Glutamate transporter dysfunction associated with nerve injury-induced pain in mice

Journal of Neurophysiology

Volumn 107, Issue 2, 2012, Pages 649-657

  Napier, Ian A ^a   Mohammadi, Sarasa A ^a   Christie, Macdonald J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Dorsal horn; Spillover; Spinal cord

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOHISTOCHEMISTRY; NEUROPATHIC PAIN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCIATIC NERVE; SPINAL CORD TRANSSECTION;

AMINO ACID TRANSPORT SYSTEM X-AG; ANALYSIS OF VARIANCE; ANIMALS; AREA UNDER CURVE; ASPARTIC ACID; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICE; MICE, INBRED C57BL; NEURONS; SCIATICA; SPINAL CORD; TIME FACTORS;

EID: 84855371238     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00763.2011     Document Type: Article

References (44)

1. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107, 1988.
2. Beurrier C, Bonvento G, Kerkerian-Le Goff L, Gubellini P. Role of glutamate transporters in corticostriatal synaptic transmission. Neuroscience 158: 1608-1615, 2009.
3. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15: 711-720, 1995.
4. Coyle DE. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23: 75-83, 1988.
5. Danbolt NC. Glutamate uptake. Prog Neurobiol 65: 1-105, 2001.
6. Dingledine R, Borges K Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61, 1999.
7. Drew GM, Mitchell VA, Vaughan CW. Glutamate spillover modulates GABAergic synaptic transmission in the rat midbrain periaqueductal grey via metabotropic glutamate receptors and endocannabinoid signaling. J Neurosci 28: 808-815, 2008.
8. Feldmeyer D, Lubke J, Silver RA, Sakmann B. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol 538: 803-822, 2002.
9. Galik J, Youn DH, Kolaj M, Randi ́c M. Involvement of group I metabotropic glutamate receptors and glutamate transporters in the slow excitatory synaptic transmission in the spinal cord dorsal horn. Neuroscience 154: 1372-1387, 2008.
10. Garry EM, Moss A, Rosie R, Delaney A, Mitchell R, Fleetwood-Walker SM. Specific involvement in neuropathic pain of AMPA receptors and adapter proteins for the GluR2 subunit. Mol Cell Neurosci 24: 10-22, 2003.
11. Graham BA, Brichta AM, Callister RJ. Moving from an averaged to specific view of spinal cord pain processing circuits. J Neurophysiol 98: 1057-1063, 2007.
12. Grosskreutz J, Zoerner A, Schlesinger F, Krampfl K, Dengler R, Bufler J. Kinetic properties of human AMPA-type glutamate receptors expressed in HEK293 cells. Eur J Neurosci 17: 1173-1178, 2003.
13. Harris JA, Corsi M, Quartaroli M, Arban R, Bentivoglio M. Upregulation of spinal glutamate receptors in chronic pain. Neuroscience 74: 7-12, 1996.
14. Liaw WJ, Stephens RL Jr, Binns BC, Chu Y, Sepkuty JP, Johns RA, Rothstein JD, Tao YX. Spinal glutamate uptake is critical for maintaining normal sensory transmission in rat spinal cord. Pain 115: 60-70, 2005.
15. Maeda S, Kawamoto A, Yatani Y, Shirakawa H, Nakagawa T, Kaneko S. Gene transfer of GLT-1, a glial glutamate transporter, into the spinal cord by recombinant adenovirus attenuates inflammatory and neuropathic pain in rats. Mol Pain 4: 65, 2008.
16. Malmberg AB, Basbaum AI. Partial sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral and neuroanatomical correlates. Pain 76: 215-222, 1998.
17. Narita M, Yoshida T, Nakajima M, Narita M, Miyatake M, Takagi T, Yajima Y, Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem 97: 1337-1348, 2006.
18. Nie H, Weng HR. Glutamate transporters prevent excessive activation of NMDA receptors and extrasynaptic glutamate spillover in the spinal dorsal horn. J Neurophysiol 101: 2041-2051, 2009.
19. Nie H, Weng HR. Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats. J Neurophysiol 103: 2570-2580, 2010.
20. Peghini P, Janzen J, Stoffel W. Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16: 3822-3832, 1997.
21. Perrais D, Veran J, Mulle C. Gating and permeation of kainate receptors: differences unveiled. Trends Pharmacol Sci 31: 516-522, 2010.
22. Popratiloff A, Weinberg RJ, Rustioni A. AMPA receptors at primary afferent synapses in substantia gelatinosa after sciatic nerve section. Eur J Neurosci 10: 3220-3230, 1998.
23. Rigaud M, Gemes G, Barabas ME, Chernoff DI, Abram SE, Stucky CL, Hogan QH. Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain 136: 188-201, 2008.
24. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16: 675-686, 1996.
25. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725, 1994.
26. Sandkuhler J. Understanding LTP in pain pathways. Mol Pain 3: 9, 2007.
27. Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368, 2007.
28. Seltzer Z, Dubner R, Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43: 205-218, 1990.
29. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T. DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53: 195-201, 1998.
30. Stoffel W, Korner R, Wachtmann D, Keller BU. Functional analysis of glutamate transporters in excitatory synaptic transmission of GLAST1 and GLAST1/EAAC1 deficient mice. Brain Res Mol Brain Res 128: 170-181, 2004.
31. Strickland IT, Martindale JC, Woodhams PL, Reeve AJ, Chessell IP, McQueen DS. Changes in the expression of NaV1.7, NaV18 and NaV19 in a distinct population of dorsal root ganglia innervating the rat knee joint in a model of chronic inflammatory joint pain. Eur J Pain 12: 564-572, 2008.
32. Stubblefield EA, Benke TA. Distinct AMPA-type glutamatergic synapses in developing rat CA1 hippocampus. J Neurophysiol 104: 1899-1912, 2010.
33. Sun W, Hoffman KM, Holley DC, Kavanaugh MP. Specificity and actions of an arylaspartate inhibitor of glutamate transport at the schaffer collateral-CA1 pyramidal cell synapse. PLos One 6: e23765, 2011.
34. 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 23: 2899-2910, 2003.
35. Sung B, Wang S, Zhou B, Lim G, Yang L, Zeng Q, Lim JA, Wang JD, Kang JX, Mao J. Altered spinal arachidonic acid turnover after peripheral nerve injury regulates regional glutamate concentration and neuropathic pain behaviors in rats. Pain 131: 121-131, 2007.
36. Tao YX. Dorsal horn alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking in inflammatory pain. Anesthesiology 112: 1259-1265, 2010.
37. Tawfik VL, Regan MR, Haenggeli C, Lacroix-Fralish ML, Nutile-McMenemy N, Perez N, Rothstein JD, DeLeo JA. Propentofylline-induced astrocyte modulation leads to alterations in glial glutamate promoter activation following spinal nerve transection. Neuroscience 152: 1086-1092, 2008.
38. Tsuda M, Inoue K, Salter MW. Neuropathic pain and spinal microglia: a big problem from molecules in small glia. Trends Neurosci 28: 101-107, 2005.
39. 2+-permeable AMPA and reduced NR2B NMDA receptor-mediated neurotransmission at dorsal horn nociceptive synapses during inflammatory pain in the rat. J Physiol 586: 515-527, 2008.
40. Wang S, Lim G, Yang L, Sung B, Mao J. Downregulation of spinal glutamate transporter EAAC1 following nerve injury is regulated by central glucocorticoid receptors in rats. Pain 120: 78-85, 2006.
41. Wang W, Wang Y, Wang Y, Huang J, Wu S, Li YQ. Temporal changes of astrocyte activation and glutamate transporter-1 expression in the spinal cord after spinal nerve ligation-induced neuropathic pain. Anat Rec (Hoboken) 291: 513-518, 2008.
42. Weng HR, Chen JH, Cata JP. Inhibition of glutamate uptake in the spinal cord induces hyperalgesia and increased responses of spinal dorsal horn neurons to peripheral afferent stimulation. Neuroscience 138: 1351-1360, 2006.
43. Xin WJ, Weng HR, Dougherty PM. Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation. Mol Pain 5: 15, 2009.
44. Yang L, Zhang FX, Huang F, Lu YJ, Li GD, Bao L, Xiao HS, Zhang X. Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur J Neurosci 19: 871-883, 2004.