Excitation/inhibition imbalance and impaired synaptic inhibition in hippocampal area CA3 of Mecp2 knockout mice

Hippocampus

Volumn 25, Issue 2, 2015, Pages 159-168

  Calfa, Gaston ^a   Li, Wei ^a   Rutherford, John M ^a   Pozzo Miller, Lucas ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

E I balance; Hippocampus; Intellectual disability; MeCP2; Rett syndrome

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; METHYL CPG BINDING PROTEIN 2; PARVALBUMIN; SOMATOSTATIN; AMPA RECEPTOR; GABRA1 PROTEIN, MOUSE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; MECP2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RETT SYNDROME; SYNAPTIC INHIBITION; ANIMAL; CONFOCAL MICROSCOPY; DEFICIENCY; DISEASE MODEL; GENETICS; METABOLISM; MINIATURE ENDPLATE POTENTIAL; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE; TISSUE CULTURE TECHNIQUE;

ANIMALS; CA3 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MINIATURE POSTSYNAPTIC POTENTIALS; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RECEPTORS, AMPA; RECEPTORS, GABA-A; RETT SYNDROME; SYNAPSES; TISSUE CULTURE TECHNIQUES;

EID: 84921305880     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22360     Document Type: Article

References (47)

1. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet, 23, 185-8.
2. Calfa G, Hablitz JJ, Pozzo-Miller L. 2011a. Network hyperexcitability in hippocampal slices from Mecp2 mutant mice revealed by voltage-sensitive dye imaging. J Neurophysiol 105:1768-1784.
3. Calfa G, Percy AK, Pozzo-Miller L. 2011b. Experimental models of Rett syndrome based on Mecp2 dysfunction. Exp Biol Med (Maywood) 236:3-19.
4. Cardoza B, Clarke A, Wilcox J, Gibbon F, Smith PE, Archer H, Hryniewiecka-Jaworska A, Kerr M. 2011. Epilepsy in Rett syndrome: Association between phenotype and genotype, and implications for practice. Seizure 20:646-649.
5. 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.
6. Chao HT, Zoghbi HY, Rosenmund C. 2007. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56:58-65.
7. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C, Zoghbi HY. 2010. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468:263-269.
8. 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.
9. Costa RM, Federov NB, Kogan JH, Murphy GG, Stern J, Ohno M, Kucherlapati R, Jacks T, Silva AJ. 2002. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 415:526-530.
10. D'Cruz JA, Wu C, Zahid T, El-Hayek Y, Zhang L, Eubanks JH. 2010. Alterations of cortical and hippocampal EEG activity in MeCP2-deficient mice. Neurobiol Dis 38:8-16.
11. Dani VS, Nelson SB. 2009. Intact long-term potentiation but reduced connectivity between neocortical layer 5 pyramidal neurons in a mouse model of Rett syndrome. J Neurosci 29:11263-11270.
12. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. 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 USA 102:12560-12565.
13. Di Cristo G. 2007. Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders. Clin Genet 72:1-8.
14. Durand S, Patrizi A, Quast KB, Hachigian L, Pavlyuk R, Saxena A, Carninci P, Hensch TK, Fagiolini M. 2012. NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76:1078-1090.
15. Ehninger D, Li W, Fox K, Stryker MP, Silva AJ. 2008. Reversing neurodevelopmental disorders in adults. Neuron 60:950-960.
16. Fernandez F, Morishita W, Zuniga E, Nguyen J, Blank M, Malenka RC, Garner CC. 2007. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat Neurosci 10:411-413.
17. Frola E, Patrizi A, Goetz T, Medrihan L, Petrini EM, Barberis A, Wulff P, Wisden W, Sassoe-Pognetto M. 2013. Synaptic competition sculpts the development of GABAergic axo-dendritic but not perisomatic synapses. PLoS One 8:e56311.
18. Gibson JR, Bartley AF, Hays SA, Huber KM. 2008. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J Neurophysiol 100:2615-2626.
19. Glaze DG, Frost JD Jr, Zoghbi HY, Percy AK. 1987. Rett's syndrome. Correlation of electroencephalographic characteristics with clinical staging. Arch Neurol 44:1053-1056.
20. Hortnagl H, Tasan RO, Wieselthaler A, Kirchmair E, Sieghart W, Sperk G. 2013. Patterns of mRNA and protein expression for 12 GABAA receptor subunits in the mouse brain. Neuroscience 236:345-372.
21. Kleschevnikov AM, Belichenko PV, Villar AJ, Epstein CJ, Malenka RC, Mobley WC. 2004. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J Neurosci 24:8153-8160.
22. 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.
23. Kohara K, Yasuda H, Huang Y, Adachi N, Sohya K, Tsumoto T. 2007. A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. J Neurosci 27:7234-7244.
24. Kron M, Howell CJ, Adams IT, Ransbottom M, Christian D, Ogier M, Katz DM. 2012. 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 32:13860-13872.
25. Lawrence JJ, McBain CJ. 2003. Interneuron diversity series: Containing the detonation--feedforward inhibition in the CA3 hippocampus. Trends Neurosci 26:631-640.
26. Li W, Pozzo-Miller L. 2014. BDNF deregulation in Rett syndrome. Neuropharmacology 76 (Part C):737-746.
27. Li W, Cui Y, Kushner SA, Brown RA, Jentsch JD, Frankland PW, Cannon TD, Silva AJ. 2005. The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr Biol 15:1961-1967.
28. Medrihan L, Tantalaki E, Aramuni G, Sargsyan V, Dudanova I, Missler M, Zhang W. 2008. Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J Neurophysiol 99:112-121.
29. Nelson ED, Kavalali ET, Monteggia LM. 2006. MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr Biol 16:710-716.
30. Nelson ED, Bal M, Kavalali ET, Monteggia LM. 2011. Selective impact of MeCP2 and associated histone deacetylases on the dynamics of evoked excitatory neurotransmission. J Neurophysiol 106:193-201.
31. Nissenkorn A, Gak E, Vecsler M, Reznik H, Menascu S, Ben Zeev B. 2010. Epilepsy in Rett syndrome-The experience of a National Rett Center. Epilepsia 51:1252-1258.
32. Noutel J, Hong YK, Leu B, Kang E, Chen C. 2011. Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron 70:35-42.
33. Ogier M, Wang H, Hong E, Wang Q, Greenberg ME, Katz DM. 2007. Brain-derived neurotrophic factor expression and respiratory function improve after ampakine treatment in a mouse model of Rett syndrome. J Neurosci 27:10912-10917.
34. Pelka GJ, Watson CM, Radziewic T, Hayward M, Lahooti H, Christodoulou J, Tam PP. 2006. Mecp2 deficiency is associated with learning and cognitive deficits and altered gene activity in the hippocampal region of mice. Brain 129:887-898.
35. Pintaudi M, Calevo MG, Vignoli A, Parodi E, Aiello F, Baglietto MG, Hayek Y, Buoni S, Renieri A, Russo S, Cogliati F, Giordano L, Canevini M, Veneselli E. 2010. Epilepsy in Rett syndrome: Clinical and genetic features. Epilepsy Behav 19:296-300.
36. Preibisch S, Saalfeld S, Tomancak P. 2009. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25:1463-1465.
37. Rubenstein JL, Merzenich MM. 2003. Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2:255-267.
38. Rueda N, Florez J, Martinez-Cue C. 2008. Chronic pentylenetetrazole but not donepezil treatment rescues spatial cognition in Ts65Dn mice, a model for Down syndrome. Neurosci Lett 433:22-27.
39. Schmid DA, Yang T, Ogier M, Adams I, Mirakhur Y, Wang Q, Massa SM, Longo FM, Katz DM. 2012. A TrkB small molecule partial agonist rescues TrkB phosphorylation deficits and improves respiratory function in a mouse model of Rett syndrome. J Neurosci 32:1803-1810.
40. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, Paylor R, Zoghbi H. 2002. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35:243-254.
41. Shepherd GM, Katz DM. 2011. Synaptic microcircuit dysfunction in genetic models of neurodevelopmental disorders: Focus on Mecp2 and Met. Curr Opin Neurobiol 21:827-833.
42. Steffenburg U, Hagberg G, Hagberg B. 2001. Epilepsy in a representative series of Rett syndrome. Acta Paediatr 90:34-39.
43. Szabadics J, Soltesz I. 2009. Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J Neurosci 29:4239-4251.
44. Vicario-Abejon C, Owens D, McKay R, Segal M. 2002. Role of neurotrophins in central synapse formation and stabilization. Nat Rev Neurosci 3:965-974.
45. Zhang L, He J, Jugloff DG, Eubanks JH. 2008. The MeCP2-null mouse hippocampus displays altered basal inhibitory rhythms and is prone to hyperexcitability. Hippocampus 18:294-309.
46. Zhang ZW, Zak JD, Liu H. 2010. MeCP2 is required for normal development of GABAergic circuits in the thalamus. J Neurophysiol 103:2470-2481.
47. Zhang W, Peterson M, Beyer B, Frankel WN, Zhang ZW. 2014. Loss of MeCP2 from forebrain excitatory neurons leads to cortical hyperexcitation and seizures. J Neurosci 34:2754-2763.