The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone (original) (raw)

References

  1. Fremeau, R.T., Jr, Voglmaier, S., Seal, R.P. & Edwards, R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 27, 98–103 (2004).
    Article CAS Google Scholar
  2. Fremeau, R.T., Jr et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. USA 99, 14488–14493 (2002).
    Article CAS Google Scholar
  3. Gras, C. et al. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22, 5442–5451 (2002).
    Article CAS Google Scholar
  4. Schafer, M.K., Varoqui, H., Defamie, N., Weihe, E. & Erickson, J.D. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem. 277, 50734–50748 (2002).
    Article Google Scholar
  5. Takamori, S., Malherbe, P., Broger, C. & Jahn, R. Molecular cloning and functional characterization of human vesicular glutamate transporter 3. EMBO Rep. 3, 798–803 (2002).
    Article CAS Google Scholar
  6. Nickerson Poulin, A., Guerci, A., El Mestikawy, S. & Semba, K. Vesicular glutamate transporter 3 immunoreactivity is present in cholinergic basal forebrain neurons projecting to the basolateral amygdala in rat. J. Comp. Neurol. 498, 690–711 (2006).
    Article Google Scholar
  7. Herzog, E. et al. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123, 983–1002 (2004).
    Article CAS Google Scholar
  8. Somogyi, J. et al. GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur. J. Neurosci. 19, 552–569 (2004).
    Article Google Scholar
  9. Kawaguchi, Y. Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J. Neurophysiol. 67, 1669–1682 (1992).
    Article CAS Google Scholar
  10. Calabresi, P., Centonze, D., Gubellini, P., Pisani, A. & Bernardi, G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci. 23, 120–126 (2000).
    Article CAS Google Scholar
  11. Zhou, F.M., Wilson, C.J. & Dani, J.A. Cholinergic interneuron characteristics and nicotinic properties in the striatum. J. Neurobiol. 53, 590–605 (2002).
    Article CAS Google Scholar
  12. Graybiel, A.M., Aosaki, T., Flaherty, A.W. & Kimura, M. The basal ganglia and adaptive motor control. Science 265, 1826–1831 (1994).
    Article CAS Google Scholar
  13. Hikida, T. et al. Increased sensitivity to cocaine by cholinergic cell ablation in nucleus accumbens. Proc. Natl. Acad. Sci. USA 98, 13351–13354 (2001).
    Article CAS Google Scholar
  14. Kaneko, S. et al. Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. Science 289, 633–637 (2000).
    Article CAS Google Scholar
  15. Kitabatake, Y., Hikida, T., Watanabe, D., Pastan, I. & Nakanishi, S. Impairment of reward-related learning by cholinergic cell ablation in the striatum. Proc. Natl. Acad. Sci. USA 100, 7965–7970 (2003).
    Article CAS Google Scholar
  16. Herbin, M., Gasc, J.P. & Renous, S. Symmetrical and asymmetrical gaits in the mouse: patterns to increase velocity. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 190, 895–906 (2004).
    PubMed Google Scholar
  17. Hitzemann, R., Qian, Y. & Hitzemann, B. Dopamine and acetylcholine cell density in the neuroleptic responsive (NR) and neuroleptic nonresponsive (NNR) lines of mice. J. Pharmacol. Exp. Ther. 266, 431–438 (1993).
    CAS PubMed Google Scholar
  18. Hikida, T., Kitabatake, Y., Pastan, I. & Nakanishi, S. Acetylcholine enhancement in the nucleus accumbens prevents addictive behaviors of cocaine and morphine. Proc. Natl. Acad. Sci. USA 100, 6169–6173 (2003).
    Article CAS Google Scholar
  19. Tzavara, E.T. et al. Procholinergic and memory enhancing properties of the selective norepinephrine uptake inhibitor atomoxetine. Mol. Psychiatry 11, 187–195 (2006).
    Article CAS Google Scholar
  20. Roseth, S., Fykse, E.M. & Fonnum, F. Uptake of l-glutamate into synaptic vesicles: competitive inhibition by dyes with biphenyl and amino- and sulphonic acid–substituted naphthyl groups. Biochem. Pharmacol. 56, 1243–1249 (1998).
    Article CAS Google Scholar
  21. Besson, M.J., Cheramy, A., Feltz, P. & Glowinski, J. Release of newly synthesized dopamine from dopamine-containing terminals in the striatum of the rat. Proc. Natl. Acad. Sci. USA 62, 741–748 (1969).
    Article CAS Google Scholar
  22. Scatton, B. & Lehmann, J. _N_-methyl-_C_-aspartate–type receptors mediate striatal 3H-acetylcholine release evoked by excitatory amino acids. Nature 297, 422–424 (1982).
    Article CAS Google Scholar
  23. Nguyen, M.L., Cox, G.D. & Parsons, S.M. Kinetic parameters for the vesicular acetylcholine transporter: two protons are exchanged for one acetylcholine. Biochemistry 37, 13400–13410 (1998).
    Article CAS Google Scholar
  24. Jentsch, T.J., Poet, M., Fuhrmann, J.C. & Zdebik, A.A. Physiological functions of CLC Cl− channels gleaned from human genetic disease and mouse models. Annu. Rev. Physiol. 67, 779–807 (2005).
    Article CAS Google Scholar
  25. Bankston, L.A. & Guidotti, G. Characterization of ATP transport into chromaffin granule ghosts. Synergy of ATP and serotonin accumulation in chromaffin granule ghosts. J. Biol. Chem. 271, 17132–17138 (1996).
    Article CAS Google Scholar
  26. Scherman, D. & Henry, J.P. Role of the proton electrochemical gradient in monoamine transport by bovine chromaffin granules. Biochim. Biophys. Acta 601, 664–677 (1980).
    Article CAS Google Scholar
  27. Hioki, H. et al. Chemically specific circuit composed of vesicular glutamate transporter 3– and preprotachykinin B–producing interneurons in the rat neocortex. Cereb. Cortex 14, 1266–1275 (2004).
    Article Google Scholar
  28. Kawano, M. et al. Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J. Comp. Neurol. 498, 581–592 (2006).
    Article CAS Google Scholar
  29. Yamaguchi, T., Sheen, W. & Morales, M. Glutamatergic neurons are present in the rat ventral tegmental area. Eur. J. Neurosci. 25, 106–118 (2007).
    Article Google Scholar
  30. Gasnier, B. The loading of neurotransmitters into synaptic vesicles. Biochimie 82, 327–337 (2000).
    Article CAS Google Scholar
  31. Contant, C., Umbriaco, D., Garcia, S., Watkins, K.C. & Descarries, L. Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum. Neuroscience 71, 937–947 (1996).
    Article CAS Google Scholar
  32. Fujiyama, F. et al. Presynaptic localization of an AMPA-type glutamate receptor in corticostriatal and thalamostriatal axon terminals. Eur. J. Neurosci. 20, 3322–3330 (2004).
    Article Google Scholar
  33. Bonsi, P. et al. Striatal metabotropic glutamate receptors as a target for pharmacotherapy in Parkinson's disease. Amino Acids 32, 189–195 (2007).
    Article CAS Google Scholar
  34. Consolo, S., Baldi, G., Giorgi, S. & Nannini, L. The cerebral cortex and parafascicular thalamic nucleus facilitate in vivo acetylcholine release in the rat striatum through distinct glutamate receptor subtypes. Eur. J. Neurosci. 8, 2702–2710 (1996).
    Article CAS Google Scholar
  35. Calabresi, P., Picconi, B., Parnetti, L. & Di Filippo, M. A convergent model for cognitive dysfunctions in Parkinson's disease: the critical dopamine-acetylcholine synaptic balance. Lancet Neurol. 5, 974–983 (2006).
    Article CAS Google Scholar
  36. Rogers, D.C. et al. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome 8, 711–713 (1997).
    Article CAS Google Scholar
  37. Crawley, J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities and specific behavioral tests. Brain Res. 835, 18–26 (1999).
    Article CAS Google Scholar
  38. Fleming, S.M. et al. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human α-synuclein. J. Neurosci. 24, 9434–9440 (2004).
    Article CAS Google Scholar
  39. Hamon, M. et al. Alterations of central serotonin and dopamine turnover in rats treated with ipsapirone and other 5-hydroxytryptamine1A agonists with potential anxiolytic properties. J. Pharmacol. Exp. Ther. 246, 745–752 (1988).
    CAS PubMed Google Scholar
  40. Kemel, M.L., Desban, M., Glowinski, J. & Gauchy, C. Distinct presynaptic control of dopamine release in striosomal and matrix areas of the cat caudate nucleus. Proc. Natl. Acad. Sci. USA 86, 9006–9010 (1989).
    Article CAS Google Scholar
  41. Paxinos, G. & Watson, C. The Mouse Brain in Stereotaxic Coordinates. (Academic Press, New York, 1997).
  42. Blanchet, F. et al. Distinct modifications by neurokinin1 (SR140333) and neurokinin2 (SR48968) tachykinin receptor antagonists of the _N_-methyl-D-aspartate-evoked release of acetylcholine in striosomes and matrix of the rat striatum. Neuroscience 85, 1025–1036 (1998).
    Article CAS Google Scholar
  43. Huttner, W.B., Schiebler, W., Greengard, P. & De Camilli, P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374–1388 (1983).
    Article CAS Google Scholar
  44. Herzog, E. et al. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci. 21, RC181 (2001).
    Article CAS Google Scholar
  45. Ferguson, S.M. et al. Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J. Neurosci. 23, 9697–9709 (2003).
    Article CAS Google Scholar
  46. Kashani, A., Betancur, C., Giros, B., Hirsch, E. & El Mestikawy, S. Altered expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in Parkinson disease. Neurobiol. Aging 28, 568–578 (2007).
    Article CAS Google Scholar
  47. Duplus, E. et al. Phosphorylation and transcriptional activity regulation of retinoid-related orphan receptor α1 by protein kinases C. J. Neurochem. published online, doi:10.1111/j.1471-4159.2007.05074.x (14 November 2007).

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