MeCP2 mutation results in compartment-specific reductions in dendritic branching and spine density in layer 5 motor cortical neurons of YFP-H mice

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Stuss, David P ^a   Boyd, Jamie D ^b   Levin, David B ^c   Delaney, Kerry R ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

YELLOW FLUORESCENT PROTEIN; METHYL CPG BINDING PROTEIN 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL DENSITY; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC SPINE; GENE EXPRESSION; GENE LOCATION; HEMIZYGOSITY; MARKER GENE; MECP2 GENE; MOTONEURON; MOTOR CORTEX; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PYRAMIDAL NERVE CELL; SOMATIC CELL; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; C57BL MOUSE; DENDRITE; DISEASE MODEL; GENETICS; MALE; METABOLISM; MUTATION; PATHOLOGY; RETT SYNDROME;

MUS;

ANIMALS; DENDRITES; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR CORTEX; MOTOR NEURONS; MUTATION; RETT SYNDROME;

EID: 84857853505     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031896     Document Type: Article

References (91)

1. 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.
2. Hagberg B, (2002) Clinical manifestations and stages of Rett syndrome. Ment Retard Dev Disabil Res Rev 8: 61-65.
3. Chahrour M, Zoghbi HY, (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56: 422-437.
4. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM, (2006) Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21: 217-227.
5. Chao HT, Zoghbi HY, Rosenmund C, (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56: 58-65.
6. Chapleau CA, Calfa GD, Lane MC, Albertson AJ, Larimore JL, et al. (2009) Dendritic spine pathologies in hippocampal pyramidal neurons from Rett syndrome brain and after expression of Rett-associated MECP2 mutations. Neurobiol Dis 35: 219-233.
7. Armstrong DD, (2001) Rett syndrome neuropathology review 2000. Brain Dev 23 (Suppl 1): S72-S76.
8. Carter JC, Lanham DC, Pham D, Bibat G, Naidu S, et al. (2008) Selective cerebral volume reduction in Rett syndrome: a multiple-approach MR imaging study. AJNR Am J Neuroradiol 29: 436-441.
9. Subramaniam B, Naidu S, Reiss AL, (1997) Neuroanatomy in Rett syndrome: cerebral cortex and posterior fossa. Neurology 48: 399-407.
10. Belichenko PV, Oldfors A, Hagberg B, Dahlstrom A, (1994) Rett syndrome: 3-D confocal microscopy of cortical pyramidal dendrites and afferents. Neuroreport 5: 1509-1513.
11. Armstrong D, Dunn JK, Antalffy B, Trivedi R, (1995) Selective dendritic alterations in the cortex of Rett syndrome. J Neuropathol Exp Neurol 54: 195-201.
12. Bauman ML, Kemper TL, Arin DM, (1995) Microscopic observations of the brain in Rett syndrome. Neuropediatrics 26: 105-108.
13. Bauman ML, Kemper TL, Arin DM, (1995) Pervasive neuroanatomic abnormalities of the brain in three cases of Rett's syndrome. Neurology 45: 1581-1586.
14. Belichenko PV, Hagberg B, Dahlstrom A, (1997) Morphological study of neocortical areas in Rett syndrome. Acta Neuropathol (Berl) 93: 50-61.
15. Armstrong DD, Dunn K, Antalffy B, (1998) Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol 57: 1013-1017.
16. Amir RE, Van den Veyver IB, Schultz R, Malicki DM, Tran CQ, et al. (2000) Influence of mutation type and X chromosome inactivation on Rett syndrome phenotypes. Ann Neurol 47: 670-679.
17. Schanen C, Houwink EJ, Dorrani N, Lane J, Everett R, et al. (2004) Phenotypic manifestations of MECP2 mutations in classical and atypical Rett syndrome. Am J Med Genet A 126: 129-140.
18. Charman T, Neilson TC, Mash V, Archer H, Gardiner MT, et al. (2005) Dimensional phenotypic analysis and functional categorisation of mutations reveal novel genotype-phenotype associations in Rett syndrome. Eur J Hum Genet 13: 1121-1130.
19. Neul JL, Fang P, Barrish J, Lane J, Caeg EB, et al. (2008) Specific mutations in methyl-CpG-binding protein 2 confer different severity in Rett syndrome. Neurology 70: 1313-1321.
20. 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.
21. 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.
22. 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.
23. Pelka GJ, Watson CM, Radziewic T, Hayward M, Lahooti H, et al. (2006) Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129: 887-898.
24. Jentarra GM, Olfers SL, Rice SG, Srivastava N, Homanics GE, et al. (2010) Abnormalities of cell packing density and dendritic complexity in the MeCP2 A140V mouse model of Rett syndrome/X-linked mental retardation. BMC Neurosci 11: 19.
25. Fukuda T, Itoh M, Ichikawa T, Washiyama K, Goto Y, (2005) Delayed maturation of neuronal architecture and synaptogenesis in cerebral cortex of Mecp2-deficient mice. J Neuropathol Exp Neurol 64: 537-544.
26. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, et al. (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26: 319-327.
27. Smrt RD, Eaves-Egenes J, Barkho BZ, Santistevan NJ, Zhao C, et al. (2007) Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol Dis 27: 77-89.
28. 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.
29. Kishi N, Macklis JD, (2010) MeCP2 functions largely cell-autonomously, but also non-cell-autonomously, in neuronal maturation and dendritic arborization of cortical pyramidal neurons. Exp Neurol 222: 51-58.
30. Belichenko NP, Belichenko PV, Li HH, Mobley WC, Francke U, (2008) Comparative study of brain morphology in Mecp2 mutant mouse models of Rett syndrome. J Comp Neurol 508: 184-195.
31. Belichenko PV, Wright EE, Belichenko NP, Masliah E, Li HH, et al. (2009) Widespread changes in dendritic and axonal morphology in Mecp2-mutant mouse models of Rett syndrome: evidence for disruption of neuronal networks. J Comp Neurol 514: 240-258.
32. Belichenko NP, Belichenko PV, Mobley WC, (2009) Evidence for both neuronal cell autonomous and nonautonomous effects of methyl-CpG-binding protein 2 in the cerebral cortex of female mice with Mecp2 mutation. Neurobiol Dis 34: 71-77.
33. Degano AL, Pasterkamp RJ, Ronnett GV, (2009) MeCP2 deficiency disrupts axonal guidance, fasciculation, and targeting by altering Semaphorin 3F function. Mol Cell Neurosci 42: 243-254.
34. Tropea D, Giacometti E, Wilson NR, Beard C, McCurry C, et al. (2009) Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Proc Natl Acad Sci U S A 106: 2029-2034.
35. Percy AK, Zoghbi HY, Lewis KR, Jankovic J, (1988) Rett syndrome: qualitative and quantitative differentiation from autism. J Child Neurol 3 (Suppl): S65-S67.
36. Akemann W, Zhong YM, Ichinohe N, Rockland KS, Knöpfel T, (2004) Transgenic mice expressing a fluorescent in vivo label in a distinct subpopulation of neocortical layer 5 pyramidal cells. J Comp Neurol 480: 72-88.
37. Molyneaux BJ, Arlotta P, Fame RM, MacDonald JL, MacQuarrie KL, et al. (2009) Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J Neurosci 29: 12343-12354.
38. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, et al. (2006) Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9: 99-107.
39. Tsiola A, Hamzei-Sichani F, Peterlin Z, Yuste R, (2003) Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex. J Comp Neurol 461: 415-428.
40. Yu J, Anderson CT, Kiritani T, Sheets PL, Wokosin DL, et al. (2008) Local-Circuit Phenotypes of Layer 5 Neurons in Motor-Frontal Cortex of YFP-H Mice. Front Neural Circuits 2: 6.
41. Hattox AM, Nelson SB, (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98: 3330-3340.
42. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
43. Zhang S, Boyd J, Delaney K, Murphy TH, (2005) Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J Neurosci 25: 5333-5338.
44. Dombeck DA, Khabbaz AN, Collman F, Adelman TL, Tank DW, (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56: 43-57.
45. Enright LE, Zhang S, Murphy TH, (2007) Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J Cereb Blood Flow Metab 27: 1185-1200.
46. Grutzendler J, Kasthuri N, Gan WB, (2002) Long-term dendritic spine stability in the adult cortex. Nature 420: 812-816.
47. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, et al. (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45: 279-291.
48. Li P, Murphy TH, (2008) Two-photon imaging during prolonged middle cerebral artery occlusion in mice reveals recovery of dendritic structure after reperfusion. J Neurosci 28: 11970-11979.
49. Miller MN, Okaty BW, Nelson SB, (2008) Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J Neurosci 28: 13716-13726.
50. Jordan C, Li HH, Kwan HC, Francke U, (2007) Cerebellar gene expression profiles of mouse models for Rett syndrome reveal novel MeCP2 targets. BMC Med Genet 8: 36.
51. 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.
52. Braunschweig D, Simcox T, Samaco RC, LaSalle JM, (2004) X-Chromosome inactivation ratios affect wild-type MeCP2 expression within mosaic Rett syndrome and Mecp2-/+ mouse brain. Hum Mol Genet 13: 1275-1286.
53. Paxinos G, Franklin KBJ, (2001) The mouse brain in stereotaxic coordinates San Diego Academic Press.
54. Caroni P, (1997) Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J Neurosci Methods 71: 3-9.
55. Adams VH, McBryant SJ, Wade PA, Woodcock CL, Hansen JC, (2007) Intrinsic disorder and autonomous domain function in the multifunctional nuclear protein, MeCP2. J Biol Chem 282: 15057-15064.
56. Beirowski B, Berek L, Adalbert R, Wagner D, Grumme DS, et al. (2004) Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J Neurosci Methods 134: 23-35.
57. Bittner T, Fuhrmann M, Burgold S, Ochs SM, Hoffmann N, et al. (2010) Multiple events lead to dendritic spine loss in triple transgenic Alzheimer's disease mice. PLoS One 5: e15477.
58. Hansen KF, Sakamoto K, Wayman GA, Impey S, Obrietan K, (2010) Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One 5: e15497.
59. Landi S, Putignano E, Boggio EA, Pizzorusso T, Ratto GM, (2011) The short-time structural plasticity of dendritic spines is altered in a model of Rett syndrome. Sci Rep 1:45: 1-7.
60. Matter C, Pribadi M, Liu X, Trachtenberg JT, (2009) Delta-catenin is required for the maintenance of neural structure and function in mature cortex in vivo. Neuron 64: 320-327.
61. Migliore M, Shepherd GM, (2005) Opinion: an integrated approach to classifying neuronal phenotypes. Nat Rev Neurosci 6: 810-818.
62. Molnár Z, Cheung AF, (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55: 105-115.
63. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD, (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427-437.
64. Kriaucionis S, Bird A, (2004) The major form of MeCP2 has a novel N-terminus generated by alternative splicing. Nucleic Acids Res 32: 1818-1823.
65. 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.
66. Mullaney BC, Johnston MV, Blue ME, (2004) Developmental expression of methyl-CpG binding protein 2 is dynamically regulated in the rodent brain. Neuroscience 123: 939-949.
67. Samaco RC, Nagarajan RP, Braunschweig D, LaSalle JM, (2004) Multiple pathways regulate MeCP2 expression in normal brain development and exhibit defects in autism-spectrum disorders. Hum Mol Genet 13: 629-639.
68. Reichwald K, Thiesen J, Wiehe T, Weitzel J, Poustka WA, et al. (2000) Comparative sequence analysis of the MECP2-locus in human and mouse reveals new transcribed regions. Mamm Genome 11: 182-190.
69. Coy JF, Sedlacek Z, Bachner D, Delius H, Poustka A, (1999) A complex pattern of evolutionary conservation and alternative polyadenylation within the long 3″-untranslated region of the methyl-CpG-binding protein 2 gene (MeCP2) suggests a regulatory role in gene expression. Hum Mol Genet 8: 1253-1262.
70. 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 81: 61-68.
71. Zhou Z, Hong EJ, Cohen S, Zhao WN, Ho HY, et al. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52: 255-269.
72. Tao J, Hu K, Chang Q, Wu H, Sherman NE, et al. (2009) Phosphorylation of MeCP2 at Serine 80 regulates its chromatin association and neurological function. Proc Natl Acad Sci U S A 106: 4882-4887.
73. Nan X, Campoy FJ, Bird A, (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88: 471-481.
74. Colantuoni C, Jeon OH, Hyder K, Chenchik A, Khimani AH, et al. (2001) Gene expression profiling in postmortem Rett Syndrome brain: differential gene expression and patient classification. Neurobiol Dis 8: 847-865.
75. Yasui DH, Peddada S, Bieda MC, Vallero RO, Hogart A, et al. (2007) Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc Natl Acad Sci U S A 104: 19416-19421.
76. 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.
77. Wu H, Tao J, Chen PJ, Shahab A, Ge W, et al. (2010) Genome-wide analysis reveals methyl-CpG-binding protein 2-dependent regulation of microRNAs in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A.
78. Young JI, Hong EP, Castle JC, Crespo-Barreto J, Bowman AB, et al. (2005) Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc Natl Acad Sci U S A 102: 17551-17558.
79. 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.
80. Urdinguio RG, Lopez-Serra L, Lopez-Nieva P, Alaminos M, Diaz-Uriarte R, et al. (2008) Mecp2-null mice provide new neuronal targets for Rett syndrome. PLoS One 3: e3669.
81. 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.
82. Gibson JH, Slobedman B, Harikrishnan KN, Williamson SL, Minchenko D, et al. (2010) Downstream targets of methyl CpG binding protein 2 and their abnormal expression in the frontal cortex of the human Rett syndrome brain. BMC Neurosci 11: 53.
83. 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.
84. Peddada S, Yasui DH, LaSalle JM, (2006) Inhibitors of differentiation (ID1, ID2, ID3 and ID4) genes are neuronal targets of MeCP2 that are elevated in Rett syndrome. Hum Mol Genet 15: 2003-2014.
85. Walters MC, Fiering S, Eidemiller J, Magis W, Groudine M, et al. (1995) Enhancers increase the probability but not the level of gene expression. Proc Natl Acad Sci U S A 92: 7125-7129.
86. Graubert TA, Hug BA, Wesselschmidt R, Hsieh CL, Ryan TM, et al. (1998) Stochastic, stage-specific mechanisms account for the variegation of a human globin transgene. Nucleic Acids Res 26: 2849-2858.
87. O'Leary DD, Stanfield BB, (1985) Occipital cortical neurons with transient pyramidal tract axons extend and maintain collaterals to subcortical but not intracortical targets. Brain Res 336: 326-333.
88. Stanfield BB, O'Leary DD, (1985) The transient corticospinal projection from the occipital cortex during the postnatal development of the rat. J Comp Neurol 238: 236-248.
89. Thong IG, Dreher B, (1987) The development of the corticotectal pathway in the albino rat: transient projections from the visual and motor cortices. Neurosci Lett 80: 275-282.
90. Cassel S, Revel MO, Kelche C, Zwiller J, (2004) Expression of the methyl-CpG-binding protein MeCP2 in rat brain. An ontogenetic study. Neurobiol Dis 15: 206-211.
91. 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.