From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors (original) (raw)

• Riedel, G. et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat. Neurosci. 2, 898–905 (1999).
  Article CAS Google Scholar
• Lomber, S.G. The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function. J. Neurosci. Methods 86, 109–117 (1999).
  Article CAS Google Scholar
• Pereira de Vasconcelos, A. et al. Reversible inactivation of the dorsal hippocampus by tetrodotoxin or lidocaine: a comparative study on cerebral functional activity and motor coordination in the rat. Neuroscience 141, 1649–1663 (2006).
  Article CAS Google Scholar
• Wulff, P. & Wisden, W. Dissecting neural circuitry by combining genetics and pharmacology. Trends Neurosci. 28, 44–50 (2005).
  Article CAS Google Scholar
• Crick, F. The impact of molecular biology on neuroscience. Phil. Trans. R. Soc. Lond. B 354, 2021–2025 (1999).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Farrant, M. & Nusser, Z. Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat. Rev. Neurosci. 6, 215–229 (2005).
  Article CAS Google Scholar
• Whiting, P.J. GABAA receptors: a viable target for novel anxiolytics? Curr. Opin. Pharmacol. 6, 24–29 (2006).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Thomson, A.M., Bannister, A.P., Hughes, D.I. & Pawelzik, H. Differential sensitivity to Zolpidem of IPSPs activated by morphologically identified CA1 interneurons in slices of rat hippocampus. Eur. J. Neurosci. 12, 425–436 (2000).
  Article CAS Google Scholar
• Campo-Soria, C., Chang, Y. & Weiss, D.S. Mechanism of action of benzodiazepines on GABAA receptors. Br. J. Pharmacol. 148, 984–990 (2006).
  Article CAS Google Scholar
• Rudolph, U. et al. Benzodiazepine actions mediated by specific γ-aminobutyric acidA receptor subtypes. Nature 401, 796–800 (1999).
  Article CAS Google Scholar
• Crestani, F., Martin, J.R., Mohler, H. & Rudolph, U. Mechanism of action of the hypnotic zolpidem in vivo. Br. J. Pharmacol. 131, 1251–1254 (2000).
  Article CAS Google Scholar
• Crestani, F., Martin, J.R., Mohler, H. & Rudolph, U. Resolving differences in GABAA receptor mutant mouse studies. Nat. Neurosci. 3, 1059 (2000).
  Article CAS Google Scholar
• McKernan, R.M. et al. Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABAA receptor α1 subtype. Nat. Neurosci. 3, 587–592 (2000).
  Article CAS Google Scholar
• Wisden, W., Laurie, D.J., Monyer, H. & Seeburg, P.H. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J. Neurosci. 12, 1040–1062 (1992).
  Article CAS Google Scholar
• Duncan, G.E. et al. Distribution of [3H]zolpidem binding sites in relation to messenger RNA encoding the α1, β2 and γ2 subunits of GABAA receptors in rat brain. Neuroscience 64, 1113–1128 (1995).
  Article CAS Google Scholar
• Niddam, R., Dubois, A., Scatton, B., Arbilla, S. & Langer, S.Z. Autoradiographic localization of [3H]zolpidem binding sites in the rat CNS: comparison with the distribution of [3H]flunitrazepam binding sites. J. Neurochem. 49, 890–899 (1987).
  Article CAS Google Scholar
• Sancar, F., Ericksen, S.S., Kucken, A.M., Teissere, J.A. & Czajkowski, C. Structural determinants for high-affinity zolpidem binding to GABAA receptors. Mol. Pharmacol. 71, 38–46 (2007).
  Article CAS Google Scholar
• Buhr, A., Baur, R. & Sigel, E. Subtle changes in residue 77 of the γ subunit of α1β2γ2 GABAA receptors drastically alter the affinity for ligands of the benzodiazepine binding site. J. Biol. Chem. 272, 11799–11804 (1997).
  Article CAS Google Scholar
• Wingrove, P.B., Thompson, S.A., Wafford, K.A. & Whiting, P.J. Key amino acids in the γ subunit of the γ-aminobutyric acidA receptor that determine ligand binding and modulation at the benzodiazepine site. Mol. Pharmacol. 52, 874–881 (1997).
  Article CAS Google Scholar
• Cope, D.W. et al. Abolition of zolpidem sensitivity in mice with a point mutation in the GABAA receptor γ2 subunit. Neuropharmacology 47, 17–34 (2004).
  Article CAS Google Scholar
• Cope, D.W. et al. Loss of zolpidem efficacy in the hippocampus of mice with the GABAA receptor γ2 F77I point mutation. Eur. J. Neurosci. 21, 3002–3016 (2005).
  Article CAS Google Scholar
• Ogris, W. et al. Affinity of various benzodiazepine site ligands in mice with a point mutation in the GABAA receptor γ2 subunit. Biochem. Pharmacol. 68, 1621–1629 (2004).
  Article CAS Google Scholar
• Smeyne, R.J. et al. Local control of granule cell generation by cerebellar Purkinje cells. Mol. Cell. Neurosci. 6, 230–251 (1995).
  Article CAS Google Scholar
• Häusser, M. & Clark, B.A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665–678 (1997).
  Article Google Scholar
• Mittmann, W., Koch, U. & Häusser, M. Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J. Physiol. (Lond.) 563, 369–378 (2005).
  Article CAS Google Scholar
• Santamaria, F., Tripp, P.G. & Bower, J.M. Feed-forward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J. Neurophysiol. 97, 248–263 (2007).
  Article Google Scholar
• Laurie, D.J., Seeburg, P.H. & Wisden, W. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J. Neurosci. 12, 1063–1076 (1992).
  Article CAS Google Scholar
• Fritschy, J.M., Panzanelli, P., Kralic, J.E., Vogt, K.E. & Sassoe-Pognetto, M. 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 (2006).
  Article CAS Google Scholar
• Gunther, U. et al. 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 (1995).
  Article CAS Google Scholar
• Schweizer, C. et al. The γ2 subunit of GABAA receptors is required for maintenance of receptors at mature synapses. Mol. Cell. Neurosci. 24, 442–450 (2003).
  Article CAS Google Scholar
• Barski, J.J., Dethleffsen, K. & Meyer, M. Cre recombinase expression in cerebellar Purkinje cells. Genesis 28, 93–98 (2000).
  Article CAS Google Scholar
• Kittler, J.T. et al. Analysis of GABAA receptor assembly in mammalian cell lines and hippocampal neurons using γ2 subunit green fluorescent protein chimeras. Mol. Cell. Neurosci. 16, 440–452 (2000).
  Article CAS Google Scholar
• Brickley, S.G., Revilla, V., Cull-Candy, S.G., Wisden, W. & Farrant, M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88–92 (2001).
  Article CAS Google Scholar
• Marder, E. & Goaillard, J.M. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7, 563–574 (2006).
  Article CAS Google Scholar
• Lima, S.Q. & Miesenbock, G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121, 141–152 (2005).
  Article CAS Google Scholar
• Zhang, F. et al. Multimodal fast optical interrogation of neural circuitry. Nature 446, 633–641 (2007).
  Article CAS Google Scholar
• Gosgnach, S. et al. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440, 215–219 (2006).
  Article CAS Google Scholar
• Tan, E.M. et al. Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. Neuron 51, 157–170 (2006).
  Article CAS Google Scholar
• Karpova, A.Y., Tervo, D.G., Gray, N.W. & Svoboda, K. Rapid and reversible chemical inactivation of synaptic transmission in genetically targeted neurons. Neuron 48, 727–735 (2005).
  Article CAS Google Scholar
• Yamamoto, M. et al. Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J. Neurosci. 23, 6759–6767 (2003).
  Article CAS Google Scholar
• Wall, M.J. & Usowicz, M.M. Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur. J. Neurosci. 9, 533–548 (1997).
  Article CAS Google Scholar
• McCartney, M.R., Deeb, T.Z., Henderson, T.N. & Hales, T.G. Tonically active GABAA receptors in hippocampal pyramidal neurons exhibit constitutive GABA-independent gating. Mol. Pharmacol. 71, 539–548 (2007).
  Article CAS Google Scholar
• Benavides, J. et al. In vivo interaction of zolpidem with central benzodiazepine (BZD) binding sites (as labeled by [3H]Ro 15–1788) in the mouse brain. Preferential affinity of zolpidem for the omega 1 (BZD1) subtype. J. Pharmacol. Exp. Ther. 245, 1033–1041 (1988).
  CAS PubMed Google Scholar
• Leppa, E. et al. Agonistic effects of the β-carboline DMCM revealed in GABAA receptor γ2 subunit F77I point-mutated mice. Neuropharmacology 48, 469–478 (2005).
  Article CAS Google Scholar
• Lein, E.S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168–176 (2007).
  Article CAS Google Scholar
• Zezula, J., Fuchs, K. & Sieghart, W. Separation of α1, α2 and α3 subunits of the GABAA-benzodiazepine receptor complex by immunoaffinity chromatography. Brain Res. 563, 325–328 (1991).
  Article CAS Google Scholar
• Oertel, W.H., Schmechel, D.E., Mugnaini, E., Tappaz, M.L. & Kopin, I.J. Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience 6, 2715–2735 (1981).
  Article CAS Google Scholar
• Korpi, E.R. et al. Cerebellar granule-cell–specific GABAA receptors attenuate benzodiazepine-induced ataxia: evidence from α6-subunit-deficient mice. Eur. J. Neurosci. 11, 233–240 (1999).
  Article CAS Google Scholar