Synaptic Competition Sculpts the Development of GABAergic Axo-Dendritic but Not Perisomatic Synapses

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Frola, Elena ^a   Patrizi, Annarita ^a,d   Goetz, Thomas ^b,e   Medrihan, Lucian ^c   Petrini, Enrica Maria ^c   Barberis, Andrea ^c   Wulff, Peer ^b   Wisden, William ^b,f   Sassoè Pognetto, Marco ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; NEUROLIGIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; EMBRYO; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GABRG2 GENE; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC MANIPULATION; GROWTH REGULATION; INNERVATION; INTRACELLULAR SPACE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVOUS SYSTEM FUNCTION; NEUROMODULATION; NONHUMAN; PROTEIN LOCALIZATION; PURKINJE CELL; PYRAMIDAL NERVE CELL; SYNAPTIC COMPETITION; SYNAPTIC INHIBITION;

ANIMALS; AXONS; CELL ADHESION MOLECULES, NEURONAL; DENDRITES; GAMMA-AMINOBUTYRIC ACID; GENE KNOCKDOWN TECHNIQUES; MICE; NERVE TISSUE PROTEINS; PURKINJE CELLS; RECEPTORS, GABA-A; SYNAPSES;

EID: 84874002732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056311     Document Type: Article

References (90)

1. Lichtman JW, Colman H, (2000) Synapse elimination and indelible memory. Neuron 25: 269-278.
2. Cohen-Cory S, (2002) The developing synapse: construction and modulation of synaptic structures and circuits. Science 298: 770-776.
3. Flavell SW, Greenberg ME, (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31: 563-590.
4. Kerschensteiner D, Morgan JL, Parker ED, Lewis RM, Wong RO, (2009) Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 460: 1016-1020.
5. Bosman LW, Takechi H, Hartmann J, Eilers J, Konnerth A, (2008) Homosynaptic long-term synaptic potentiation of the "winner" climbing fiber synapse in developing Purkinje cells. J Neurosci 28: 798-807.
6. Ohtsuki G, Hirano T, (2008) Bidirectional plasticity at developing climbing fiber-Purkinje neuron synapses. Eur J Neurosci 28: 2393-2400.
7. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M, (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63: 106-118.
8. Südhof TC, Malenka RC, (2008) Understanding synapses: past, present, and future. Neuron 60: 469-476.
9. Somogyi P, Tamás G, Lujan R, Buhl EH, (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res Rev 26: 113-135.
10. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
11. Burkhalter A, (2008) Many specialists for suppressing cortical excitation. Front Neurosci 2: 155-167.
12. Huang ZJ, (2006) Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules. Nat Neurosci 9: 163-166.
13. Shen K, Scheiffele P, (2010) Genetics and cell biology of building specific synaptic connectivity. Annu Rev Neurosci 33: 473-507.
14. Akerman CJ, Cline HT, (2007) Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci 30: 382-389.
15. Huang ZJ, Scheiffele P, (2008) GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr Opin Neurobiol 18: 77-83.
16. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, et al. (2007) GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54: 889-903.
17. Fritschy JM, Panzanelli P, Kralic JE, Vogt K, Sassoè-Pognetto M, (2006) Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the α1 subunit in Purkinje cells. J Neurosci 26: 3245-3255.
18. Patrizi A, Scelfo B, Viltono L, Briatore F, Fukaya M, et al. (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci USA 105: 13151-13156.
19. Günther U, Benson J, Benke D, Fritschy JM, Reyes G, et al. (1995) Benzodiazepine-insensitive mice generated by targeted disruption of the γ2 subunit gene of γ-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 92: 7749-7753.
20. Mu W, Burt DR, (1999) Transcriptional regulation of GABAA receptor gamma2 subunit gene. Mol Brain Res 67: 137-147.
21. Cope DW, Wulff P, Oberto A, Aller MI, Capogna M, et al. (2004) Abolition of zolpidem sensitivity in mice with a point mutation in the GABAA receptor gamma2 subunit. Neuropharmacology 47: 17-34.
22. Wisden W, Morris BJ (1994) In situ hybridization with synthetic oligonucleotide probes. In: Wisden W, Morris BJ eds. In Situ Hybridization Protocols for the Brain- The Biological Techniques Series. Academic Press. pp 9-34.
23. Gao B, Fritschy JM, Benke D, Mohler H, (1993) Neuron-specific expression of GABAA-receptor subtypes: differential association of the α1- and α3-subunits with serotonergic and GABAergic neurons. Neuroscience 54: 881-892.
24. Benke D, Honer M, Michel C, Mohler H, (1996) GABAA receptor subtypes differentiated by their γ-subunit variants: prevalence, pharmacology and subunit architecture. Neuropharmacology 35: 1413-1423.
25. Kralic JE, Sidler C, Parpan F, Homanics GE, Morrow AL, et al. (2006) Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495: 408-421.
26. Varoqueaux F, Jamain S, Brose N, (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83: 449-456.
27. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP, (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345: 315-319.
28. Lévi S, Grady RM, Henry MD, Campbell KP, Sanes JR, et al. (2002) Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22: 4274-4285.
29. Celio M, (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475.
30. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, et al. (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94: 1488-1493.
31. Huesa G, Yáñez J, Anadón R, (2002) Calbindin and calretinin immunoreactivities in the retina of a chondrostean, Acipenser baeri. Cell Tissue Res 309: 355-360.
32. Celio MR, Baier W, Schärer L, de Viragh PA, Gerday C, (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9: 81-86.
33. Bu J, Sathyendra V, Nagykery N, Geula C, (2003) Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp Neurol 182: 220-231.
34. Chang YC, Gottlieb DI, (1988) Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J Neurosci 8: 2123-2130.
35. Butler MH, Solimena M, Dirkx R Jr, Hayday A, De Camilli P, (1993) Identification of a dominant epitope of glutamic acid decarboxylase (GAD-65) recognized by autoantibodies in stiff-man syndrome. J Exp Med 178: 2097-2106.
36. Kim J, Richter W, Aanstoot HJ, Shi Y, Fu Q, et al. (1993) Differential expression of GAD65 and GAD67 in human, rat, and mouse pancreatic islets. Diabetes 42: 799-1808.
37. Tanaka J, Nakagawa S, Kushiya E, Yamasaki M, Fukaya M, et al. (2000) Gq protein alpha subunits Galphaq and Galpha11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12: 781-792.
38. Ferraguti F, Cobden P, Pollard M, Cope D, Shigemoto R, et al. (2004) Immunolocalization of metabotropic glutamate receptor 1alpha (mGluR1alpha) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus 14: 193-215.
39. Goldstein ME, Sternberger LA, Sternberger NH, (1983) Microheterogeneity ("neurotypy") of neurofilament proteins. Proc Natl Acad Sci USA 80: 3101-3105.
40. Cipelletti B, Avanzini G, Vitellaro-Zuccarello L, Franceschetti S, Sancini G, et al. (2002) Morphological organization of somatosensory cortex in Otx1-/- mice. Neuroscience 115: 657-667.
41. Garbelli R, Inverardi F, Medici V, Amadeo A, Verderio C, et al. (2008) Heterogeneous expression of SNAP-25 in rat and human brain. J Comp Neurol 506: 373-386.
42. Viltono L, Patrizi A, Fritschy JM, Sassoè-Pognetto M, (2008) Synaptogenesis in the cerebellar cortex: Differential regulation of gephyrin and GABAA receptors at somatic and dendritic synapses of Purkinje cells. J Comp Neurol 508: 579-591.
43. D'Angelo E, De Filippi G, Rossi P, Taglietti V, (1998) Ionic mechanism of electroresponsiveness in cerebellar granule cells implicates the action of a persistent sodium current. J Neurophysiol 80: 493-503.
44. Wulff P, Goetz T, Leppä E, Linden AM, Renzi M, et al. (2007) From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors. Nat Neurosci 10: 923-929.
45. Laurie DJ, Wisden W, Seeburg PH, (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12: 4151-4172.
46. Essrich C, Lorez M, Benson JA, Fritschy JM, Lüscher B, (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the γ2 subunit and gephyrin. Nature Neurosci 1: 563-571.
47. Schweizer C, Balsiger S, Bluethmann H, Mansuy IM, Fritschy JM, et al. (2003) The γ2 subunit of GABAA receptors is required for maintenance of receptors at mature synapses. Mol Cell Neurosci 24: 442-450.
48. Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, et al. (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci USA 106: 3561-3566.
49. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoè-Pognetto M, et al. (2009) Role of GABAergic interneurons in cerebellar motor learning. Nat Neurosci 12: 1042-1049.
50. Luscher B, Fuchs T, Kilpatrick CL, (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70: 385-409.
51. Briatore F, Patrizi A, Viltono L, Sassoè-Pognetto M, Wulff P, (2010) Quantitative organization of GABAergic synapses in the molecular layer of the mouse cerebellar cortex. PLoS One 5: e12119.
52. Lorez M, Benke D, Luscher B, Mohler H, Benson JA, (2000) Single-channel properties of neuronal GABAA receptors from mice lacking the γ2 subunit. J Physiol 527: 11-31.
53. Alldred MJ, Mulder-Rosi J, Lingenfelter SE, Chen G, Luscher B, (2005) Distinct γ2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J Neurosci 25: 594-603.
54. Leppä E, Linden AM, Rabe H, Vekovischeva OY, Wulff P, et al. (2011) Actions of two GABAA receptor benzodiazepine-site ligands that are mediated via non- γ2-dependent modulation. Eur J Pharmacol 666: 111-121.
55. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR, (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15: 1287-1298.
56. Behar TN, Schaffner AE, Scott CA, Greene CL, Barker JL, (2000) GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex 10: 899-909.
57. Haydar TF, Wang F, Schwartz ML, Rakic P, (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20: 5764-5774.
58. Liu X, Wang Q, Haydar TF, Bordey A, (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 8: 1179-1187.
59. Heck N, Kilb W, Reiprich P, Kubota H, Furukawa T, et al. (2007) GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex 17: 138-148.
60. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, et al. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-93.
61. Represa A, Ben-Ari Y, (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28: 278-283.
62. Wang DD, Kriegstein AR, (2009) Defining the role of GABA in cortical development. J Physiol 587: 1873-1879.
63. Homanics GE, DeLorey TM, Firestone LL, Quinlan JJ, Handforth A, et al. (1997) Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci USA 94: 4143-4148.
64. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, et al. (1997) Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94: 14060-14065.
65. Ji F, Kanbara N, Obata K, (1999) GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase. Neurosci Res 33: 187-194.
66. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, et al. (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50: 575-587.
67. Hensch TK, (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6: 877-888.
68. Freund TF, Katona I, (2007) Perisomatic inhibition. Neuron 56: 33-42.
69. Klausberger T, Somogyi P, (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321: 53-57.
70. Sohal VS, Zhang F, Yizhar O, Deisseroth K, (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702.
71. Yuan X, Yao J, Norris D, Tran DD, Bram RJ, et al. (2008) Calcium-modulating cyclophilin ligand regulates membrane trafficking of postsynaptic GABA(A) receptors. Mol Cell Neurosci 38: 277-289.
72. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, et al. (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54: 919-931.
73. Panzanelli P, Gunn BG, Schlatter MC, Benke D, Tyagarajan SK, et al. (2011) Distinct mechanisms regulate GABAA receptor and gephyrin clustering at perisomatic and axo-axonic synapses on CA1 pyramidal cells. J Physiol 589: 4959-4980.
74. Gibson JR, Huber KM, Südhof TC, (2009) Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. J Neurosci 29: 13883-13897.
75. Hoon M, Bauer G, Fritschy JM, Moser T, Falkenburger BH, et al. (2009) Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J Neurosci 29: 8039-8050.
76. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, et al. (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63: 628-642.
77. Jedlicka P, Hoon M, Papadopoulos T, Vlachos A, Winkels R, et al. (2011) Increased dentate gyrus excitability in neuroligin-2-deficient mice in vivo. Cereb Cortex 21: 357-367.
78. Sassoè-Pognetto M, Frola E, Pregno G, Briatore F, Patrizi A, (2011) Understanding the molecular diversity of GABAergic synapses. Front Cell Neurosci 5: 4.
79. Li RW, Yu W, Christie S, Miralles CP, Bai J, et al. (2005) Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J Neurochem 95: 756-770.
80. Fang C, Deng L, Keller CA, Fukata M, Fukata Y, et al. (2006) GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J Neurosci 26: 12758-12768.
81. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P, (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-78.
82. Halasy K, Buhl EH, Lörinczi Z, Tamás G, Somogyi P, (1996) Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6: 306-329.
83. Tamás G, Szabadics J, Lörincz A, Somogyi P, (2004) Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur J Neurosci 20: 2681-2690.
84. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF, (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815-823.
85. Tamás G, Buhl EH, Somogyi P, (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500: 715-738.
86. Pouille F, Scanziani M, (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429: 717-723.
87. Trigo FF, Bouhours B, Rostaing P, Papageorgiou G, Corrie JE, et al. (2010) Presynaptic miniature GABAergic currents in developing interneurons. Neuron 66: 235-247.
88. Burke SN, Barnes CA, (2010) Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 33: 153-161.
89. Cossart R, Bernard C, Ben-Ari Y, (2005) Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28: 108-115.
90. Marchionni I, Maccaferri G, (2009) Quantitative dynamics and spatial profile of perisomatic GABAergic input during epileptiform synchronization in the CA1 hippocampus. J Physiol 587: 5691-5708.