Nuclear calcium signaling controls methyl-CpG-binding protein 2 (MeCP2) phosphorylation on serine 421 following synaptic activity

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 30967-30974

  Buchthal, Bettina ^a   Lau, David ^a   Weiss, Ursula ^a   Weislogel, Jan Marek ^a,b   Bading, Hilmar ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM SIGNALING; CAMP-RESPONSE ELEMENT-BINDING PROTEINS; CELL NUCLEUS; CYTOSOLS; HIPPOCAMPAL NEURONS; IMMUNOLOCALIZATION; ISOFORMS; METHYL-CPG-BINDING; PHARMACOLOGICAL INHIBITION; SUBCELLULAR FRACTIONATION; TARGET GENES;

AMINO ACIDS; CAMS; ENZYMES; GENES; NEURONS; PHOSPHORYLATION; TRANSCRIPTION;

CALMODULIN;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II BETA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II DELTA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II GAMMA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOSOL RECEPTOR; ISOPROTEIN; METHYL CPG BINDING PROTEIN 2; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CATALYSIS; CELL FRACTIONATION; CELL NUCLEUS; CHROMATIN; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SYNAPSE; TRANSCRIPTION REGULATION;

ANIMALS; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CELL NUCLEUS; CELLS, CULTURED; CREB-BINDING PROTEIN; HIPPOCAMPUS; METHYL-CPG-BINDING PROTEIN 2; MICE; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; SERINE; SYNAPSES; TRANSCRIPTION, GENETIC;

EID: 84866092403     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.382507     Document Type: Article

References (48)

1. Hendrich, B., and Bird, A. (1998) Identification and characterization of a family of mammalian methyl-CpG-binding proteins. Mol. Cell Biol. 18, 6538-6547
2. Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P., and Kouzarides, T. (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035-4040
3. Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T., Qin, J., and Zoghbi, H. Y. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229
4. Chen, W. G., Chang, Q., Lin, Y., Meissner, A., West, A. E., Griffith, E. C., Jaenisch, R., and Greenberg, M. E. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302, 885-889
5. Shahbazian, M. D., Antalffy, B., Armstrong, D. L., and Zoghbi, H. Y. (2002) Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 11, 115-124
6. Alvarez-Saavedra, M., Carrasco, L., Sura-Trueba, S., Demarchi Aiello, V., Walz, K., Neto, J. X., and Young, J. I. (2010) Elevated expression of MeCP2 in cardiac and skeletal tissues is detrimental for normal development. Hum. Mol. Genet. 19, 2177-2190
7. Guy, J., Cheval, H., Selfridge, J., and Bird, A. (2011) The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol. 27, 631-652
8. Zhou, Z., Hong, E. J., Cohen, S., Zhao, W. N., Ho, H. Y., Schmidt, L., Chen, W. G., Lin, Y., Savner, E., Griffith, E. C., Hu, L., Steen, J. A., Weitz, C. J., and Greenberg, M. E. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269
9. Cohen, S., Gabel, H. W., Hemberg, M., Hutchinson, A. N., Sadacca, L. A., Ebert, D. H., Harmin, D. A., Greenberg, R. S., Verdine, V. K., Zhou, Z., Wetsel, W. C., West, A. E., and Greenberg, M. E. (2011) Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function. Neuron 72, 72-85
10. Skene, P. J., Illingworth, R. S., Webb, S., Kerr, A. R., James, K. D., Turner, D. J., Andrews, R., and Bird, A. P. (2010) Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457-468
11. Gonzales, M. L., and LaSalle, J. M. (2010) The role of MeCP2 in brain development and neurodevelopmental disorders. Curr. Psychiatry Rep. 12, 127-134
12. Hagberg, B., Aicardi, J., Dias, K., and Ramos, O. (1983) A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett syndrome: report of 35 cases. Ann. Neurol 14, 471-479
13. Bienvenu, T., and Chelly, J. (2006) Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7, 415-426
14. Chahrour, M., and Zoghbi, H. Y. (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422-437
15. Chen, R. Z., Akbarian, S., Tudor, M., and 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
16. West, A. E., and Greenberg, M. E. (2011) Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 3, a005744
17. Li, H., Zhong, X., Chau, K. F., Williams, E. C., and Chang, Q. (2011) Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP, and spatial memory. Nat. Neurosci. 14, 1001-1008
18. Zhang, S. J., Steijaert, M. N., Lau, D., Schütz, G., Delucinge-Vivier, C., Descombes, P., and Bading, H. (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53, 549-562
19. Zhang, S. J., Zou, M., Lu, L., Lau, D., Ditzel, D. A., Delucinge-Vivier, C., Aso, Y., Descombes, P., and Bading, H. (2009) Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet. 5, e1000604
20. Hardingham, G. E., Chawla, S., Johnson, C. M., and Bading, H. (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260-265
21. Limbäck-Stokin, K., Korzus, E., Nagaoka-Yasuda, R., and Mayford, M. (2004) Nuclear calcium/calmodulin regulates memory consolidation. J. Neurosci. 24, 10858-10867
22. Zhang, S. J., Buchthal, B., Lau, D., Hayer, S., Dick, O., Schwaninger, M., Veltkamp, R., Zou, M., Weiss, U., and Bading, H. (2011) A signaling cascade of nuclear calcium-CREB-ATF3 activated by synaptic NMDA receptors defines a gene repression module that protects against extrasynaptic NMDAreceptor-induced neuronal cell death and ischemic brain damage. J. Neurosci. 31, 4978-4990
23. Mauceri, D., Freitag, H. E., Oliveira, A. M., Bengtson, C. P., and Bading, H. (2011) Nuclear calcium-VEGFD signaling controls maintenance of dendrite arborization necessary for memory formation. Neuron 71, 117-130
24. Hardingham, G. E., and Bading, H. (2010) Synaptic versus extrasynaptic NMDA receptor signaling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696
25. Bading, H., and Greenberg, M. E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912-914
26. Bading, H., Ginty, D. D., and Greenberg, M. E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186
27. Bading, H., Segal, M. M., Sucher, N. J., Dudek, H., Lipton, S. A., and Greenberg, M. E. (1995) N-Methyl-D-aspartate receptors are critical for mediating the effects of glutamate on intracellular calcium concentration and immediate early gene expression in cultured hippocampal neurons. Neuroscience 64, 653-664
28. Kairisalo, M., Korhonen, L., Sepp, M., Pruunsild, P., Kukkonen, J. P., Kivinen, J., Timmusk, T., Blomgren, K., and Lindholm, D. (2009) NF-κB-dependent regulation of brain-derived neurotrophic factor in hippocampal neurons by X-linked inhibitor of apoptosis protein. Eur. J. Neurosci. 30, 958-966
29. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450
30. Wang, J., Campos, B., Jamieson, G. A., Jr., Kaetzel, M. A., and Dedman, J. R. (1995) Functional elimination of calmodulin within the nucleus by targeted expression of an inhibitor peptide. J. Biol. Chem. 270, 30245-30248
31. Hardingham, G. E., Arnold, F. J., and Bading, H. (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4, 261-267
32. Arnold, F. J., Hofmann, F., Bengtson, C. P., Wittmann, M., Vanhoutte, P., and Bading, H. (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity. J. Physiol. 564, 3-19
33. Hardingham, G. E., Arnold, F. J., and Bading, H. (2001) A calcium microdomain near NMDA receptors: on switch for ERK-dependent syn- apse-to-nucleus communication. Nat. Neurosci. 4, 565-566
34. 2+ channels. Neuropharmacology 34, 731-741
35. Gao, L., Blair, L. A., and Marshall, J. (2006) CaMKII-independent effects of KN93 and its inactive analog KN92: reversible inhibition of L-type calcium channels. Biochem. Biophys. Res. Commun. 345, 1606-1610
36. Vanhoutte, P., Barnier, J. V., Guibert, B., Pagès, C., Besson, M. J., Hipskind, R. A., and Caboche, J. (1999) Glutamate induces phosphorylation of Elk-1 and CREB, along with c-fos activation, via an extracellular signal-regulated kinase-dependent pathway in brain slices. Mol. Cell Biol. 19, 136-146
37. Chow, F. A., Anderson, K. A., Noeldner, P. K., and Means, A. R. (2005) The autonomous activity of calcium/calmodulin-dependent protein kinase IV is required for its role in transcription. J. Biol. Chem. 280, 20530-20538
38. Mishra, S., Gray, C. B., Miyamoto, S., Bers, D. M., and Brown, J. H. (2011) Location matters: clarifying the concept of nuclear and cytosolic CaMKII subtypes. Circ. Res. 109, 1354-1362
39. Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., Chang, S., Ling, H., Bers, D. M., Maier, L. S., Olson, E. N., and Brown, J. H. (2007) CaMKIIδ isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J. Biol. Chem. 282, 35078-35087
40. 2+/calmodulin-dependent protein kinase II in rat cerebellar granule cells. J. Neurochem. 72, 815-825
41. 2+/calmodulin-dependent protein kinase II in rat astrocytes and their subcellular localization. J. Neurochem. 74, 2557-2567
42. Chawla, S., Hardingham, G. E., Quinn, D. R., and Bading, H. (1998) CBP: a signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science 281, 1505-1509
43. Chawla, S., Vanhoutte, P., Arnold, F. J., Huang, C. L., Bading, H. (2003) Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem. 85, 151-159
44. Miller, C. A., and Sweatt, J. D. (2007) Covalent modification of DNA regulates memory formation. Neuron 53, 857-869
45. Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M. H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., Zhang, K., Ming, G. L., Gao, Y., and Song, H. (2011) Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 14, 1345-1351
46. Oliveira, A. M., Hemstedt, T. J., and Bading, H. (2012) Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nat. Neurosci. 15, 1111-1113
47. Smrt, R. D., Eaves-Egenes, J., Barkho, B. Z., Santistevan, N. J., Zhao, C., Aimone, J. B., Gage, F. H., and Zhao, X. (2007) Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol. Dis. 27, 77-89
48. Deng, J. V., Rodriguiz, R. M., Hutchinson, A. N., Kim, I. H., Wetsel, W. C., and West, A. E. (2010) MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat. Neurosci. 13, 1128-1136