Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1)

European Journal of Neuroscience

Volumn 25, Issue 1, 2007, Pages 281-290

  Tordera, R M ^a   Totterdell, S ^b   Wojcik, S M ^c   Brose, N ^a   Elizalde, N ^a   Lasheras, B ^a   Del Rio, J ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Depression; Learning; Spatial memory; Ultrastructure; VGLUT

Indexed keywords

4 AMINOBUTYRIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CELL ULTRASTRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; EXPLORATORY BEHAVIOR; FRONTAL CORTEX; GENE EXPRESSION; GENE EXPRESSION REGULATION; HETEROZYGOSITY; HIPPOCAMPUS; LEARNING; LOCOMOTION; MEMORY; MENTAL DISEASE; MOUSE; MOUSE MUTANT; NERVE ENDING; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PHENOTYPE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RECOGNITION; SYNAPSE VESICLE; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; BRAIN; DEPRESSION; EXPLORATORY BEHAVIOR; FEMALE; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MOTOR ACTIVITY; NEUROTRANSMITTER AGENTS; REACTION TIME; RECOGNITION (PSYCHOLOGY); SWIMMING; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 33846231792     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05259.x     Document Type: Article

References (55)

1. Akirav, I. & Maroun, M. (2006) Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cereb. Cortex, 16, 1759-1765.
2. Broadbent, N.J., Squire, L.R. & Clark, R.E. (2004) Spatial memory, recognition memory, and the hippocampus. Proc. Natl Acad. Sci. USA, 101, 14515-14520.
3. Crawley, J.N., Belknap, J.K., Collins, A., Crabbe, J.C., Frankel, W., Henderson, N., Hitzemann, R.J., Maxson, S.C., Miner, L.L., Silva, A.J., Wehner, J.M., Wynshaw-Boris, A. & Paylor, R. (1997) Behavioural phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl.), 132, 107-124.
4. Crawley, J. & Goodwin, F.K. (1980) Preliminary report of a simple animal behaviour model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav., 13, 167-170.
5. Cryan, J.F., Kelly, P.H., Neijt, H.C., Sansig, G., Flor, P.J. & van Der Putten, H. (2003) Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur. J. Neurosci., 17, 2409-2417.
6. Cryan, J.F., Markou, A. & Lucki, I. (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci., 23, 238-245.
7. Daniels, R.W., Collins, C.A., Gelfand, M.V., Dant, J., Brooks, E.S., Krantz, D.E. & DiAntonio, A. (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J. Neurosci., 24, 10466-10474.
8. Duva, C.A., Floresco, S.B., Wunderlich, G.R., Lao, T.L., Pinel, J.P. & Phillips, A.G. (1997) Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. Behav. Neurosci., 111, 1184-1196.
9. Ennaceur, A. & Delacour, J. (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res., 31, 47-59.
10. Fremeau, R.T. Jr, Kam, K., Qureshi, T., Johnson, J., Copenhagen, D.R., Storm-Mathisen, J., Chaudhry, F.A., Nicoll, R.A. & Edwards, R.H. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science, 304, 1815-1819.
11. Fremeau, R.T. Jr, Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. & Edwards, R.H. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
12. Galani, R., Obis, S., Coutureau, E., Jarrard, L. & Cassel, J.C. (2002) A comparison of the effects of fimbria-fornix, hippocampal, or entorhinal cortex lesions on spatial reference and working memory in rats: short versus long postsurgical recovery period. Neurobiol. Learn. Mem, 77, 1-16.
13. Garcia-Alloza, M., Tsang, S.W., Gil-Bea, F.J., Francis, P.T., Lai, M.K., Marcos, B., Chen, C.P. & Ramirez, M.J. (2005) Involvement of the GABAergic system in depressive symptoms of Alzheimer's disease. Neurobiol. Aging, 27, 1110-1117.
14. Gras, C., Herzog, E., Bellenchi, G.C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B. & El Mestikawy, S. (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci., 22, 5442-5451.
15. Gras, C., Vinatier, J., Amilhon, B., Guerci, A., Christov, C., Ravassard, P., Giros, B. & El Mestikawy, S. (2005) Developmentally regulated expression of VGLUT3 during early post-natal life. Neuropharmacology, 49, 901-911.
16. Griebel, G., Belzung, C., Perrault, G. & Sanger, D.J. (2000) Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychopharmacology (Berl), 148, 164-170.
17. Griebel, G., Simiand, J., Serradeil-Le Gal, C., Wagnon, J., Pascal, M., Scatton, B., Maffrand, J.P. & Soubrie, P. (2002) Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc. Natl Acad. Sci. USA, 99, 6370-6375.
18. Halasy, K., Hajszan, T., Kovacs, E.G., Lam, T.T. & Leranth, C. (2004) Distribution and origin of vesicular glutamate transporter 2-immunoreactive fibers in the rat hippocampus. Hippocampus, 14, 908-918.
19. Herzog, E., Bellenchi, G.C., Gras, C., Bernard, V., Ravassard, P., Bedet, C., Gasnier, B., Giros, B. & El Mestikawy, S. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci. 21: RC181.
20. Herzog, E., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Giros, B., Gaspar, P. & El Mestikawy, S. (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience, 123, 983-1002.
21. Herzog, E., Takamori, S., Jahn, R., Brose, N. & Wojcik, S.M. (2006) Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J. Neurochem., 99, 1011-1018.
22. Hisano, S., Sawada, K., Kawano, M., Kanemoto, M., Xiong, G., Mogi, K., Sakata-Haga, H., Takeda, J., Fukui, Y. & Nogami, H. (2002) Expression of inorganic phosphate/vesicular glutamate transporters (BNPI/VGLUT1 and DNPI/VGLUT2) in the cerebellum and precerebellar nuclei of the rat. Brain Res. Mol. Brain Res., 107, 23-31.
23. Javitt, D.C. (2004) Glutamate as a therapeutic target in psychiatric disorders. Mol. Psychiatry, 9, 984-997.
24. Kaneko, T. & Fujiyama, F. (2002) Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci. Res., 42, 243-250.
25. Kendell, S.F., Krystal, J.H. & Sanacora, G. (2005) GABA and glutamate systems as therapeutic targets in depression and mood disorders. Expert Opin. Ther. Targets, 9, 153-168.
26. Kugaya, A. & Sanacora, G. (2005) Beyond monoamines: glutamatergic function in mood disorders. CNS Spectr., 10, 808-819.
27. Lister, R.G. (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl.), 92, 180-185.
28. Meunier, M., Bachevalier, J. & Mishkin, M. (1997) Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychologia, 35, 999-1015.
29. Minelli, A., Edwards, R.H., Manzoni, T. & Conti, F. (2003) Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortex. Brain Res. Dev. Brain Res., 140, 309-314.
30. Miyazaki, T., Fukaya, M., Shimizu, H. & Watanabe, M. (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur. J. Neurosci., 17, 2563-2572.
31. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Meth., 11, 47-60.
32. Moser, E., Moser, M.B. & Andersen, P. (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci., 13, 3916-3925.
33. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P. & Morris, R.G. (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl Acad. Sci. USA, 92, 9697-9701.
34. Moutsimilli, L., Farley, S., Dumas, S., El Mestikawy, S., Giros, B. & Tzavara, E.T. (2005) Selective cortical VGLUT1 increase as a marker for antidepressant activity. Neuropharmacology, 49, 890-900.
35. Olsen, R.W. & Betz, H. (2006) GABA and glycine. In Siegel, G.J., Albers, R.W., Brady, S.T. & Price, D.L. (eds), Basic Neurochemistry, 7th edn. Elsevier, Amsterdam, pp. 291-301.
36. Parsons, R.L., Calupca, M.A., Merriam, L.A. & Prior, C. (1999) Empty synaptic vesicles recycle and undergo exocytosis at vesamicol-treated motor nerve terminals. J. Neurophysiol., 81, 2696-2700.
37. Perez-Otaño, I., Herrero, M.T., Oset, C., De Ceballos, M.L., Luquin, M.R., Obeso, J.A. & Del Rio, J. (1991) Extensive loss of brain dopamine and serotonin induced by chronic administration of MPTP in the marmoset. Brain Res., 567, 127-132.
38. Porsolt, R.D. (2000) Animal models of depression: utility for transgenic research. Rev. Neurosci., 11, 53-58.
39. Pothos, E.N. (2002) Regulation of dopamine quantal size in midbrain and hippocampal neurons. Behav. Brain Res., 130, 203-207.
40. Ragozzino, M.E., Detrick, S. & Kesner, R.P. (2002) The effects of prelimbic and infralimbic lesions on working memory for visual objects in rats. Neurobiol. Learn. Mem., 77, 29-43.
41. Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol., 17, 208-212.
42. Robbins, T.W. & Murphy, E.R. (2006) Behavioural pharmacology: 40+ years of progress, with a focus on glutamate receptors and cognition. Trends Pharmacol. Sci., 27, 141-148.
43. Schafer, M.K., Varoqui, H., Defamie, N., Weihe, E. & Erickson, J.D. (2002) 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.
44. Seong, E., Seasholtz, A.F. & Burmeister, M. (2002) Mouse models for psychiatric disorders. Trends Genet., 18, 643-650.
45. Solberg, L.C., Horton, T.H. & Turek, F.W. (1999) Circadian rhythms and depression: effects of exercise in an animal model. Am. J. Physiol., 276, R152-R161.
46. Song, H., Ming, G., Fon, E., Bellocchio, E., Edwards, R.H. & Poo, M. (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron, 18, 815-826.
47. Strekalova, T., Spanagel, R., Bartsch, D., Henn, F.A. & Gass, P. (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology, 29, 2007-2017.
48. Svenningsson, P., Chergui, K., Rachleff, I., Flajolet, M., Zhang, X., El Yacoubi, M., Vaugeois, J.M., Nomikos, G.G. & Greengard, P. (2006) Alterations in 5-HT1B receptor function by p11 in depression-like states. Science, 311, 77-80.
49. Takamori, S., Rhee, J.S., Rosenmund, C. & Jahn, R. (2001) Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci., 21, RC182.
50. Tannenbaum, B., Tannenbaum, G.S., Sudom, K. & Anisman, H. (2002) Neurochemical and behavioral alterations elicited by a chronic intermittent stressor regimen: implications for allostatic load. Brain Res., 953, 82-92.
51. Tordera, R.M., Pei, Q. & Sharp, T. (2005) Evidence for increased expression of the vesicular glutamate transporter, VGLUT1, by a course of antidepressant treatment. J. Neurochem., 94, 875-883.
52. Varoqui, H., Schafer, M.K., Zhu, H., Weihe, E. & Erickson, J.D. (2002) Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J. Neurosci., 22, 142-155.
53. Wilson, N.R., Kang, J., Hueske, E.V., Leung, T., Varoqui, H., Murnick, J.G., Erickson, J.D. & Liu, G. (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J. Neurosci., 25, 6221-6234.
54. Wojcik, S.M., Rhee, J.S., Herzog, E., Sigler, A., Jahn, R., Takamori, S., Brose, N. & Rosenmund, C. (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl Acad. Sci. USA, 101, 7158-7163.
55. Zhou, Q., Petersen, C.C. & Nicoll, R.A. (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J. Physiol. (Lond.), 525, 195-206.