Expression of VGLUTs contributes to degeneration and acquisition of learning and memory

Neurobiology of Learning and Memory

Volumn 95, Issue 3, 2011, Pages 361-375

  Cheng, Xiao Rui ^a   Yang, Yong ^a   Zhou, Wen Xia ^a   Zhang, Yong Xiang ^a  

^a BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

Author keywords

Learning and memory; Senescence accelerated mouse; Vesicular glutamate transporter

Indexed keywords

MESSENGER RNA; SYNAPTOPHYSIN; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE EXPRESSION; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MENTAL CAPACITY; MENTAL PERFORMANCE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RISK FACTOR; SENESCENCE ACCELERATED MOUSE;

AGING; AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; CEREBRAL CORTEX; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, NEUROLOGIC MUTANTS; MICE, TRANSGENIC; RNA, MESSENGER; SYNAPTOPHYSIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 79952625346     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.01.010     Document Type: Article

References (90)

1. Aihara Y., Mashima H., Onda H., Hisano S., Kasuya H., Hori T., et al. Molecular cloning of a novel brain-type Na (+)-dependent inorganic phosphate cotransporter. Journal of Neurochemistry 2000, 74:2622-2625.
2. Alicja L., Markowska Edward., Spangler L., Ingram Donald K. Behavioral assessment of the senescence accelerated mouse (SAM P8 and R1). Physiology and Behavior 1998, 64:15-26.
3. Anlauf E., Derouiche A. Astrocytic exocytosis vesicles and glutamate: a high-resolution immunofluorescence study. Glia 2005, 49:96-106.
4. Bell K.F., Ducatenzeiler A., Ribeiro-da-Silva A., Duff K., Bennett D.A., Cuello A.C. The amyloid pathology progresses in a neurotransmitter-specific manner. Neurobiology of Aging 2006, 27:1644-1657.
5. Bellocchio E.E., Reimer R.J., Fremeau R.T.J., Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 2000, 289:957-960.
6. Bergersen L.H., Gundersen V. Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 2009, 158:260-265.
7. Bezzi P., Gundersen V., Galbete J.L., Seifert G., Steinhäuser C., Pilati E., et al. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nature Neuroscience 2004, 7:613-620.
8. Boikess S.R., O'Dell S.J., Marshall J.F. A sensitizing d-amphetamine dose regimen induces long-lasting spinophilin and VGLUT1 protein upregulation in the rat diencephalon. Neuroscience Letters 2010, 469:49-54.
9. Bole D.G., Ueda T. Inhibition of vesicular glutamate uptake by Rose Bengal-related compounds: structure-activity relationship. Neurochemistry Research 2005, 30:363-369.
10. Boulland J.L., Qureshi T., Seal R.P., Rafiki A., Gundersen V., Bergersen L.H., et al. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. Journal of Comparative Neurology 2004, 480:264-280.
11. Bozarth M.A. A computer approach to measuring shuttle box activity and conditioned place preference. Brain Research Bulletin 1983, 11:751-753.
12. Butterfield D.A., Poon H.F. The senescence-accelerated prone mouse (SAMP8): a model of age-related cognitive decline with relevance to alterations of the gene expression and protein abnormalities in Alzheimer's disease. Experimental Gerontology 2005, 40:774-783.
13. Canudas A.M., Gutierrez-Cuesta J., Rodriguez M.I., Acuna-Castroviejo D., Sureda F.X., Camins A., et al. Hyperphosphorylation of microtubule-associated protein tau in senescence-accelerated mouse (SAM). Mechanisms of Ageing and Development 2005, 126:1300-1304.
14. Carrigan C.N., Bartlett R.D., Esslinger C.S., Cybulski K.A., Tongcharoensirikul P., Bridges R.J., et al. Synthesis and in vitro pharmacology of substituted quinoline-2, 4-dicarboxylic acids as inhibitors of vesicular glutamate transport. Journal Medicinal Chemistry 2002, 45:2260-2276.
15. Cuomo V., De Salvia M.A., Petruzzi S., Alleva E. Appropriate end points for the characterization of behavioral changes in developmental toxicology. Environ Health Perspect 1996, 104(Suppl 2):307-315.
16. Daniels R.W., Collins C.A., Chen K., Gelfand M.V., Featherstone D.E., DiAntonio A. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 2006, 49:11-16.
17. Del Valle J., Duran-Vilaregut J., Manich G., Casadesús G., Smith M.A., Camins A., et al. Early amyloid accumulation in the hippocampus of SAMP8 Mice. Journal of Alzheimer's Disease 2010, 19:1303-1315.
18. Del Valle J., Duran-Vilaregut J., Manich G., Camins A., Pallàs M., Vilaplana J., et al. Time-course of blood-brain barrier disruption in senescence-accelerated mouse prone 8 (SAMP8) mice. International Journal of Developmental Neuroscience 2009, 27:47-52.
19. Ding Y., Li J., Lai Q., Azam S., Rafols J.A., Diaz F.G. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurology Research 2002, 24:829-836.
20. Etoga J.L., Ahmed S.K., Patel S., Bridges R.J., Thompson C.M. Conformationally-restricted amino acid analogues bearing a distal sulfonic acid show selective inhibition of system xc- over the vesicular glutamate transporter. Bioorganic and Medicinal Chemistry Letters 2010, 20:2680-2683.
21. Flood J.F., Morley J.E. Learning and memory in the SAMP8 mouse. Neuroscience Biobehavior Review 1998, 22:1-20.
22. Flood J.E., Morley J.E. Age-related changes in foot shock avoidance acquisition and retention in senescence accelerated mouse (SAM). Neurobiology of Aging 1993, 14:153-157.
23. Fremeau R.T., Burman J., Qureshi T., Tran C.H., Proctor J., Johnson J., et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proceedings of the National Academy of Sciences 2002, 99:14488-14493.
24. Fremeau R.T., Kam K., Qureshi T., Johnson J., Copenhagen D.R., Storm-Mathisen J., et al. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 2004, 304:1815-1819.
25. Fremeau R.T., Troyer M.D., Pahner I., Nygaard G.O., Tran C.H., Reimer R.J., et al. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 2001, 31:247-260.
26. Fujiyama F., Furuta T., Kaneko T. Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. Journal of Comparative Neurology 2001, 435:379-387.
27. Garcia-Garcia A.L., Elizalde N., Matrov D., Harro J., Wojcik S.M., Venzala E., et al. Increased vulnerability to depressive-like behavior of mice with decreased expression of VGLUT1. Biology and Psychiatry 2009, 66:275-282.
28. Gras C., Herzog E., Bellenchi G.C., Bernard V., Ravassard P., Pohl M., et al. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. The Journal of Neuroscience 2002, 22:5442-5451.
29. Herzog, E., Bellenchi, G.C., Gras, C., Bernard, V., Ravassard, P., Bedet, C.,Gasnier, B., Giros, B., El, M. (2001). The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. The Journal of Neuroscience 21, RC181.
30. Ishikawa T., Sahara Y., Takahashi T. A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 2002, 34:613-621.
31. Kaneko T., Fujiyama F. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosciense Research 2002, 42:243-250.
32. Kaneko T., Fujiyama F., Hioki H. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. Journal of Comparative Neurology 2002, 444:39-62.
33. Kashani A., Lepicard E., Poirel O., Videau C., David J.P., Fallet-Bianco C., et al. Loss of VGLUT1 and VGLUT2 in the prefrontal cortex is correlated with cognitive decline in Alzheimer disease. Neurobiology of Aging 2008, 29:1619-1630.
34. Kawamata T., Akiguchi I., Yagi H., Irino M., Sugiyama H., Akiyama H., et al. Neuropathological studies on strains of senescenceaccelerated mice (SAM) with age-related deficits in learning and memory. Experimental Gerontology 1997, 32:161-170.
35. Khan M., De Sevilla L., Mahesh V.B., Brann D.W. Enhanced glutamatergic and decreased gabaergic synaptic appositions to GnRH neurons onproestrus in the rat: modulatory effect of aging. PLoS ONE 2010, 5:e10172.
36. Kirvell, S.L., Fremeau, R.T., Francis, P.T. (2002). Vesicular glutamate transporter 1 in Alzheimer's disease. Society Neuroscience 2002 Abstract Viewer 785.15 (Abstract).
37. Kiss J., Kocsis K., Csaki A., Halasz B. Evidence for vesicular glutamate transporter synapses onto gonadotropin-releasing hormone and other neurons in the rat medial preoptic area. European Journal of Neuroscience 2003, 18:3267-3278.
38. Kondziella D., Bidar A., Urfjell B., Sletvold O., Sonnewald U. The pentylenetetrazole-kindling model of epilepsy in SAMP8 mice. Behavior and metabolism. Neurochemistry International 2002, 40:413-418.
39. Lacey C.J., Boyes J., Gerlach O., Chen L., Magill P.J., Bolam J.P. GABAb receptors as glutamatergic synapses in the rat striatum. Neuroscience 2005, 136:1083-1095.
40. LeVay S., Stryker M.P., Shatz C.J. Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. Journal of Comparative Neurology 1978, 179:223-244.
41. Massie A., Schallier A., Vermoesen K., Arckens L., Michotte Y. Biphasic and bilateral changes in striatal VGLUT1 and 2 protein expression in hemi-Parkinson rats. Neurochemistry International 2010, 57:111-118.
42. Miyamoto M. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 And SAMP 10. Experimental Gerontology 1997, 32:139-148.
43. Miró-Bernié N., Ichinohe N., Pérez-Clausell J., Rockland K.S. Zinc-rich transient vertical modules in the rat retrosplenial cortex during postnatal development. Neuroscience 2006, 138:523-535.
44. Miyamoto M., Kiyota Y., Yamazaki N., Nagaoka A., Matsuo T., Nagawa Y., et al. Age-related changes in learning and memory in the senescence-accelerated mouse (SAM). Physioogy and Behavior 1986, 38:399-406.
45. Moechars D., Weston M.C., Leo S., Callaerts-Vegh Z., Goris I., Daneels G., et al. Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. The Journal of Neuroscience 2006, 26:12055-12066.
46. Montana V., Ni Y., Sunjara V., Hua X., Parpura V. Vesicular glutamate transporter-dependent glutamate release from astrocytes. The Journal of Neuroscience 2004, 24:2633-2642.
47. Morley J.E. The SAMP8 mouse: a model of Alzheimer disease?. Biogerontology 2002, 3:57-60.
48. Morley J.E., Banks W.A., Kumar V.B., Farr S.A. The SAMP8 mouse as a model for Alzheimer disease: studies from Saint Louis University. International Congress Series 2004, 1260:23-28.
49. Morley J.E., Kumar V.B., Bernardo A.E., Farr S.A., Uezu K., Tumosa N., et al. Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 2000, 21:1761-1767.
50. Nakahara H., Kanno T., Inai Y., Utsumi K., Hiramatsu M., Mori A., et al. Mitochondrial dysfunction in the senescence accelerated mouse (SAM). Free Radical Biology and Medicine 1998, 24:85-92.
51. Nithianantharajah J., Levis H., Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95. Neurobiology of Learning and Memory 2004, 81:200-210.
52. Nomura Y., Okuma Y. Age-related defects in lifespan and learning ability in SAMP8 mice. Neurobiology of Aging 1999, 20:111-115.
53. Nomura Y., Kitamura Y., Ohnuki T., et al. Alterations in acetylcholine, NMDA, benzodiozepine receptors and protein kinase C in the brain of the senescence-accelerated mouse: an animal model useful for studies on cognitive enhances. Behavioural Brain Research 1997, 83:51-55.
54. Ogita K., Hirata K., Bole D.G., Yoshida S., Tamura Y., Leckenby A.M., et al. Inhibition of vesicular glutamate storage and exocytotic release by Rose Bengal. Journal of Neurochemistry 2001, 77:34-42.
55. Ohta A., Hirano T., Yagi H., Tanaka S., Hosokawa M., Takeda T. Behavioral characteristics of the SAM-P/8 strain in Sidman active avoidance task. Brain Research 1989, 498:195-198.
56. Onozuka M., Watanabe K., Fujita M., Tomida M., Ozono S. Changes in the septohippocampal cholinergic system following removal of molar teeth in the aged SAMP8 mouse. Behavior Brain Research 2002, 133:197-204.
57. Parpura V., Zorec R. Gliotransmission: Exocytotic release from astrocytes. Brain Research Review 2010, 63:83-92.
58. Patel S.A., Nagy J.O., Bolstad E.D., Gerdes J.M., Thompson C.M. Tetrapeptide inhibitors of the glutamate vesicular transporter (VGLUT). Bioorganic and Medicinal Chemistry Letters 2007, 17:5125-5128.
59. Pelegrí C., Canudas A.M., del Valle J., Casadesús G., Smith M.A., Camins A., et al. Increased permeability of blood-brain barrier on the hippocampus of a murine model of senescence. Mechanisms of Ageing and Development 2007, 128:522-528.
60. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., Skuladottir G.V. Lipid peroxidation in brain during aging in the senescence-accelerated mouse (SAM). Neurobiology of Aging 2007, 28:1170-1178.
61. Pietrancosta N., Kessler A., Favre-Besse F.C., Triballeau N., Quentin T., Giros B., et al. Rose Bengal analogs and vesicular glutamate transporters (VGLUTs). Bioorganic and Medicinal Chemistry 2010, 18:6922-6933.
62. Raju D.V., Ahern T.H., Shah D.J., Wright T.M., Standaert D.G., Hall R.A., et al. Differential synaptic plasticity of the corticostriatal and thalamostriatal systems in an MPTP-treated monkey model of parkinsonism. European Journal of Neuroscience 2008, 27:1647-1658.
63. Reimer R.J., Edwards R.H. Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Archieve 2004, 447:629-635.
64. Riedel G., Reymann K.G. Metabotropic glutamate receptors in hippocampal long-term potentiation and learning and memory. Acta Physiologica Scandinavica 1996, 157:1-19.
65. Rueda N., Llorens-Martín M., Flórez J., Valdizán E., Banerjee P., Trejo J.L., et al. Memantine normalizes several phenotypic features in the Ts65Dn mouse model of Down syndrome. Journal of Alzheimers Disease 2010, 21:277-290.
66. Santos M.S., Li H., Voglmaier S.M. Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience 2009, 158:189-203.
67. Spangler E.L., Patel N., Speer D., Speer D., Hyman M., Hengemihle J., et al. Passive avoidance and complex maze learning in the senescence accelerated mouse (SAM): age and strain comparisons of SAM P8 and R1. The Journals of Gerontology, Series A: Biological Sciences Medical Sciences 2002, 57:B61-B68.
68. Seal R.P., Akil O., Yi E., Weber C.M., Grant L., Yoo J., et al. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 2008, 57:263-275.
69. Shen Y.C., Liao D.L., Lu C.L., Chen J.Y., Liou Y.J., Chen T.T., et al. Resequencing of the vesicular glutamate transporter 2 gene (VGLUT2) reveals some rare genetic variants that may increase the genetic burden in schizophrenia. Schizophrenia Research 2010, 121:179-186.
70. Shigeri Y., Seal R.P., Shimamoto K. Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Research Review 2004, 45:250-265.
71. Stenovec M., Kreft M., Grilc S., Potokar M., Kreft M.E., Pangrsic T., et al. Ca2+ dependent mobility of vesicles capturing anti-VGLUT1 antibodies. Experimental Cell Research 2007, 313:3809-3818.
72. Stornetta R.L., Sevigny C.P., Guyenet P.G. Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. The Journal of Comparative Neurology 2002, 444:191-206.
73. Tajes M., Gutierrez-Cuesta J., Folch J., Ferrer I., Caballero B., Smith M.A., et al. Lithium treatment decreases activities of tau kinases in a murine model of senescence. Journal of Neuropathology and Experimental Neurology 2008, 67:612-623.
74. Takamori, S., Rhee, J.S., Rosenmund, C., Jahn, R. (2001). Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter. The Journal of Neuroscience, 21, RC182.
75. Takamori S. VGLUTs: 'exciting' times for glutamatergic research?. Neuroscience Research 2006, 55:343-351.
76. Takamori S., Rhee J.S., Rosenmund C., Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 2000, 407:189-194.
77. Takeda T., Hosokawa M., Takeshita S., Rino M., Higuchi K., Matsushita T., et al. A new murine model of accelerated senescence. Mechanisms of Ageing and Development 1981, 17:183-194.
78. Thompson C.M., Davis E., Carrigan C.N., Cox H.D., Bridges R.J., Gerdes J.M. Inhibitors of the glutamate vesicular transporter (VGLUT). Current Medicine Chemistry 2005, 12:2041-2056.
79. Tordera R.M., Totterdell S., Wojcik S.M., Brose N., Elizalde N., Lasheras B., et al. 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 2007, 25:281-290.
80. Tsvetkov E., Shin R.M., Bolshakov V.Y. Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 2004, 41:139-151.
81. Ueno M., Sakamoto H., Kanenishi K., Onodera M., Akiguchi I., Hosokawa M. Ultrastructural and permeability features of microvessels in the hippocampus, cerebellum and pons of senescence-accelerated mice (SAM). Neurobiology of Aging 2001, 22:469-478.
82. Wilson N.R., Kang J., Hueske E.V., Leung T., Varoqui H., Murnick J.G., et al. Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. The Journal of Neuroscience 2005, 25:6221-6234.
83. Wojcik S.M., Rhee J.S., Herzog E., Sigler A., Jahn R., Takamori S., et al. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proceedings of the National Academy of Sciences 2004, 101:7158-7163.
84. G93A mice. Neurobiology of Disease 2010, 37:58-66.
85. Yagi H., Katoh S., Akiguchi I., Takeda T. Age-related deterioration of ability of acquisition in memory and learning in senescence accelerated mouse: SAM-P/8 as an animal model of disturbances in recent memory. Brain Research 1988, 474:86-93.
86. Yagi H., Irino M., Matsushita T., Katoh S., Umezawa M., Tsuboyama T., et al. Spontaneous spongy degeneration of the brain stem in SAM-P/8 mice, a newly developed memory-deficient strain. Journal of Neuropathology and Experimental Neurology 1989, 48:577-590.
87. Zhang Q., Pangrsic T., Kreft M., Krzan M., Li N., Sul J.Y., et al. Fusion-related release of glutamate from astrocytes. The Journal of biological chemistry 2004, 279:12724-12733.
88. Zhang Q.P., Ding H.Q., Li W.X., Fan Z.Q., Sun A.Y., Luo J., et al. Senescence accelerated mouse strain is sensitive to neurodegeneration induced by mild impairment of oxidative metabolism. Brain research 2009, 1264:111-118.
89. Ziegler D.R., Cullinan W.E., Herman J.P. Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. The Journal of Comparative Neurology 2001, 448:217-229.
90. Zink M., Vollmayr B., Gebicke-Haerter P.J., Henn F.A. Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression. Neuropharmacology 2010, 58:465-473.