Altered neuronal network and rescue in a human MECP2 duplication model

Molecular Psychiatry

Volumn 21, Issue 2, 2016, Pages 178-188

  Nageshappa, S ^a   Carromeu, C ^b,c   Trujillo, C A ^b,c   Mesci, P ^b,c   Espuny Camacho, I ^d,e   Pasciuto, E ^e,f   Vanderhaeghen, P ^d,e,g   Verfaillie, C M ^f   Raitano, S ^f   Kumar, A ^f,h   Carvalho, C M B ^i,j   Bagni, C ^e,f,k   Ramocki, M B ⁱ   Araujo, B H S ^b,c   Torres, L B ^b,c   Lupski, J R ⁱ   Van Esch, H ^a,l   Muotri, A R ^b,c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g WELBIO   (Belgium)

^h Manipal Academy of Higher Education   (India)

ⁱ BAYLOR COLLEGE OF MEDICINE   (United States)

^j INSTITUTO OSWALDO CRUZ   (Brazil)

^k UNIVERSITY OF ROME TOR VERGATA   (Italy)

^l UNIVERSITY HOSPITALS LEUVEN   (Belgium)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; METHYL CPG BINDING PROTEIN 2; NCH 51; UNCLASSIFIED DRUG;

ARTICLE; AUTISM; BRAIN CELL; CASE REPORT; COMPULSION; COPY NUMBER VARIATION; DEVELOPMENTAL DISORDER; EPILEPSY; FEEDING DIFFICULTY; GENE DOSAGE; GENETIC SCREENING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; LANGUAGE DELAY; MALE; MECP2 DUPLICATION SYNDROME; MENTAL DISEASE; MUSCLE HYPOTONIA; NERVE CELL NETWORK; PLURIPOTENT STEM CELL; PNEUMONIA; PRIORITY JOURNAL; RECURRENT INFECTION; SYNAPTOGENESIS; CELL DIFFERENTIATION; COMPARATIVE STUDY; DENDRITE; GENE DUPLICATION; GENETIC ASSOCIATION STUDY; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

CELL DIFFERENTIATION; DENDRITES; GENE DOSAGE; GENE DUPLICATION; GENETIC ASSOCIATION STUDIES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; METHYL-CPG-BINDING PROTEIN 2; NERVE NET; NEUROGENESIS; NEURONS;

EID: 84955192128     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.128     Document Type: Article

References (36)

1. Van Esch H, Bauters M, Ignatius J, Jansen M, Raynaud M, Hollanders K 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 2005; 77: 442-453.
2. del Gaudio D, Fang P, Scaglia F, Ward PA, Craigen WJ, Glaze DG et al. Increased MECP2 gene copy number as the result of genomic duplication in neurodevelopmentally delayed males. Genet Med 2006; 8: 784-792.
3. Ramocki MB, Peters SU, Tavyev YJ, Zhang F, Carvalho CM, Schaaf CP et al. Autism and other neuropsychiatric symptoms are prevalent in individuals with MeCP2 duplication syndrome. Ann Neurol 2009; 66: 771-782.
4. Ramocki MB, Tavyev YJ, Peters SU. The MECP2 duplication syndrome. Am J Med Genet A 2010; 152A: 1079-1088.
5. Van Esch H. MECP2 Duplication Syndrome. Mol Syndromol 2012; 2: 128-136.
6. Luikenhuis S, Giacometti E, Beard CF, Jaenisch R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc Natl Acad Sci USA 2004; 101: 6033-6038.
7. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 2004; 13: 2679-2689.
8. Na ES, Nelson ED, Adachi M, Autry AE, Mahgoub MA, Kavalali ET et al. A mouse model for MeCP2 duplication syndrome: MeCP2 overexpression impairs learning and memory and synaptic transmission. J Neurosci 2012; 32: 3109-3117.
9. Samaco RC, Mandel-Brehm C, McGraw CM, Shaw CA, McGill BE, Zoghbi HY. Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nat Genet 2012; 44: 206-211.
10. Jung BP, Jugloff DG, Zhang G, Logan R, Brown S, Eubanks JH. The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J Neurobiol 2003; 55: 86-96.
11. Jiang M, Ash RT, Baker SA, Suter B, Ferguson A, Park J et al. Dendritic arborization and spine dynamics are abnormal in the mouse model of MECP2 duplication syndrome. J Neurosci 2013; 33: 19518-19533.
12. Chahrour M, Zoghbi HY. The story of Rett syndrome: from clinic to neurobiology. Neuron 2007; 56: 422-437.
13. Chailangkarn T, Acab A, Muotri AR. Modeling neurodevelopmental disorders using human neurons. Curr Opin Neurobiol 2012; 22: 785-790.
14. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 2010; 143: 527-539.
15. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K et al. L1 retrotransposition in neurons is modulated by MeCP2. Nature 2010; 468: 443-446.
16. Carvalho CM, Zhang F, Liu P, Patel A, Sahoo T, Bacino CA et al. Complex rearrangements in patients with duplications of MECP2 can occur by fork stalling and template switching. Hum Mol Genet 2009; 18: 2188-2203.
17. Carvalho CM, Pehlivan D, Ramocki MB, Fang P, Alleva B, Franco LM et al. Replicative mechanisms for CNV formation are error prone. Nat Genet 2013; 45: 1319-1326.
18. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
19. Griesi-Oliveira K, Acab A, Gupta AR, Sunaga DY, Chailangkarn T, Nicol X et al. Modeling non-syndromic autism and the impact of TRPC6 disruption in human neurons. Mol Psychiatry 2014 [Epub ahead of print].
20. Espuny-Camacho I, Michelsen KA, Gall D, Linaro D, Hasche A, Bonnefont J et al. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 2013; 77: 440-456.
21. Ohashi Y, Tsubota T, Sato A, Koyano KW, Tamura K, Miyashita Y. A bicistronic lentiviral vector-based method for differential transsynaptic tracing of neural circuits. Mol Cell Neurosci 2011; 46: 136-147.
22. Damak S, Mosinger B, Margolskee RF. Transsynaptic transport of wheat germ agglutinin expressed in a subset of type II taste cells of transgenic mice. BMC Neurosci 2008; 9: 96.
23. Harris KM, Jensen FE, Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 1992; 12: 2685-2705.
24. Bauters M, Van Esch H, Friez MJ, Boespflug-Tanguy O, Zenker M, Vianna-Morgante AM et al. Nonrecurrent MECP2 duplications mediated by genomic architecture-driven DNA breaks and break-induced replication repair. Genome Res 2008; 18: 847-858.
25. Kundakovic M, Chen Y, Guidotti A, Grayson DR. The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Mol Pharmacol 2009; 75: 342-354.
26. Spira ME, Hai A. Multi-electrode array technologies for neuroscience and cardiology. Nat Nanotechnol 2013; 8: 83-94.
27. Chao HT, Zoghbi HY, Rosenmund C. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 2007; 56: 58-65.
28. Jugloff DG, Jung BP, Purushotham D, Logan R, Eubanks JH. Increased dendritic complexity and axonal length in cultured mouse cortical neurons overexpressing methyl-CpG-binding protein MeCP2. Neurobiol Dis 2005; 19: 18-27.
29. Zhou Z, Hong EJ, Cohen S, Zhao WN, Ho HY, Schmidt L et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 2006; 52: 255-269.
30. Sala C, Segal M. Dendritic spines: The locus of structural and functional plasticity. Physiol Rev 2014; 94: 141-188.
31. Cubelos B, Sebastián-Serrano A, Beccari L, Calcagnotto ME, Cisneros E, Kim S et al. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 2010; 66: 523-535.
32. Grueber WB, Jan LY, Jan YN. Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 2003; 112: 805-818.
33. Li Y, Wang H, Muffat J, Cheng AW, Orlando DA, Lovén J et al. Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons. Cell Stem Cell 2013; 13: 446-458.
34. Wainger BJ, Kiskinis E, Mellin C, Wiskow O, Han SS, Sandoe J et al. Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons. Cell Rep 2014; 7: 1-11.
35. Odawara A, Saitoh Y, Alhebshi AH, Gotoh M, Suzuki I. Long-term electrophysiological activity and pharmacological response of a human induced pluripotent stem cell-derived neuron and astrocyte co-culture. Biochem Biophys Res Commun 2014; 443: 1176-1181.
36. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393: 386-389.