Cell-autonomous alterations in dendritic arbor morphology and connectivity induced by overexpression of MeCP2 in Xenopus central neurons in vivo

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Marshak, Sonya ^a   Meynard, Margarita M ^a   de Vries, Ymkje A ^a   Kidane, Adhanet H ^a   Cohen Cory, Susana ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYL CPG BINDING PROTEIN 2; COMPLEMENTARY DNA; FLUORESCENT PROTEIN 583; MECP2 PROTEIN, HUMAN; PHOTOPROTEIN; PRIMER DNA;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; DEVELOPMENTAL STAGE; DNA SEQUENCE; FEMALE; GENE; GENE DOSAGE; GENE OVEREXPRESSION; IN VIVO STUDY; METHYL CPG BINDING PROTEIN 2 GENE; NERVE CELL NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC MEMBRANE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRUCTURE ANALYSIS; UPREGULATION; XENOPUS LAEVIS; ANIMAL; BIOLOGICAL MODEL; BRAIN; CYTOLOGY; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME LAPSE IMAGING; ULTRASTRUCTURE; XENOPUS;

XENOPUS LAEVIS;

ANIMALS; BRAIN; DENDRITES; DNA PRIMERS; DNA, COMPLEMENTARY; HUMANS; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; METHYL-CPG-BINDING PROTEIN 2; MICROSCOPY, CONFOCAL; MODELS, NEUROLOGICAL; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME-LAPSE IMAGING; XENOPUS;

EID: 84857948615     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033153     Document Type: Article

References (62)

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. Friez MJ, Jones JR, Clarkson K, Lubs H, Abuelo D, et al. (2006) Recurrent infections, hypotonia, and mental retardation caused by duplication of MECP2 and adjacent region in Xq28. Pediatrics 118: e1687-1695.
3. Lugtenberg D, de Brouwer AP, Kleefstra T, Oudakker AR, Frints SG, et al. (2006) Chromosomal copy number changes in patients with non-syndromic X linked mental retardation detected by array CGH. J Med Genet 43: 362-370.
4. Van Esch H, Bauters M, Ignatius J, Jansen M, Raynaud M, et al. (2005) Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Am J Hum Genet 77: 442-453.
5. del Gaudio D, Fang P, Scaglia F, Ward PA, Craigen WJ, et al. (2006) Increased MECP2 gene copy number as the result of genomic duplication in neurodevelopmentally delayed males. Genet Med 8: 784-792.
6. Stancheva I, Collins AL, Van den Veyver IB, Zoghbi H, Meehan RR, (2003) A mutant form of MeCP2 protein associated with human Rett syndrome cannot be displaced from methylated DNA by notch in Xenopus embryos. Mol Cell 12: 425-435.
7. Coverdale LE, Martyniuk CJ, Trudeau VL, Martin CC, (2004) Differential expression of the methyl-cytosine binding protein 2 gene in embryonic and adult brain of zebrafish. Brain Res Dev Brain Res 153: 281-287.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. Jung BP, Jugloff DG, Zhang G, Logan R, Brown S, et al. (2003) The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J Neurobiol 55: 86-96.
14. Chahrour M, Zoghbi HY, (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56: 422-437.
15. Boggio EM, Lonetti G, Pizzorusso T, Giustetto M, (2010) Synaptic determinants of rett syndrome. Front Synaptic Neurosci 2: 28.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. Chao HT, Zoghbi HY, Rosenmund C, (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56: 58-65.
22. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, et al. (2005) Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 102: 12560-12565.
23. 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.
24. Jugloff DG, Jung BP, Purushotham D, Logan R, Eubanks JH, (2005) Increased dendritic complexity and axonal length in cultured mouse cortical neurons overexpressing methyl-CpG-binding protein MeCP2. Neurobiol Dis 19: 18-27.
25. 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.
26. Nelson ED, Kavalali ET, Monteggia LM, (2006) MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr Biol 16: 710-716.
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. 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.
29. Nieuwkoop PD, Faber J, (1956) Normal Table of Xenopus laevis The Netherlands Elsevier North Holland.
30. Sanchez AL, Matthews BJ, Meynard MM, Hu B, Javed S, et al. (2006) BDNF increases synapse density in dendrites of developing tectal neurons in vivo. Development 133: 2477-2486.
31. Marshak S, Nikolakopoulou AM, Dirks R, Martens GJ, Cohen-Cory S, (2007) Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J Neurosci 27: 2444-2456.
32. Tao HW, Poo MM, (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45: 829-836.
33. Cline HT, (2001) Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11: 118-126.
34. Cohen-Cory S, Lom B, (2004) Neurotrophic regulation of retinal ganglion cell synaptic connectivity: from axons and dendrites to synapses. Int J Dev Biol 48: 947-956.
35. Niell CM, Smith SJ, (2004) Live optical imaging of nervous system development. Annu Rev Physiol 66: 771-798.
36. Hossain S, Hewapathirane DS, Haas K, (2011) Dynamic Morphometrics reveals contributions of dendritic growth cones and filopodia to dendritogenesis in the intact and awake embryonic brain. Dev Neurobiol.
37. Armstrong DD, (1992) The neuropathology of the Rett syndrome. Brain Dev 14 (Suppl): S89-98.
38. 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.
39. 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.
40. Shepherd GM, Katz DM, (2011) Synaptic microcircuit dysfunction in genetic models of neurodevelopmental disorders: focus on Mecp2 and Met. Curr Opin Neurobiol.
41. 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.
42. Belichenko PV, Dahlstrom A, (1995) Studies on the 3-dimensional architecture of dendritic spines and varicosities in human cortex by confocal laser scanning microscopy and Lucifer yellow microinjections. J Neurosci Methods 57: 55-61.
43. Tripodi M, Evers JF, Mauss A, Bate M, Landgraf M, (2008) Structural homeostasis: compensatory adjustments of dendritic arbor geometry in response to variations of synaptic input. PLoS Biol 6: e260.
44. 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.
45. 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.
46. Hite KC, Adams VH, Hansen JC, (2009) Recent advances in MeCP2 structure and function. Biochem Cell Biol 87: 219-227.
47. Chao HT, Zoghbi HY, (2009) The yin and yang of MeCP2 phosphorylation. Proc Natl Acad Sci U S A 106: 4577-4578.
48. Chen WG, Chang Q, Lin Y, Meissner A, West AE, et al. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302: 885-889.
49. Martinowich K, Hattori D, Wu H, Fouse S, He F, et al. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302: 890-893.
50. Larimore JL, Chapleau CA, Kudo S, Theibert A, Percy AK, et al. (2009) Bdnf overexpression in hippocampal neurons prevents dendritic atrophy caused by Rett-associated MECP2 mutations. Neurobiol Dis 34: 199-211.
51. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R, (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49: 341-348.
52. Kline DD, Ogier M, Kunze DL, Katz DM, (2010) Exogenous brain-derived neurotrophic factor rescues synaptic dysfunction in Mecp2-null mice. J Neurosci 30: 5303-5310.
53. Alsina B, Vu T, Cohen-Cory S, (2001) Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat Neurosci 4: 1093-1101.
54. Hu B, Nikolakopoulou AM, Cohen-Cory S, (2005) BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 132: 4285-4298.
55. Cohen-Cory S, Escandon E, Fraser SE, (1996) The cellular patterns of BDNF and trkB expression suggest multiple roles for BDNF during Xenopus visual system development. Dev Biol 179: 102-115.
56. Samaco RC, Neul JL, (2011) Complexities of Rett syndrome and MeCP2. J Neurosci 31: 7951-7959.
57. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, et al. (2010) Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468: 263-269.
58. Samaco RC, Mandel-Brehm C, Chao HT, Ward CS, Fyffe-Maricich SL, et al. (2009) Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc Natl Acad Sci U S A 106: 21966-21971.
59. 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.
60. 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.
61. 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.
62. 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.