GABA-A receptor-dependent mechanisms prevent excessive spine elimination during postnatal maturation of the mouse cortex in vivo

FEBS Letters

Volumn 588, Issue 24, 2014, Pages 4551-4560

  Chen, Yachi ^a  

^a Stony Brook University   (United States)

Author keywords

Bicuculline; Cortex; Dendritic spine; Development; GABA A receptor

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; PLACEBO; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN MATURATION; BRAIN REGION; CELL LABELING; CELL LOSS; CELL MATURATION; CELL METABOLISM; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENDRITIC SPINE; DENDRITIC SPINE ELIMINATION; DEVELOPMENTAL STAGE; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE ANALYSIS; IMMUNOELECTRON MICROSCOPY; IN VIVO STUDY; LASER MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR STABILITY; MOUSE; MULTIPHOTON MICROSCOPY; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROMODULATION; NONHUMAN; OPTICAL RESOLUTION; POSTNATAL DEVELOPMENT; POSTSYNAPTIC DENSITY; POSTSYNAPTIC MEMBRANE; PRIMARY SOMATOSENSORY CORTEX; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RECEPTOR BLOCKING; SPATIOTEMPORAL ANALYSIS; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION; TRANSGENIC MOUSE; ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE; METABOLISM; NEWBORN; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; DENDRITIC SPINES; HUMANS; MALE; MICE; MOLECULAR IMAGING; NEOCORTEX; RECEPTORS, GABA-A; SYNAPSES;

EID: 84915731837     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.10.023     Document Type: Article

References (55)

1. V.A. Alvarez, and B.L. Sabatini Anatomical and physiological plasticity of dendritic spines Annu. Rev. Neurosci. 30 2007 79 97
2. M. Bosch, and Y. Hayashi Structural plasticity of dendritic spines Curr. Opin. Neurobiol. 22 2012 383 388
3. Y. Chen, and B.L. Sabatini Signaling in dendritic spines and spine microdomains Curr. Opin. Neurobiol. 22 2012 389 396
4. L.A. Colgan, and R. Yasuda Plasticity of dendritic spines: subcompartmentalization of signaling Annu. Rev. Physiol. 76 2014 365 385
5. A.J. Koleske Molecular mechanisms of dendrite stability Nat. Rev. Neurosci. 14 2013 536 550
6. T.M. Newpher, and M.D. Ehlers Spine microdomains for postsynaptic signaling and plasticity Trends Cell Biol. 19 2009 218 227
7. N.L. Rochefort, and A. Konnerth Dendritic spines: from structure to in vivo function EMBO Rep. 13 2012 699 708
8. R. Yuste Dendritic spines and distributed circuits Neuron 71 2011 772 781
9. S.B. Hofer, T.D. Mrsic-Flogel, T. Bonhoeffer, and M. Hubener Experience leaves a lasting structural trace in cortical circuits Nature 457 2009 313 317
10. A. Holtmaat, and K. Svoboda Experience-dependent structural synaptic plasticity in the mammalian brain Nat. Rev. Neurosci. 10 2009 647 658
11. A. Holtmaat, L. Wilbrecht, G.W. Knott, E. Welker, and K. Svoboda Experience-dependent and cell-type-specific spine growth in the neocortex Nature 441 2006 979 983
12. H. Kasai, M. Fukuda, S. Watanabe, A. Hayashi-Takagi, and J. Noguchi Structural dynamics of dendritic spines in memory and cognition Trends Neurosci. 33 2010 121 129
13. J.T. Trachtenberg Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex Nature 420 2002 788 794
14. T. Xu, X. Yu, A.J. Perlik, W.F. Tobin, J.A. Zweig, K. Tennant, T. Jones, and Y. Zuo Rapid formation and selective stabilization of synapses for enduring motor memories Nature 462 2009 915 919
15. Y. Zuo, G. Yang, E. Kwon, and W.B. Gan Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex Nature 436 2005 261 265
16. B. Anderson, and V. Rutledge Age and hemisphere effects on dendritic structure Brain 119 Pt 6 1996 1983 1990
17. B. Jacobs, L. Driscoll, and M. Schall Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study J. Comp. Neurol. 386 1997 661 680
18. Z. Petanjek, M. Judas, G. Simic, M.R. Rasin, H.B. Uylings, P. Rakic, and I. Kostovic Extraordinary neoteny of synaptic spines in the human prefrontal cortex Proc. Natl. Acad. Sci. U.S.A. 108 2011 13281 13286
19. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation Nature 397 1999 251 255
20. - uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1 J. Physiol. 557 2004 829 841
21. G. Barbin, H. Pollard, J.L. Gaiarsa, and Y. Ben-Ari Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons Neurosci. Lett. 152 1993 150 154
22. L. Cancedda, H. Fiumelli, K. Chen, and M.M. Poo Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo J. Neurosci. 27 2007 5224 5235
23. N. Heck, W. Kilb, P. Reiprich, H. Kubota, T. Furukawa, A. Fukuda, and H.J. Luhmann GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo Cereb. Cortex 17 2007 138 148
24. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298
25. D.D. Wang, and A.R. Kriegstein GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation J. Neurosci. 28 2008 5547 5558
26. M. Farrant, and Z. Nusser Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors Nat. Rev. Neurosci. 6 2005 215 229
27. J. Glykys, and I. Mody Activation of GABAA receptors: views from outside the synaptic cleft Neuron 56 2007 763 770
28. H. Mohler GABA(A) receptor diversity and pharmacology Cell Tissue Res. 326 2006 505 516
29. S.R. Cobb, E.H. Buhl, K. Halasy, O. Paulsen, and P. Somogyi Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons Nature 378 1995 75 78
30. F. Pouille, and M. Scanziani Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition Science 293 2001 1159 1163
31. D. Belelli, N.L. Harrison, J. Maguire, R.L. Macdonald, M.C. Walker, and D.W. Cope Extrasynaptic GABAA receptors: form, pharmacology, and function J. Neurosci. 29 2009 12757 12763
32. S.G. Brickley, and I. Mody Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease Neuron 73 2012 23 34
33. S. Pirker, C. Schwarzer, A. Wieselthaler, W. Sieghart, and G. Sperk GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain Neuroscience 101 2000 815 850
34. R.N. Fernando, B. Eleuteri, S. Abdelhady, A. Nussenzweig, M. Andang, and P. Ernfors Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells Proc. Natl. Acad. Sci. U.S.A. 108 2011 5837 5842
35. L. Nguyen, B. Malgrange, I. Breuskin, L. Bettendorff, G. Moonen, S. Belachew, and J.M. Rigo Autocrine/paracrine activation of the GABA(A) receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum J. Neurosci. 23 2003 3278 3294
36. C. Fuchs, K. Abitbol, J.J. Burden, A. Mercer, L. Brown, J. Iball, F. Anne Stephenson, A.M. Thomson, and J.N. Jovanovic GABA(A) receptors can initiate the formation of functional inhibitory GABAergic synapses Eur. J. Neurosci. 38 2013 3146 3158
37. Z.J. Huang, and P. Scheiffele GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development Curr. Opin. Neurobiol. 18 2008 77 83
38. C.Q. Chiu, G. Lur, T.M. Morse, N.T. Carnevale, G.C. Ellis-Davies, and M.J. Higley Compartmentalization of GABAergic inhibition by dendritic spines Science 340 2013 759 762
39. C. Beaulieu, and M. Colonnier A laminar analysis of the number of round-asymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat J. Comp. Neurol. 231 1985 180 189
40. J.L. Chen, K.L. Villa, J.W. Cha, P.T. So, Y. Kubota, and E. Nedivi Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex Neuron 74 2012 361 373
41. K. Flurkey, J.M. Currer, and D.E. Harrison The mouse in aging research J.G. Fox, S.W. Barthold, M.T. Davisson, C.E. Newcomer, F.W. Quimby, A.L. Smith, The Mouse in Biomedical Research 2007 Elsevier Burlington, MA 637 642
42. T. Keck, T.D. Mrsic-Flogel, M. Vaz Afonso, U.T. Eysel, T. Bonhoeffer, and M. Hubener Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex Nat. Neurosci. 11 2008 1162 1167
43. T.C. Jacob, Q. Wan, M. Vithlani, R.S. Saliba, F. Succol, M.N. Pangalos, and S.J. Moss GABA(A) receptor membrane trafficking regulates spine maturity Proc. Natl. Acad. Sci. U.S.A. 106 2009 12500 12505
44. K. Heinen, R.E. Baker, S. Spijker, T. Rosahl, J. van Pelt, and A.B. Brussaard Impaired dendritic spine maturation in GABAA receptor alpha1 subunit knockout mice Neuroscience 122 2003 699 705
45. U.V. Nagerl, N. Eberhorn, S.B. Cambridge, and T. Bonhoeffer Bidirectional activity-dependent morphological plasticity in hippocampal neurons Neuron 44 2004 759 767
46. Q. Zhou, K.J. Homma, and M.M. Poo Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses Neuron 44 2004 749 757
47. Z.W. Zhang, M. Peterson, and H. Liu Essential role of postsynaptic NMDA receptors in developmental refinement of excitatory synapses Proc. Natl. Acad. Sci. U.S.A. 110 2013 1095 1100
48. E.R. Korpi, and S.T. Sinkkonen GABA(A) receptor subtypes as targets for neuropsychiatric drug development Pharmacol. Ther. 109 2006 12 32
49. H. Mohler Molecular regulation of cognitive functions and developmental plasticity: impact of GABAA receptors J. Neurochem. 102 2007 1 12
50. U. Rudolph, and F. Knoflach Beyond classical benzodiazepines: novel therapeutic potential of GABAA receptor subtypes Nat. Rev. Drug Discov. 10 2012 685 697
51. G. Feng Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP Neuron 28 2000 41 51
52. F.W. Grillo Increased axonal bouton dynamics in the aging mouse cortex Proc. Natl. Acad. Sci. U.S.A. 110 2013 E1514 E1523
53. M. De Roo, P. Klauser, A. Briner, I. Nikonenko, P. Mendez, A. Dayer, J.Z. Kiss, D. Muller, and L. Vutskits Anesthetics rapidly promote synaptogenesis during a critical period of brain development PLoS One 4 2009 e7043
54. G. Yang, P.C. Chang, A. Bekker, T.J. Blanck, and W.B. Gan Transient effects of anesthetics on dendritic spines and filopodia in the living mouse cortex Anesthesiology 115 2011 718 726
55. J. Grutzendler, N. Kasthuri, and W.-B. Gan Long-term dendritic spine stability in the adult cortex Nature 420 2002 812 816