Global transcriptional and translational repression in human-embryonic- stem-cell-derived rett syndrome neurons

Cell Stem Cell

Volumn 13, Issue 4, 2013, Pages 446-458

  Li, Yun ^a   Wang, Haoyi ^a   Muffat, Julien ^a   Cheng, Albert W ^a,b   Orlando, David A ^a   Lovén, Jakob ^a   Kwok, Show Ming ^b   Feldman, Danielle A ^b   Bateup, Helen S ^c   Gao, Qing ^a   Hockemeyer, Dirk ^a   Mitalipova, Maisam ^a   Lewis, Caroline A ^b   Vander Heiden, Matthew G ^b   Sur, Mriganka ^b   Young, Richard A ^a,b   Jaenisch, Rudolf ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALRETININ; DOUBLECORTIN; GLUTAMATE DECARBOXYLASE 67; GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN S6; REELIN; RIBOSOME RNA; SYNAPSIN; TETRODOTOXIN; TRANSCRIPTOME; TRANSFER RNA; VESICULAR GLUTAMATE TRANSPORTER 1; MECP2 PROTEIN, HUMAN;

ALLELE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EXON; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENETIC TRANSCRIPTION; HAPTEN CARRIER COMPLEX; HUMAN; HUMAN CELL; NERVE CELL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RETT SYNDROME; RNA TRANSLATION; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING; CELL CULTURE; GENETICS; METABOLISM; MUTATION; PATHOLOGY;

CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; METHYL-CPG-BINDING PROTEIN 2; MUTATION; NEURONS; PROTEIN BIOSYNTHESIS; RETT SYNDROME; TRANSCRIPTION, GENETIC;

EID: 84885107449     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.09.001     Document Type: Article

References (59)

1. S. Akbarian Diseases of the mind and brain: Rett's syndrome Am. J. Psychiatry 159 2002 1103
2. R.E. Amir, I.B. Van den Veyver, M. Wan, C.Q. Tran, U. Francke, and H.Y. Zoghbi Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2 Nat. Genet. 23 1999 185 188
3. G. Ananiev, E.C. Williams, H. Li, and Q. Chang Isogenic pairs of wild type and mutant induced pluripotent stem cell (iPSC) lines from Rett syndrome patients as in vitro disease model PLoS ONE 6 2011 e25255
4. M.C. Anguera, R. Sadreyev, Z. Zhang, A. Szanto, B. Payer, S.D. Sheridan, S. Kwok, S.J. Haggarty, M. Sur, and J. Alvarez Molecular signatures of human induced pluripotent stem cells highlight sex differences and cancer genes Cell Stem Cell 11 2012 75 90
5. H.S. Bateup, C.A. Johnson, C.L. Denefrio, J.L. Saulnier, K. Kornacker, and B.L. Sabatini Excitatory/inhibitory synaptic imbalance leads to hippocampal hyperexcitability in mouse models of tuberous sclerosis Neuron 78 2013 510 522
6. S. Ben-Shachar, M. Chahrour, C. Thaller, C.A. Shaw, and H.Y. Zoghbi Mouse models of MeCP2 disorders share gene expression changes in the cerebellum and hypothalamus Hum. Mol. Genet. 18 2009 2431 2442
7. J.D. Cahoy, B. Emery, A. Kaushal, L.C. Foo, J.L. Zamanian, K.S. Christopherson, Y. Xing, J.L. Lubischer, P.A. Krieg, and S.A. Krupenko A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function J. Neurosci. 28 2008 264 278
8. M. Chahrour, S.Y. Jung, C. Shaw, X. Zhou, S.T. Wong, J. Qin, and H.Y. Zoghbi MeCP2, a key contributor to neurological disease, activates and represses transcription Science 320 2008 1224 1229
9. S.M. Chambers, C.A. Fasano, E.P. Papapetrou, M. Tomishima, M. Sadelain, and L. Studer Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling Nat. Biotechnol. 27 2009 275 280
10. Q. Chang, G. Khare, V. Dani, S. Nelson, and R. Jaenisch The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression Neuron 49 2006 341 348
11. H.T. Chao, H. Chen, R.C. Samaco, M. Xue, M. Chahrour, J. Yoo, J.L. Neul, S. Gong, H.C. Lu, and N. Heintz Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes Nature 468 2010 263 269
12. R.Z. Chen, S. Akbarian, M. Tudor, and R. Jaenisch Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice Nat. Genet. 27 2001 327 331
13. A.Y. Cheung, L.M. Horvath, D. Grafodatskaya, P. Pasceri, R. Weksberg, A. Hotta, L. Carrel, and J. Ellis Isolation of MECP2-null Rett Syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation Hum. Mol. Genet. 20 2011 2103 2115
14. M.E. Cornford, M. Philippart, B. Jacobs, A.B. Scheibel, and H.V. Vinters Neuropathology of Rett syndrome: case report with neuronal and mitochondrial abnormalities in the brain J. Child Neurol. 9 1994 424 431
15. D.H. Ebert, H.W. Gabel, N.D. Robinson, N.R. Kastan, L.S. Hu, S. Cohen, A.J. Navarro, M.J. Lyst, R. Ekiert, A.P. Bird, and M.E. Greenberg Activity-dependent phosphorylation of MeCP2 threonine 308 regulates interaction with NCoR Nature 499 2013 341 345
16. E. Giacometti, S. Luikenhuis, C. Beard, and R. Jaenisch Partial rescue of MeCP2 deficiency by postnatal activation of MeCP2 Proc. Natl. Acad. Sci. USA 104 2007 1931 1936
17. J. Guy, B. Hendrich, M. Holmes, J.E. Martin, and A. Bird A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome Nat. Genet. 27 2001 322 326
18. J. Guy, J. Gan, J. Selfridge, S. Cobb, and A. Bird Reversal of neurological defects in a mouse model of Rett syndrome Science 315 2007 1143 1147
19. D. Hockemeyer, H. Wang, S. Kiani, C.S. Lai, Q. Gao, J.P. Cassady, G.J. Cost, L. Zhang, Y. Santiago, and J.C. Miller Genetic engineering of human pluripotent cells using TALE nucleases Nat. Biotechnol. 29 2011 731 734
20. C. Jordan, H.H. Li, H.C. Kwan, and U. Francke Cerebellar gene expression profiles of mouse models for Rett syndrome reveal novel MeCP2 targets BMC Med. Genet. 8 2007 36
21. D.D. Kline, M. Ogier, D.L. Kunze, and D.M. Katz Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice J. Neurosci. 30 2010 5303 5310
22. S. Kriaucionis, A. Paterson, J. Curtis, J. Guy, N. Macleod, and A. Bird Gene expression analysis exposes mitochondrial abnormalities in a mouse model of Rett syndrome Mol. Cell. Biol. 26 2006 5033 5042
23. M. Kron, C.J. Howell, I.T. Adams, M. Ransbottom, D. Christian, M. Ogier, and D.M. Katz 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 2012 13860 13872
24. S. Kügler, E. Kilic, and M. Bähr Human synapsin 1 gene promoter confers highly neuron-specific long-term transgene expression from an adenoviral vector in the adult rat brain depending on the transduced area Gene Ther. 10 2003 337 347
25. C.H. Kwon, B.W. Luikart, C.M. Powell, J. Zhou, S.A. Matheny, W. Zhang, Y. Li, S.J. Baker, and L.F. Parada Pten regulates neuronal arborization and social interaction in mice Neuron 50 2006 377 388
26. C.J. Lengner, A.A. Gimelbrant, J.A. Erwin, A.W. Cheng, M.G. Guenther, G.G. Welstead, R. Alagappan, G.M. Frampton, P. Xu, and J. Muffat Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations Cell 141 2010 872 883
27. Y. Li, B.W. Luikart, S. Birnbaum, J. Chen, C.H. Kwon, S.G. Kernie, R. Bassel-Duby, and L.F. Parada TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment Neuron 59 2008 399 412
28. Y. Li, D. Yui, B.W. Luikart, R.M. McKay, Y. Li, J.L. Rubenstein, and L.F. Parada Conditional ablation of brain-derived neurotrophic factor-TrkB signaling impairs striatal neuron development Proc. Natl. Acad. Sci. USA 109 2012 15491 15496
29. C.Y. Lin, J. Lovén, P.B. Rahl, R.M. Paranal, C.B. Burge, J.E. Bradner, T.I. Lee, and R.A. Young Transcriptional amplification in tumor cells with elevated c-Myc Cell 151 2012 56 67
30. J. Lovén, D.A. Orlando, A.A. Sigova, C.Y. Lin, P.B. Rahl, C.B. Burge, D.L. Levens, T.I. Lee, and R.A. Young Revisiting global gene expression analysis Cell 151 2012 476 482
31. B.W. Luikart, E. Schnell, E.K. Washburn, A.L. Bensen, K.R. Tovar, and G.L. Westbrook Pten knockdown in vivo increases excitatory drive onto dentate granule cells J. Neurosci. 31 2011 4345 4354
32. M.J. Lyst, R. Ekiert, D.H. Ebert, C. Merusi, J. Nowak, J. Selfridge, J. Guy, N.R. Kastan, N.D. Robinson, and F. de Lima Alves Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor Nat. Neurosci. 16 2013 898 902
33. M.C. Marchetto, C. Carromeu, A. Acab, D. Yu, G.W. Yeo, Y. Mu, G. Chen, F.H. Gage, and A.R. Muotri A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells Cell 143 2010 527 539
34. S. Mekhoubad, C. Bock, A.S. de Boer, E. Kiskinis, A. Meissner, and K. Eggan Erosion of dosage compensation impacts human iPSC disease modeling Cell Stem Cell 10 2012 595 609
35. M. Mellén, P. Ayata, S. Dewell, S. Kriaucionis, and N. Heintz MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system Cell 151 2012 1417 1430
36. X. Nan, F.J. Campoy, and A. Bird MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin Cell 88 1997 471 481
37. U.A. Nuber, S. Kriaucionis, T.C. Roloff, J. Guy, J. Selfridge, C. Steinhoff, R. Schulz, B. Lipkowitz, H.H. Ropers, M.C. Holmes, and A. Bird Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome Hum. Mol. Genet. 14 2005 2247 2256
38. D.J. Pagliarini, S.E. Calvo, B. Chang, S.A. Sheth, S.B. Vafai, S.E. Ong, G.A. Walford, C. Sugiana, A. Boneh, and W.K. Chen A mitochondrial protein compendium elucidates complex I disease biology Cell 134 2008 112 123
39. M. Pirooznia, T. Wang, D. Avramopoulos, D. Valle, G. Thomas, R.L. Huganir, F.S. Goes, J.B. Potash, and P.P. Zandi SynaptomeDB: an ontology-based knowledgebase for synaptic genes Bioinformatics 28 2012 897 899
40. S. Ricciardi, E.M. Boggio, S. Grosso, G. Lonetti, G. Forlani, G. Stefanelli, E. Calcagno, N. Morello, N. Landsberger, and S. Biffo Reduced AKT/mTOR signaling and protein synthesis dysregulation in a Rett syndrome animal model Hum. Mol. Genet. 20 2011 1182 1196
41. I. Sansal, and W.R. Sellers The biology and clinical relevance of the PTEN tumor suppressor pathway J. Clin. Oncol. 22 2004 2954 2963
42. E. Scala, I. Longo, F. Ottimo, C. Speciale, K. Sampieri, E. Katzaki, R. Artuso, M.A. Mencarelli, T. D'Ambrogio, and G. Vonella MECP2 deletions and genotype-phenotype correlation in Rett syndrome Am. J. Med. Genet. A. 143A 2007 2775 2784
43. P.J. Skene, R.S. Illingworth, S. Webb, A.R. Kerr, K.D. James, D.J. Turner, R. Andrews, and A.P. Bird Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state Mol. Cell 37 2010 457 468
44. F. Soldner, and R. Jaenisch Medicine. iPSC disease modeling Science 338 2012 1155 1156
45. F. Soldner, D. Hockemeyer, C. Beard, Q. Gao, G.W. Bell, E.G. Cook, G. Hargus, A. Blak, O. Cooper, and M. Mitalipova Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors Cell 136 2009 964 977
46. F. Soldner, J. Laganière, A.W. Cheng, D. Hockemeyer, Q. Gao, R. Alagappan, V. Khurana, L.I. Golbe, R.H. Myers, and S. Lindquist Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations Cell 146 2011 318 331
47. D. Su, Y.M. Cha, and A.E. West Mutation of MeCP2 alters transcriptional regulation of select immediate-early genes Epigenetics 7 2012 146 154
48. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
49. C.C. Thoreen, L. Chantranupong, H.R. Keys, T. Wang, N.S. Gray, and D.M. Sabatini A unifying model for mTORC1-mediated regulation of mRNA translation Nature 485 2012 109 113
50. D. Tropea, E. Giacometti, N.R. Wilson, C. Beard, C. McCurry, D.D. Fu, R. Flannery, R. Jaenisch, and M. Sur Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice Proc. Natl. Acad. Sci. USA 106 2009 2029 2034
51. M. Tudor, S. Akbarian, R.Z. Chen, and R. Jaenisch Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain Proc. Natl. Acad. Sci. USA 99 2002 15536 15541
52. J.W. Tullai, M.E. Schaffer, S. Mullenbrock, G. Sholder, S. Kasif, and G.M. Cooper Immediate-early and delayed primary response genes are distinct in function and genomic architecture J. Biol. Chem. 282 2007 23981 23995
53. R.G. Urdinguio, L. Lopez-Serra, P. Lopez-Nieva, M. Alaminos, R. Diaz-Uriarte, A.F. Fernandez, and M. Esteller Mecp2-null mice provide new neuronal targets for Rett syndrome PLoS ONE 3 2008 e3669
54. D.H. Yasui, S. Peddada, M.C. Bieda, R.O. Vallero, A. Hogart, R.P. Nagarajan, K.N. Thatcher, P.J. Farnham, and J.M. Lasalle Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes Proc. Natl. Acad. Sci. USA 104 2007 19416 19421
55. M. Yazdani, R. Deogracias, J. Guy, R.A. Poot, A. Bird, and Y.A. Barde Disease modeling using embryonic stem cells: MeCP2 regulates nuclear size and RNA synthesis in neurons Stem Cells 30 2012 2128 2139
56. J. Yu, M.A. Vodyanik, K. Smuga-Otto, J. Antosiewicz-Bourget, J.L. Frane, S. Tian, J. Nie, G.A. Jonsdottir, V. Ruotti, and R. Stewart Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
57. J. Zhou, P. Su, D. Li, S. Tsang, E. Duan, and F. Wang High-efficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors Stem Cells 28 2010 1741 1750
58. R. Zoncu, A. Efeyan, and D.M. Sabatini mTOR: from growth signal integration to cancer, diabetes and ageing Nat. Rev. Mol. Cell Biol. 12 2011 21 35
59. I. Zvetkova, A. Apedaile, B. Ramsahoye, J.E. Mermoud, L.A. Crompton, R. John, R. Feil, and N. Brockdorff Global hypomethylation of the genome in XX embryonic stem cells Nat. Genet. 37 2005 1274 1279