MeCP2 Dependent Heterochromatin Reorganization during Neural Differentiation of a Novel Mecp2-Deficient Embryonic Stem Cell Reporter Line

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Bertulat, Bianca ^a   de Bonis, Maria Luigia ^b   Della Ragione, Floriana ^b,c   Lehmkuhl, Anne ^a   Milden, Manuela ^a   Storm, Christian ^a   Jost, K Laurence ^a   Scala, Simona ^c   Hendrich, Brian ^d   D'Esposito, Maurizio ^b,c   Cardoso, M Cristina ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c IRCCS NEUROMED   (Italy)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; METHYL CYTOSINE BINDING PROTEIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EPIGENETICS; GLIA CELL; HETEROCHROMATIN; IMMUNOBLOTTING; IN VITRO STUDY; MACROGLIA; MECP2 GENE; MORPHOLOGY; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ANIMALS; CELL LINE; EMBRYONIC STEM CELLS; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROCHROMATIN; HUMANS; METHYL-CPG-BINDING PROTEIN 2; MICE; NEUROGENESIS; NEURONS; RETT SYNDROME;

MURINAE;

EID: 84868153046     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047848     Document Type: Article

References (80)

1. Probst AV, Almouzni G, (2011) Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet 27: 177-185.
2. Dillon N, Festenstein R, (2002) Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. Trends Genet 18: 252-258.
3. Terranova R, Sauer S, Merkenschlager M, Fisher AG, (2005) The reorganisation of constitutive heterochromatin in differentiating muscle requires HDAC activity. Exp Cell Res 310: 344-356.
4. Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, et al. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137: 356-368.
5. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, et al. (2005) Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J Cell Biol 169: 733-743.
6. Marchi M, Guarda A, Bergo A, Landsberger N, Kilstrup-Nielsen C, et al. (2007) Spatio-temporal dynamics and localization of MeCP2 and pathological mutants in living cells. Epigenetics 2: 187-197.
7. Liu Y, Rao MS, (2003) Transdifferentiation-fact or artifact. J Cell Biochem 88: 29-40.
8. Terranova R, Pereira CF, Du Roure C, Merkenschlager M, Fisher AG, (2006) Acquisition and extinction of gene expression programs are separable events in heterokaryon reprogramming. J Cell Sci 119: 2065-2072.
9. Lachner M, O'Sullivan RJ, Jenuwein T, (2003) An epigenetic road map for histone lysine methylation. J Cell Sci 116: 2117-2124.
10. Bird A, Tate P, Nan X, Campoy J, Meehan R, et al. (1995) Studies of DNA methylation in animals. J Cell Sci Suppl 19: 37-39.
11. Guenatri M, Bailly D, Maison C, Almouzni G, (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505.
12. Baccarini P, (1908) Sulle cinesi vegetative del "Cynomorium coccineum L.". Nuovo Giornale Botanico Italiano XV: 189-203.
13. Heitz E, (1929) Heterochromatin, Chromocentren, Chromomeren. Ber der Deutschen Bot Gesellsch XLVII: 274-284.
14. Agarwal N, Hardt T, Brero A, Nowak D, Rothbauer U, et al. (2007) MeCP2 interacts with HP1 and modulates its heterochromatin association during myogenic differentiation. Nucleic Acids Res 35: 5402-5408.
15. Dhasarathy A, Wade PA, (2008) The MBD protein family-reading an epigenetic mark? Mutat Res 647: 39-43.
16. Wade PA, (2001) Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20: 3166-3173.
17. Bird A, (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21.
18. Klose RJ, Bird AP, (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31: 89-97.
19. D'Esposito M, Quaderi NA, Ciccodicola A, Bruni P, Esposito T, et al. (1996) Isolation, physical mapping, and northern analysis of the X-linked human gene encoding methyl CpG-binding protein, MECP2. Mamm Genome 7: 533-535.
20. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, et al. (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69: 905-914.
21. Meehan RR, Lewis JD, Bird AP, (1992) Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA. Nucleic Acids Res 20: 5085-5092.
22. Nan X, Meehan RR, Bird A, (1993) Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res 21: 4886-4892.
23. Hendrich B, Bird A, (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18: 6538-6547.
24. Guy J, Cheval H, Selfridge J, Bird A, (2011) The role of MeCP2 in the brain. Annu Rev Cell Dev Biol 27: 631-652.
25. Adkins NL, Georgel PT, (2011) MeCP2: structure and function. Biochem Cell Biol 89: 1-11.
26. de Leon-Guerrero SD, Pedraza-Alva G, Perez-Martinez L, (2011) In sickness and in health: the role of methyl-CpG binding protein 2 in the central nervous system. Eur J Neurosci 33: 1563-1574.
27. Bienvenu T, Chelly J, (2006) Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat Rev Genet 7: 415-426.
28. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, et al. (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl- CpG-binding protein 2. Nat Genet 23: 185-188.
29. Hagberg B, Aicardi J, Dias K, Ramos O, (1983) 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: 471-479.
30. Rett A, (1966) [On a unusual brain atrophy syndrome in hyperammonemia in childhood]. Wien Med Wochenschr 116: 723-726.
31. Samaco RC, Neul JL, (2011) Complexities of Rett syndrome and MeCP2. J Neurosci 31: 7951-7959.
32. Luikenhuis S, Giacometti E, Beard CF, Jaenisch R, (2004) Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc Natl Acad Sci U S A 101: 6033-6038.
33. Chen RZ, Akbarian S, Tudor M, 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.
34. Guy J, Hendrich B, Holmes M, Martin JE, Bird A, (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27: 322-326.
35. Chandler SP, Guschin D, Landsberger N, Wolffe AP, (1999) The methyl-CpG binding transcriptional repressor MeCP2 stably associates with nucleosomal DNA. Biochemistry 38: 7008-7018.
36. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, et al. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389.
37. Nan X, Campoy FJ, Bird A, (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88: 471-481.
38. Nan X, Bird A, (2001) The biological functions of the methyl-CpG-binding protein MeCP2 and its implication in Rett syndrome. Brain Dev 23 (Suppl 1): S32-37.
39. Kudo S, (1998) Methyl-CpG-binding protein MeCP2 represses Sp1-activated transcription of the human leukosialin gene when the promoter is methylated. Mol Cell Biol 18: 5492-5499.
40. Kishi N, Macklis JD, (2004) 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.
41. Skene PJ, Illingworth RS, Webb S, Kerr AR, James KD, et al. (2010) Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol Cell 37: 457-468.
42. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, et al. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320: 1224-1229.
43. Ben-Shachar S, Chahrour M, Thaller C, Shaw CA, Zoghbi HY, (2009) Mouse models of MeCP2 disorders share gene expression changes in the cerebellum and hypothalamus. Hum Mol Genet 18: 2431-2442.
44. Ballas N, Lioy DT, Grunseich C, Mandel G, (2009) Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12: 311-317.
45. Maezawa I, Jin LW, (2010) Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30: 5346-5356.
46. Maezawa I, Swanberg S, Harvey D, LaSalle JM, Jin LW, (2009) Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions. J Neurosci 29: 5051-5061.
47. Lioy DT, Garg SK, Monaghan CE, Raber J, Foust KD, et al. (2011) A role for glia in the progression of Rett's syndrome. Nature 475: 497-500.
48. Chao HT, Zoghbi HY, (2012) MeCP2: only 100% will do. Nat Neurosci 15: 176-177.
49. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, et al. (2004) Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 13: 2679-2689.
50. Kudo S, Nomura Y, Segawa M, Fujita N, Nakao M, et al. (2001) Functional analyses of MeCP2 mutations associated with Rett syndrome using transient expression systems. Brain Dev 23 (Suppl 1): S165-173.
51. Nan X, Cross S, Bird A, (1998) Gene silencing by methyl-CpG-binding proteins. Novartis Found Symp 214: 6-16.
52. Chadwick LH, Wade PA, (2007) MeCP2 in Rett syndrome: transcriptional repressor or chromatin architectural protein? Curr Opin Genet Dev 17: 121-125.
53. Bird AP, Wolffe AP, (1999) Methylation-induced repression-belts, braces, and chromatin. Cell 99: 451-454.
54. Georgel PT, Horowitz-Scherer RA, Adkins N, Woodcock CL, Wade PA, et al. (2003) Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J Biol Chem 278: 32181-32188.
55. Singleton MK, Gonzales ML, Leung KN, Yasui DH, Schroeder DI, et al. (2011) MeCP2 is required for global heterochromatic and nucleolar changes during activity-dependent neuronal maturation. Neurobiol Dis 43: 190-200.
56. Armstrong L, (2012) Epigenetic control of embryonic stem cell differentiation. Stem Cell Rev 8: 67-77.
57. Arney KL, Fisher AG, (2004) Epigenetic aspects of differentiation. J Cell Sci 117: 4355-4363.
58. Fussner E, Djuric U, Strauss M, Hotta A, Perez-Iratxeta C, et al. (2011) Constitutive heterochromatin reorganization during somatic cell reprogramming. EMBO J 30: 1778-1789.
59. Cheval H, Guy J, Merusi C, De Sousa D, Selfridge J, et al. (2012) Postnatal inactivation reveals enhanced requirement for MeCP2 at distinct age windows. Hum Mol Genet 21: 3806-3814.
60. Tucker KL, Meyer M, Barde YA, (2001) Neurotrophins are required for nerve growth during development. Nat Neurosci 4: 29-37.
61. Ochman H, Gerber AS, Hartl DL, (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621-623.
62. Ying QL, Stavridis M, Griffiths D, Li M, Smith A, (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21: 183-186.
63. Wernig M, Tucker KL, Gornik V, Schneiders A, Buschwald R, et al. (2002) Tau EGFP embryonic stem cells: an efficient tool for neuronal lineage selection and transplantation. J Neurosci Res 69: 918-924.
64. Jost KL, Rottach A, Milden M, Bertulat B, Becker A, et al. (2011) Generation and characterization of rat and mouse monoclonal antibodies specific for MeCP2 and their use in X-inactivation studies. PLoS One 6: e26499.
65. Littell RC, G.A M, Stroup WW, Wolfinger RD (2006) SAS System for mixed models.
66. Littell RC, Henry PR, Ammerman CB, (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76: 1216-1231.
67. Fernández G (2007) Model selection in PROC MIXED - A user-friendly SAS® macro application. Proceedings of 2007 SAS Global Forum. Orlando FL, US. pp. paper 191-2007.
68. Moser E (2004) Repeated measures modeling with PROC MIXED. Proceedings of the 29th Annual SAS Users Group International Conference (SUGI). SAS Institute Inc., Cary, NC, US. pp. Statistics and Data Analysis: Paper 188-129.
69. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, et al. (2008) Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22: 152-165.
70. Wilson PG, Stice SS, (2006) Development and differentiation of neural rosettes derived from human embryonic stem cells. Stem Cell Rev 2: 67-77.
71. Shahbazian MD, Antalffy B, Armstrong DL, Zoghbi HY, (2002) Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum Mol Genet 11: 115-124.
72. Cohen DR, Matarazzo V, Palmer AM, Tu Y, Jeon OH, et al. (2003) Expression of MeCP2 in olfactory receptor neurons is developmentally regulated and occurs before synaptogenesis. Mol Cell Neurosci 22: 417-429.
73. Balmer D, Goldstine J, Rao YM, LaSalle JM, (2003) Elevated methyl-CpG-binding protein 2 expression is acquired during postnatal human brain development and is correlated with alternative polyadenylation. J Mol Med (Berl) 81: 61-68.
74. LaSalle JM, Goldstine J, Balmer D, Greco CM, (2001) Quantitative localization of heterogeneous methyl-CpG-binding protein 2 (MeCP2) expression phenotypes in normal and Rett syndrome brain by laser scanning cytometry. Hum Mol Genet 10: 1729-1740.
75. Nan X, Tate P, Li E, Bird A, (1996) DNA methylation specifies chromosomal localization of MeCP2. Mol Cell Biol 16: 414-421.
76. Agarwal N, Becker A, Jost KL, Haase S, Thakur BK, et al. (2011) MeCP2 Rett mutations affect large scale chromatin organization. Hum Mol Genet 20: 4187-4195.
77. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, et al. (2002) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35: 243-254.
78. Matarazzo V, Cohen D, Palmer AM, Simpson PJ, Khokhar B, et al. (2004) The transcriptional repressor Mecp2 regulates terminal neuronal differentiation. Mol Cell Neurosci 27: 44-58.
79. Nectoux J, Florian C, Delepine C, Bahi-Buisson N, Khelfaoui M, et al. (2012) Altered microtubule dynamics in Mecp2-deficient astrocytes. J Neurosci Res 90: 990-998.
80. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SB, et al. (2012) Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484: 105-109.