Q., Maffei A., Turrigiano G.G., Jaenisch R., and Nelson S.B. 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 (2005) 12560-12565
13. Gaudilliere B., Konishi Y., de la Iglesia N., Yao G., and Bonni A. A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41 (2004) 229-241
14. Gorski J.A., Zeiler S.R., Tamowski S., and Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J. Neurosci. 23 (2003) 6856-6865
15. Guy J., Hendrich B., Holmes M., Martin J.E., and Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27 (2001) 322-326
16. Hagberg B., Aicardi J., Dias K., and Ramos O. A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases. Ann. Neurol. 14 (1983) 471-479
17. Hardingham G.E., Fukunaga Y., and Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5 (2002) 405-414
18. Hong E.J., West A.E., and Greenberg M.E. Transcriptional control of cognitive development. Curr. Opin. Neurobiol. 15 (2005) 21-28
19. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996) 1133-1138
20. Kishi N., and 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 (2004) 306-321
21. Klose R.J., and Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31 (2006) 89-97
22. Kornhauser J.M., Mayo K.E., and Takahashi J.S. Light, immediate-early genes, and circadian rhythms. Behav. Genet. 26 (1996) 221-240
23. Kornhauser J.M., Cowan C.W., Shaywitz A.J., Dolmetsch R.E., Griffith E.C., Hu L.S., Haddad C., Xia Z., and Greenberg M.E. CREB transcriptional activity in neurons is regulated by multiple, calcium-specific phosphorylation events. Neuron 34 (2002) 221-233
24. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., and Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92 (1995) 8856-8860
25. Kriaucionis S., and Bird A. DNA methylation and Rett syndrome. Hum. Mol. Genet. 12 Spec. No. 2 (2003) R221-R227
26. Lanahan A., and Worley P. Immediate-early genes and synaptic function. Neurobiol. Learn. Mem. 70 (1998) 37-43
27. Lewis J.D., Meehan R.R., Henzel W.J., Maurer-Fogy I., Jeppesen P., Klein F., and Bird A. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69 (1992) 905-914
28. Lisman J., Schulman H., and Cline H. The molecular basis of CaMKII function in synaptic and behavioral memory. Nat. Rev. Neurosci. 3 (2002) 175-190
29. Lois C., Hong E.J., Pease S., Brown E.J., and Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295 (2002) 868-872
30. Lom B., and Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19 (1999) 9928-9938
31. Lugtenberg D., de Brouwer A.P., Kleefstra T., Oudakker A.R., Frints S.G., Schrander-Stumpel C.T., Fryns J.P., Jensen L.R., Chelly J., Moraine C., et al. Chromosomal copy number changes in patients with nonsyndromic X linked mental retardation detected by array CGH. J. Med. Genet. 43 (2006) 362-370
32. Luikenhuis S., Giacometti E., Beard C.F., and Jaenisch R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc. Natl. Acad. Sci. USA 101 (2004) 6033-6038
33. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., Fan G., and Sun Y.E. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302 (2003) 890-893
34. McAllister A.K., Lo D.C., and Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15 (1995) 791-803
35. Meins M., Lehmann J., Gerresheim F., Herchenbach J., Hagedorn M., Hameister K., and Epplen J.T. Submicroscopic duplication in Xq28 causes increased expression of the MECP2 gene in a boy with severe mental retardation and features of Rett syndrome. J. Med. Genet. 42 (2005) e12
36. Moretti P., and Zoghbi H.Y. MeCP2 dysfunction in Rett syndrome and related disorders. Curr. Opin. Genet. Dev. 16 (2006) 276-281
37. Moretti P., Bouwknecht J.A., Teague R., Paylor R., and Zoghbi H.Y. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum. Mol. Genet. 14 (2005) 205-220
38. Moretti P., Levenson J.M., Battaglia F., Atkinson R., Teague R., Antalffy B., Armstrong D., Arancio O., Sweatt J.D., and Zoghbi H.Y. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 26 (2006) 319-327
39. Nelson E.D., Kavalali E.T., and Monteggia L.M. MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr. Biol. 16 (2006) 710-716
40. Nimchinsky E.A., Sabatini B.L., and Svoboda K. Structure and function of dendritic spines. Annu. Rev. Physiol. 64 (2002) 313-353
41. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., and Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16 (1996) 1137-1145
42. Pelka G.J., Watson C.M., Radziewic T., Hayward M., Lahooti H., Christodoulou J., and Tam P.P. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129 (2006) 887-898
43. Poo M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2 (2001) 24-32
44. Redmond L., Kashani A.H., and Ghosh A. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34 (2002) 999-1010
45. Reppert S.M., and Weaver D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63 (2001) 647-676
46. Rett A. On a unusual brain atrophy syndrome in hyperammonemia in childhood. Wien. Med. Wochenschr. 116 (1966) 723-726
47. Shahbazian M., Young J., Yuva-Paylor L., Spencer C., Antalffy B., Noebels J., Armstrong D., Paylor R., and Zoghbi H. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35 (2002) 243-254
48. Shen K., Teruel M.N., Subramanian K., and Meyer T. CaMKIIβ functions as an F-actin targeting module that localizes CaMKIIα/β heterooligomers to dendritic spines. Neuron 21 (1998) 593-606
49. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37 (1991) 173-182
50. Van Esch H., Bauters M., Ignatius J., Jansen M., Raynaud M., Hollanders K., Lugtenberg D., Bienvenu T., Jensen L.R., Gecz J., et al. Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Am. J. Hum. Genet. 77 (2005) 442-453
51. Wayman G.A., Impey S., Marks D., Saneyoshi T., Grant W.F., Derkach V., and Soderling T.R. Activity-dependent dendritic arborization mediated by CaM-Kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50 (2006) 897-909
52. West A.E., Griffith E.C., and Greenberg M.E. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3 (2002) 921-931
53. Xia Z., Dudek H., Miranti C.K., and Greenberg M.E. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16 (1996) 5425-5436
54. Zoghbi H.Y. Postnatal neurodevelopmental disorders: meeting at the synapse?. Science 302 (2003) 826-830