Transcript expression of vesicular glutamate transporters in lumbar dorsal root ganglia and the spinal cord of mice - Effects of peripheral axotomy or hindpaw inflammation

Neuroscience

Volumn 248, Issue , 2013, Pages 95-111

  Malet, M ^a,b   Vieytes, C A ^a   Lundgren, K H ^c   Seal, R P ^d   Tomasella, E ^a,b   Seroogy, K B ^c   Hokfelt T ^e   Gebhart, G F ^d   Brumovsky, P R ^a,b,d  

^a UNIVERSIDAD AUSTRAL   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Axotomy; DRGs; Hindpaw inflammation; Hybridization; Spinal cord; VGLUT; VGLUTs

Indexed keywords

MESSENGER RNA; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3; AMINO ACID TRANSPORTER; SLC17A6 PROTEIN, MOUSE; SLC17A7 PROTEIN, MOUSE; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 3, MOUSE;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DORSAL NUCLEUS OF CLARKE; HINDLIMB; IN SITU HYBRIDIZATION; LUMBOSACRAL SPINE; MALE; MOUSE; NERVE FIBER TRANSECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAW EDEMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RNA PROBE; SCIATIC NERVE; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD VENTRAL HORN; SPINAL GANGLION; THORACOLUMBAR SPINE; ANIMAL; BAGG ALBINO MOUSE; INFLAMMATION; INJURIES; METABOLISM; NERVE CELL;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; AXOTOMY; GANGLIA, SPINAL; HINDLIMB; INFLAMMATION; MALE; MICE; MICE, INBRED BALB C; NEURONS; RNA, MESSENGER; SCIATIC NERVE; SPINAL CORD; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84880144097     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.05.044     Document Type: Article

References (100)

1. Agrawal S.G., Evans R.H. The primary afferent depolarizing action of kainate in the rat. Br J Pharmacol 1986, 87:345-355.
2. Aihara Y., Mashima H., Onda H., Hisano S., Kasuya H., Hori T., Yamada S., Tomura H., Yamada Y., Inoue I., Kojima I., Takeda J. Molecular cloning of a novel brain-type Na(+)-dependent inorganic phosphate cotransporter. J Neurochem 2000, 74:2622-2625.
3. Alvarez F.J., Villalba R.M., Zerda R., Schneider S.P. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 2004, 472:257-280.
4. Anseloni V.C., He F., Novikova S.I., Turnbach R.M., Lidow I.A., Ennis M., Lidow M.S. Alterations in stress-associated behaviors and neurochemical markers in adult rats after neonatal short-lasting local inflammatory insult. Neuroscience 2005, 131:635-645.
5. Bai L., Xu H., Collins J.F., Ghishan F.K. Molecular and functional analysis of a novel neuronal vesicular glutamate transporter. J Biol Chem 2001, 276:36764-36769.
6. Bellocchio E.E., Reimer R.J., Fremeau R.T., Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 2000, 289:957-960.
7. Binns B.C., Huang Y., Goettl V.M., Hackshaw K.V., Stephens R.L. Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model. Brain Res 2005, 1041:38-47.
8. Boulland J.L., Qureshi T., Seal R.P., Rafiki A., Gundersen V., Bergersen L.H., Fremeau R.T., Edwards R.H., Storm-Mathisen J., Chaudhry F.A. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 2004, 480:264-280.
9. Brumovsky P.R., Shi T.J., Matsuda H., Kopp J., Villar M.J., Hökfelt T. NPY Y1 receptors are present in axonal processes of DRG neurons. Exp Neurol 2002, 174:1-10.
10. Brumovsky P., Watanabe M., Hökfelt T. Expression of the vesicular glutamate transporters-1 and -2 in adult mouse dorsal root ganglia and spinal cord and their regulation by nerve injury. Neuroscience 2007, 147:469-490.
11. Brumovsky P.R., Robinson D.R., La J.H., Seroogy K.B., Lundgren K.H., Albers K.M., Kiyatkin M.E., Seal R.P., Edwards R.H., Watanabe M., Hökfelt T., Gebhart G.F. Expression of vesicular glutamate transporters type 1 and 2 in sensory and autonomic neurons innervating the mouse colorectum. J Comp Neurol 2011, 519:3346-3366.
12. Brumovsky P.R., Seroogy K.B., Lundgren K.H., Watanabe M., Hökfelt T., Gebhart G.F. Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT(2)-positive perineuronal baskets. Exp Neurol 2011, 230:258-272.
13. Brumovsky P.R., Seal R.P., Lundgren K.H., Seroogy K.B., Watanabe M., Gebhart G.F. Expression of vesicular glutamate transporters in sensory and autonomic neurons innervating the mouse bladder. J Urol 2012, 189:2342-2349.
14. Carlton S.M., Hargett G.L., Coggeshall R.E. Localization and activation of glutamate receptors in unmyelinated axons of rat glabrous skin. Neurosci Lett 1995, 197:25-28.
15. Chaudhry F.A., Boulland J.L., Jenstad M., Bredahl M.K., Edwards R.H. Pharmacology of neurotransmitter transport into secretory vesicles. Handb Exp Pharmacol 2008, 77-106.
16. Chiosa L., Gane P. Action of glutamic acid on the higher nervous activity of small laboratory animals (rats); considerations on the relations between the biochemical substratum and the higher nervous activity. Rev Sci Med 1956, 1:165-171.
17. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 2002, 3:16.
18. Curtis D.R., Phillis J.W., Watkins J.C. The chemical excitation of spinal neurones by certain acidic amino acids. J Physiol 1960, 150:656-682.
19. Daniels R.W., Miller B.R., DiAntonio A. Increased vesicular glutamate transporter expression causes excitotoxic neurodegeneration. Neurobiol Dis 2011, 41:415-420.
20. deGroot J., Zhou S., Carlton S.M. Peripheral glutamate release in the hindpaw following low and high intensity sciatic stimulation. Neuroreport 2000, 11:497-502.
21. Dittman J.S., Regehr W.G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 1998, 18:6147-6162.
22. Du B.A., Shakya S.S., Bannatyne B.A., Jalicy S.M., Linnen S., Maxwell D.J. Neurotransmitter phenotypes of descending systems in the rat lumbar spinal cord. Neuroscience 2012, 227:67-79.
23. Edwards R.H. The neurotransmitter cycle and quantal size. Neuron 2007, 55:835-858.
24. Evans R.H., Evans S.J., Pook P.C., Sunter D.C. A comparison of excitatory amino acid antagonists acting at primary afferent C fibres and motoneurones of the isolated spinal cord of the rat. Br J Pharmacol 1987, 91:531-537.
25. Featherstone D.E. Intercellular glutamate signaling in the nervous system and beyond. ACS Chem Neurosci 2010, 1:4-12.
26. Fremeau R.T., 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. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 2001, 31:247-260.
27. Fremeau R.T., Burman J., Qureshi T., Tran C.H., Proctor J., Johnson J., Zhang H., Sulzer D., Copenhagen D.R., Storm-Mathisen J., Reimer R.J., Chaudhry F.A., Edwards R.H. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci U S A 2002, 99:14488-14493.
28. Fremeau R.T., Voglmaier S., Seal R.P., Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 2004, 27:98-103.
29. Gebre S.A., Reeber S.L., Sillitoe R.V. Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2. Brain Struct Funct 2012, 217:165-180.
30. Gras C., Herzog E., Bellenchi G.C., Bernard V., Ravassard P., Pohl M., Gasnier B., Giros B., El M.S. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 2002, 22:5442-5451.
31. Graziano A., Liu X.B., Murray K.D., Jones E.G. Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse. J Comp Neurol 2008, 507:1258-1276.
32. Guillery R.W. On counting and counting errors. J Comp Neurol 2002, 447:1-7.
33. Hayashi M., Otsuka M., Morimoto R., Hirota S., Yatsushiro S., Takeda J., Yamamoto A., Moriyama Y. Differentiation-associated Na+-dependent inorganic phosphate cotransporter (DNPI) is a vesicular glutamate transporter in endocrine glutamatergic systems. J Biol Chem 2001, 276:43400-43406.
34. Hemmerle A.M., Dickerson J.W., Herring N.R., Schaefer T.L., Vorhees C.V., Williams M.T., Seroogy K.B. (+/-)3,4-Methylenedioxymethamphetamine ("ecstasy") treatment modulates expression of neurotrophins and their receptors in multiple regions of adult rat brain. J Comp Neurol 2012, 520:2459-2474.
35. Herzog E., Bellenchi G.C., Gras C., Bernard V., Ravassard P., Bedet C., Gasnier B., Giros B., El M.S. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 2001, 21:RC181.
36. Herzog E., Takamori S., Jahn R., Brose N., Wojcik S.M. Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J Neurochem 2006, 99:1011-1018.
37. Hoffman E.M., Miller K.E. Peripheral inhibition of glutaminase reduces carrageenan-induced Fos expression in the superficial dorsal horn of the rat. Neurosci Lett 2010, 472:157-160.
38. Hökfelt T., Brumovsky P., Villar M.J. Retrograde cellular changes after nerve injury. Encyclopedia of pain 2007, 2122-2126. Springer. R.F. Schmidt, W.D. Willis (Eds.).
39. Hökfelt T., Zhang X., Villar M.J., Xu X.J., Wiesenfeld-Hallin Z. Central consequences of peripheral nerve damage. Textbook of pain 2013, Elsevier. S. McMahon, M. Koltzenburg, I. Tracey, D.C. Turk (Eds.).
40. Hughes D.I., Polgar E., Shehab S.A., Todd A.J. Peripheral axotomy induces depletion of the vesicular glutamate transporter VGLUT1 in central terminals of myelinated afferent fibres in the rat spinal cord. Brain Res 2004, 1017:69-76.
41. Hwang S.J., Burette A., Rustioni A., Valtschanoff J.G. Vanilloid receptor VR1-positive primary afferents are glutamatergic and contact spinal neurons that co-express neurokinin receptor NK1 and glutamate receptors. J Neurocytol 2004, 33:321-329.
42. Jackson D.L., Graff C.B., Richardson J.D., Hargreaves K.M. Glutamate participates in the peripheral modulation of thermal hyperalgesia in rats. Eur J Pharmacol 1995, 284:321-325.
43. Kaneko T., Fujiyama F. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 2002, 42:243-250.
44. Kapadia S.E., LaMotte C.C. Deafferentation-induced alterations in the rat dorsal horn: I. Comparison of peripheral nerve injury vs. rhizotomy effects on presynaptic, postsynaptic, and glial processes. J Comp Neurol 1987, 266:183-197.
45. Karim F., Bhave G., Gereau R.W. Metabotropic glutamate receptors on peripheral sensory neuron terminals as targets for the development of novel analgesics. Mol Psychiatry 2001, 6:615-617.
46. Kawano M., Kawasaki A., Sakata-Haga H., Fukui Y., Kawano H., Nogami H., Hisano S. Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J Comp Neurol 2006, 498:581-592.
47. Kawasaki A., Hoshi K., Kawano M., Nogami H., Yoshikawa H., Hisano S. Up-regulation of VGLUT2 expression in hypothalamic-neurohypophysial neurons of the rat following osmotic challenge. Eur J Neurosci 2005, 22:672-680.
48. Kullander K., Butt S.J., Lebret J.M., Lundfald L., Restrepo C.E., Rydstrom A., Klein R., Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 2003, 299:1889-1892.
49. Lagerström M.C., Rogoz K., Abrahamsen B., Persson E., Reinius B., Nordenankar K., Olund C., Smith C., Mendez J.A., Chen Z.F., Wood J.N., Wallen-Mackenzie A., Kullander K. VGLUT2-dependent sensory neurons in the TRPV1 population regulate pain and itch. Neuron 2010, 68:529-542.
50. Landry M., Bouali-Benazzouz R., El M.S., Ravassard P., Nagy F. Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J Comp Neurol 2004, 468:380-394.
51. Leo S., Moechars D., Callaerts-Vegh Z., D'Hooge R., Meert T. Impairment of VGLUT2 but not VGLUT1 signaling reduces neuropathy-induced hypersensitivity. Eur J Pain 2009, 13:1008-1017.
52. Li J.L., Fujiyama F., Kaneko T., Mizuno N. Expression of vesicular glutamate transporters, VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J Comp Neurol 2003, 457:236-249.
53. Li J.L., Xiong K.H., Dong Y.L., Fujiyama F., Kaneko T., Mizuno N. Vesicular glutamate transporters, VGluT1 and VGluT2, in the trigeminal ganglion neurons of the rat, with special reference to coexpression. J Comp Neurol 2003, 463:212-220.
54. Liaw W.J., Stephens R.L., Binns B.C., Chu Y., Sepkuty J.P., Johns R.A., Rothstein J.D., Tao Y.X. Spinal glutamate uptake is critical for maintaining normal sensory transmission in rat spinal cord. Pain 2005, 115:60-70.
55. Liu Y., Abdel S.O., Zhang L., Duan B., Tong Q., Lopes C., Ji R.R., Lowell B.B., Ma Q. VGLUT2-dependent glutamate release from nociceptors is required to sense pain and suppress itch. Neuron 2010, 68:543-556.
56. Llewellyn-Smith I.J., Martin C.L., Fenwick N.M., Dicarlo S.E., Lujan H.L., Schreihofer A.M. VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. J Comp Neurol 2007, 503:741-767.
57. Lou S., Duan B., Vong L., Lowell B.B., Ma Q. Runx1 controls terminal morphology and mechanosensitivity of VGLUT3-expressing C-mechanoreceptors. J Neurosci 2013, 33:870-882.
58. Mann M.D. Clarke's column and the dorsal spinocerebellar tract: a review. Brain Behav Evol 1973, 7:34-83.
59. Maxwell D.J., Belle M.D., Cheunsuang O., Stewart A., Morris R. Morphology of inhibitory and excitatory interneurons in superficial laminae of the rat dorsal horn. J Physiol 2007, 584:521-533.
60. Mayhew T.M., Gundersen H.J. If you assume, you can make an ass out of u and me: a decade of the disector for stereological counting of particles in 3D space. J Anat 1996, 188:1-15.
61. Meister B., Arvidsson U., Zhang X., Jacobsson G., Villar M.J., Hokfelt T. Glutamate transporter mRNA and glutamate-like immunoreactivity in spinal motoneurones. Neuroreport 1993, 5:337-340.
62. Miller K.E., Balbas J.C., Benton R.L., Lam T.S., Edwards K.M., Kriebel R.M., Schechter R. Glutaminase immunoreactivity and enzyme activity is increased in the rat dorsal root ganglion following peripheral inflammation. Pain Res Treat 2012, 2012:414697.
63. Minami T., Matsumura S., Okuda-Ashitaka E., Shimamoto K., Sakimura K., Mishina M., Mori H., Ito S. Characterization of the glutamatergic system for induction and maintenance of allodynia. Brain Res 2001, 895:178-185.
64. Moechars D., Weston M.C., Leo S., Callaerts-Vegh Z., Goris I., Daneels G., Buist A., Cik M., van der S.P., Kass S., Meert T., D'Hooge R., Rosenmund C., Hampson R.M. Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci 2006, 26:12055-12066.
65. Morris J.L., Konig P., Shimizu T., Jobling P., Gibbins I.L. Most peptide-containing sensory neurons lack proteins for exocytotic release and vesicular transport of glutamate. J Comp Neurol 2005, 483:1-16.
66. Nakamura K., Watakabe A., Hioki H., Fujiyama F., Tanaka Y., Yamamori T., Kaneko T. Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient. Eur J Neurosci 2007, 26:3054-3067.
67. Navarro X., Vivo M., Valero-Cabre A. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 2007, 82:163-201.
68. Ni B., Rosteck P.R., Nadi N.S., Paul S.M. Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci U S A 1994, 91:5607-5611.
69. Olave M.J., Maxwell D.J. Axon terminals possessing the alpha 2c-adrenergic receptor in the rat dorsal horn are predominantly excitatory. Brain Res 2003, 965:269-273.
70. Oliveira A.L., Hydling F., Olsson E., Shi T., Edwards R.H., Fujiyama F., Kaneko T., Hökfelt T., Cullheim S., Meister B. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 2003, 50:117-129.
71. Persson S., Boulland J.L., Aspling M., Larsson M., Fremeau R.T., Edwards R.H., Storm-Mathisen J., Chaudhry F.A., Broman J. Distribution of vesicular glutamate transporters 1 and 2 in the rat spinal cord, with a note on the spinocervical tract. J Comp Neurol 2006, 497:683-701.
72. Ren K., Novikova S.I., He F., Dubner R., Lidow M.S. Neonatal local noxious insult affects gene expression in the spinal dorsal horn of adult rats. Mol Pain 2005, 1:27.
73. Robinson D.R., Gebhart G.F. Inside information: the unique features of visceral sensation. Mol Interv 2008, 8:242-253.
74. Rustioni A., Weinberg R.J. The somatosensory system. Handbook of Chemical Neuroanatomy 1989, 219-321. Elsevier, Amsterdam. A. Björklund, T. Hökfelt, L.W. Swanson (Eds.).
75. Sakata-Haga H., Kanemoto M., Maruyama D., Hoshi K., Mogi K., Narita M., Okado N., Ikeda Y., Nogami H., Fukui Y., Kojima I., Takeda J., Hisano S. Differential localization and colocalization of two neuron-types of sodium-dependent inorganic phosphate cotransporters in rat forebrain. Brain Res 2001, 902:143-155.
76. Santos M.S., Li H., Voglmaier S.M. Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience 2009, 158:189-203.
77. Schäfer 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 2002, 277:50734-50748.
78. Scherrer G., Low S.A., Wang X., Zhang J., Yamanaka H., Urban R., Solorzano C., Harper B., Hnasko T.S., Edwards R.H., Basbaum A.I. VGLUT2 expression in primary afferent neurons is essential for normal acute pain and injury-induced heat hypersensitivity. Proc Natl Acad Sci U S A 2010, 107:22296-22301.
79. Schneider S.P., Walker T.M. Morphology and electrophysiological properties of hamster spinal dorsal horn neurons that express VGLUT2 and enkephalin. J Comp Neurol 2007, 501:790-809.
80. Seal R.P., Edwards R.H. The diverse roles of vesicular glutamate transporter 3. Handb Exp Pharmacol 2006, 137-150.
81. Seal R.P., Wang X., Guan Y., Raja S.N., Woodbury C.J., Basbaum A.I., Edwards R.H. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 2009, 462:651-655.
82. Seroogy K.B., Herman J.P. In situ hybridization approaches to the study of the nervous system. Neurochemistry - a practical approach 1997, 121-150. Oxford University Press, Oxford. A.J. Turner, H.S. Bachelard (Eds.).
83. Sillitoe R.V., Vogel M.W., Joyner A.L. Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J Neurosci 2010, 30:10015-10024.
84. Smith R.E., Haroutunian V., Davis K.L., Meador-Woodruff J.H. Vesicular glutamate transporter transcript expression in the thalamus in schizophrenia. Neuroreport 2001, 12:2885-2887.
85. Sung B., Lim G., Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 2003, 23:2899-2910.
86. Takamori S. VGLUTs: 'exciting' times for glutamatergic research?. Neurosci Res 2006, 55:343-351.
87. 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.
88. Takamori S., Rhee J.S., Rosenmund C., Jahn R. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci 2001, 21:RC182.
89. Tao Y.X., Gu J., Stephens R.L. Role of spinal cord glutamate transporter during normal sensory transmission and pathological pain states. Mol Pain 2005, 1:30.
90. Tian Y.L., Guo Y., Cao D.Y., Zhang Q., Wang H.S., Zhao Y. Local application of morphine suppresses glutamate-evoked activities of C and Adelta afferent fibers in rat hairy skin. Brain Res 2005, 1059:28-34.
91. Todd A.J., Hughes D.I., Polgár E., Nagy G.G., Mackie M., Ottersen O.P., Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 2003, 17:13-27.
92. Tong Q., Ma J., Kirchgessner A.L. Vesicular glutamate transporter 2 in the brain-gut axis. Neuroreport 2001, 12:3929-3934.
93. Varoqui H., Schafer M.K., Zhu H., Weihe E., Erickson J.D. Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 2002, 22:142-155.
94. Vieytes CA, Lundgren KH, Malet M, Tomasella E, Seroogy KB, Gebhart GF, Hökfelt T, Brumovsky PR (2013). Expression of vesicular glutamate transporters type-1 and -2 in lumbar 4 and 5 dorsal root ganglia - effects of axotomy of the sciatic nerve or hindpaw inflammation. In: 42nd society for neuroscience congress. Ref type: abstract.
95. Waerhaug O., Ottersen O.P. Demonstration of glutamate-like immunoreactivity at rat neuromuscular junctions by quantitative electron microscopic immunocytochemistry. Anat Embryol (Berl) 1993, 188:501-513.
96. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., Yang L., Huang W.J., Fu G., Xu S.H., Cheng X.P., Yan Q., Zhu Z.D., Zhang X., Chen Z., Han Z.G., Zhang X. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci U S A 2002, 99:8360-8365.
97. Xu Z.Q., Shi T.J., Hökfelt T. Expression of galanin and a galanin receptor in several sensory systems and bone anlage of rat embryos. Proc Natl Acad Sci U S A 1996, 93:14901-14905.
98. Yang C.-Q., Wei Y.-Y., Leng Y.-X., Zhong C.-J., Zhang Y.-S., Wan Y., Duan L.-P. Vesicular glutamate transporter-3 contributes to visceral hyperalgesia induced by Trichinella spiralis infection in rats. Dig Dis Sci 2012, 57:865-872.
99. Yasaka T., Tiong S.Y., Hughes D.I., Riddell J.S., Todd A.J. Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 2010, 151:475-488.
100. Zhang X., Bean A.J., Wiesenfeld-Hallin Z., Xu X.J., Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord - III. Effects of peripheral axotomy with special reference to galanin. Neuroscience 1995, 64:893-915.