Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome

Journal of Neurophysiology

Volumn 99, Issue 1, 2008, Pages 112-121

  Medrihan, L ^a   Tantalaki, E ^a   Aramuni, G ^a   Sargsyan, V ^a   Dudanova, I ^a,b   Missler, M ^a,b   Zhang, W ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; METHYL CPG BINDING PROTEIN 2;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ARTICLE; BRAIN STEM; CONTROLLED STUDY; FEMALE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; MALE; MEDULLA OBLONGATA; MOUSE; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RETT SYNDROME; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN STEM; DISEASE MODELS, ANIMAL; EFFERENT PATHWAYS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENETIC PREDISPOSITION TO DISEASE; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RESPIRATORY CENTER; RETICULAR FORMATION; RETT SYNDROME; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 38349055166     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00826.2007     Document Type: Article

References (57)

1. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23: 185-188, 1999.
2. Asaka Y, Jugloff DG, Zhang L, Eubanks JH, Fitzsimonds RM. Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21: 217-227, 2006.
3. Baumann SW, Baur R, Sigel E. Subunit arrangement of gamma-aminobutyric acid type A receptors. J Biol Chem 276: 36275-36280, 2001.
4. Bosman LW, Rosahl TW, Brussaard AB. Neonatal development of the rat visual cortex: synaptic function of GABAA receptor alpha subunits. J Physiol 545: 169-181, 2002.
5. Brunig I, Scotti E, Sidler C, Fritschy JM. Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443: 43-55, 2002.
6. Carrasco MA, Castro P, Sepulveda FJ, Tapia JC, Gatica K, Davis MI, Aguayo LG. Regulation of glycinergic and GABAergic synaptogenesis by brain-derived neurotrophic factor in developing spinal neurons. Neuroscience 145: 484-494, 2007.
7. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49: 341-348, 2006.
8. Chao HT, Zoghbi HY, Rosenmund C. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56: 58-65, 2007.
9. Chen RZ, Akbarian S, Tudor M, Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27: 327-331, 2001.
10. Cohen DR, Matarazzo V, Palmer AM, Tu Y, Jeon OH, Pevsner J, Ronnett GV. Expression of MeCP2 in olfactory receptor neurons is developmentally regulated and occurs before synaptogenesis. Mol Cell Neurosci 22: 417-429, 2003.
11. Cruz DA, Eggan SM, Lewis DA. Postnatal development of pre- and postsynaptic GABA markers at chandelier cell connections with pyramidal neurons in monkey prefrontal cortex. J Comp Neurol 465: 385-400, 2003.
12. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. 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, 2005.
13. Einspieler C, Kerr AM, Prechtl HF. Abnormal general movements in girls with Rett disorder: the first four months of life. Brain Dev 27, Suppl. 1: S8-S13, 2005a.
14. Einspieler C, Kerr AM, Prechtl HF. Is the early development of girls with Rett disorder really normal? Pediatr Res 57: 696-700, 2005b.
15. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229, 2005.
16. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
17. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1997.
18. Fritschy JM, Paysan J, Enna A, Mohler H. Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study. J Neurosci 14: 5302-5324, 1994.
19. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27: 322-326, 2001.
20. Hanefeld F, Hanefeld U, Wilichowski E, Schmidtke J. Rett syndrome - search for genetic markers. Am J Med Genet Suppl 1: 377-382, 1986.
21. Johnston MV, Jeon OH, Pevsner J, Blue ME, Naidu S. Neurobiology of Rett syndrome: a genetic disorder of synapse development. Brain Dev 23, Suppl. 1: S206-S213, 2001.
22. Jonas P, Bischofberger J, Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424, 1998.
23. Kerr AM, Burford B. Towards a full life with Rett disorder. Pediatr Rehabil 4: 155-168, 2001.
24. Kozinetz CA, Skender ML, MacNaughton N, Almes MJ, Schultz RJ, Percy AK, Glaze DG. Epidemiology of Rett syndrome: a population-based registry. Pediatrics 91: 445-450, 1993.
25. Laurie DJ, Wisden W, Seeburg PH. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12: 4151-4172, 1992.
26. Liu Q, Wong-Riley MT. Developmental changes in the expression of GABAA receptor subunits alpha1, alpha2, and alpha3 in the rat pre-Botzinger complex. J Appl Physiol 96: 1825-1831, 2004.
27. Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, Rudolph U. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290: 131-134, 2000.
28. Marty S, Wehrle R, Sotelo C. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 20: 8087-8095, 2000.
29. McClellan AM, Twyman RE. Receptor system response kinetics reveal functional subtypes of native murine and recombinant human GABAA receptors. J Physiol 515: 711-727, 1999.
30. 2+ channels to synaptic vesicle exocytosis. Nature 423: 939-948, 2003.
31. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, Arancio O, Sweatt JD, Zoghbi HY. Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26: 319-327, 2006.
32. Mullaney BC, Johnston MV, Blue ME. Developmental expression of methyl-CpG binding protein 2 is dynamically regulated in the rodent brain. Neuroscience 123: 939-949, 2004.
33. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7: 17-23, 2004.
34. Nelson ED, Kavalali ET, Monteggia LM. MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr Biol 16: 710-716, 2006.
35. Nomura Y. Early behavior characteristics and sleep disturbance in Rett syndrome. Brain Dev 27, Suppl. 1: S35-S42, 2005.
36. Okada M, Onodera K, Van Renterghem C, Sieghart W, Takahashi T. Functional correlation of GABA(A) receptor alpha subunits expression with the properties of IPSCs in the developing thalamus. J Neurosci 20: 2202-2208, 2000.
37. Perrais D, Ropert N. Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses. J Neurosci 19: 578-588, 1999.
38. Picker JD, Yang R, Ricceri L, Berger-Sweeney J. An altered neonatal behavioral phenotype in Mecp2 mutant mice. Neuroreport 17: 541-544, 2006.
39. Richter DW, Spyer KM. Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci 24: 464-472, 2001.
40. Ritter B, Zhang W. Early postnatal maturation of GABAA-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur J Neurosci 12: 2975-2984, 2000.
41. Rosenmund C, Stevens CF. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207, 1996.
42. Rudolph U, Mohler H. Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44: 475-498, 2004.
43. Samaco RC, Hogart A, LaSalle JM. Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Hum Mol Genet 14: 483-492, 2005.
44. Santos M, Silva-Fernandes A, Oliveira P, Sousa N, Maciel P. Evidence for abnormal early development in a mouse model of Rett syndrome. Genes Brain Behav 6: 277-286, 2007.
45. Shahbazian MD, Antalffy B, Armstrong DL, Zoghbi HY. Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum Mol Genet 11: 115-124, 2002.
46. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
47. Stettner GM, Huppke P, Brendel C, Richter DW, Gartner J, Dutschmann M. Breathing dysfunctions associated with impaired control of postinspiratory activity in Mecp2-/y knockout mice. J Physiol 579: 863-876, 2007.
48. Thoby-Brisson M, Cauli B, Champagnat J, Fortin G, Katz DM. Expression of functional tyrosine kinase B receptors by rhythmically active respiratory neurons in the pre-Botzinger complex of neonatal mice. J Neurosci 23: 7685-7689, 2003.
49. Trevarthen C, Daniel S. Disorganized rhythm and synchrony: early signs of autism and Rett syndrome. Brain Dev 27, Suppl. 1: S25-S34, 2005.
50. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Sudhof TC, Brose N. Neuroligins determine synapse maturation and function. Neuron 51: 741-754, 2006.
51. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79: 555-566, 1998.
52. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Pena F, Zanella S, Bevengut M, Barthelemy-Requin M, Herzing LB, Moncla A, Mancini J, Ramirez JM, Villard L, Hilaire G. Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J Neurosci 25: 11521-11530, 2005.
53. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50: 575-587, 2006.
54. Yamada MK, Nakanishi K, Ohba S, Nakamura T, Ikegaya Y, Nishiyama N, Matsuki N. Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J Neurosci 22: 7580-7585, 2002.
55. Yamashita Y, Matsuishi T, Ishibashi M, Kimura A, Onishi Y, Yonekura Y, Kato H. Decrease in benzodiazepine receptor binding in the brains of adult patients with Rett syndrome. J Neurol Sci 154: 146-150, 1998.
56. 2+ channels. J Neurosci 25: 4330-4342, 2005.
57. Zoghbi HY. Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302: 826-830, 2003.