The glutamatergic system as a target for neuropathic pain relief

Experimental Physiology

Volumn 98, Issue 2, 2013, Pages 372-384

  Osikowicz, Maria ^a   Mika, Joanna ^a   Przewlocka, Barbara ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; 4,6 DICHLORO 3 (2 OXO 1 PHENYL 3 PYRROLIDINYLIDENEMETHYL) 1H INDOLE 2 CARBOXYLIC ACID; 6 METHYL 2 PHENYLAZO 3 PYRIDINOL; AMN 082; ANALGESIC AGENT; DEXTROMETHORPHAN; DIACYLGLYCEROL; DIZOCILPINE; EXCITATORY AMINO ACID TRANSPORTER 3; FENOBAM; GLUTAMIC ACID; KAINIC ACID; KAINIC ACID RECEPTOR; KETAMINE; MEMANTINE; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR 6; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8; METHADONE; MINOCYCLINE; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PENTOXIFYLLINE; PROPENTOFYLLINE; PROTEIN KINASE C; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER;

ANALGESIA; ARTICLE; AUTONOMIC NERVOUS SYSTEM; COMPETITIVE INHIBITION; DOWN REGULATION; DRUG EFFICACY; ENZYME ACTIVATION; EXCITOTOXICITY; GLIA; GLUTAMATERGIC SYSTEM; HUMAN; HYPERALGESIA; NEUROMODULATION; NEUROPATHIC PAIN; NOCICEPTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84872702412     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2012.069922     Document Type: Article

References (124)

1. 2+ signal transduction. J Biol Chem 267, 13361-13368.
2. Agrawal SK, Theriault E & Fehlings MG (1998). Role of group I metabotropic glutamate receptors in traumatic spinal cord white matter injury. J Neurotrauma 15, 929-941.
3. al-Ghoul WM, Volsi GL, Weinberg RJ & Rustioni A (1993). Glutamate immunocytochemistry in the dorsal horn after injury or stimulation of the sciatic nerve of rats. Brain Res Bull 30, 453-459.
4. Araque A, Sanzgiri RP, Parpura V & Haydon PG (1998). Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci 18, 6822-6829.
5. Attwell D (2000). Brain uptake of glutamate: food for thought. J Nutr 130, 1023S-1025S.
6. Attwell PJ, Kaura S, Sigala G, Bradford HF, Croucher MJ, Jane DE & Watkins JC (1995). Blockade of both epileptogenesis and glutamate release by (1S, 3S)-ACPD, a presynaptic glutamate receptor agonist. Brain Res 698, 155-162.
7. Baron R (2000). Peripheral neuropathic pain: from mechanisms to symptoms. Clin J Pain 16, S12-S20.
8. Battaglia G, Monn JA & Schoepp DD (1997). In vivo inhibition of veratridine-evoked release of striatal excitatory amino acids by the group II metabotropic glutamate receptor agonist LY354740 in rats. Neurosci Lett 229, 161-164.
9. Benquet P, Gee CE & Gerber U (2002). Two distinct signaling pathways upregulate NMDA receptor responses via two distinct metabotropic glutamate receptor subtypes. J Neurosci 22, 9679-9686.
10. Berenbaum MC (1989). What is synergy Pharmacol Rev 41, 93-141.
11. Bhave G, Karim F, Carlton SM & Gereau RW 4th (2001). Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci 4, 417-423.
12. Biber K, Laurie DJ, Berthele A, Sommer B, Tölle TR, Gebicke-Härter PJ, van Calker D & Boddeke HW (1999). Expression and signaling of group I metabotropic glutamate receptors in astrocytes and microglia. J Neurochem 72, 1671-1680.
13. Binns BC, Huang Y, Goettl VM, Hackshaw KV & Stephens RL Jr. (2005). Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model. Brain Res 1041, 38-47.
14. Bleakman D, Alt A & Nisenbaum ES (2006). Glutamate receptors and pain. Semin Cell Dev Biol 17, 592-604.
15. Bond A, Jones NM, Hicks CA, Whiffin GM, Ward MA, O'Neill MF, Kingston AE, Monn JA, Ornstein PL, Schoepp DD, Lodge D & O'Neill MJ (2000). Neuroprotective effects of LY379268, a selective mGlu2/3 receptor agonist: investigations into possible mechanism of action in vivo. J Pharmacol Exp Ther 294, 800-809.
16. Budai D & Larson AA (1998). The involvement of metabotropic glutamate receptors in sensory transmission in dorsal horn of the rat spinal cord. Neuroscience 83, 571-580.
17. Carlton SM (2001). Peripheral excitatory amino acids. Curr Opin Pharmacol 1, 52-56.
18. Chen SR & Pan HL (2005). Distinct roles of group III metabotropic glutamate receptors in control of nociception and dorsal horn neurons in normal and nerve-injured rats. J Pharmacol Exp Ther 312, 120-126.
19. Chen W, Mahadomrongkul V, Berger UV, Bassan M, DeSilva T, Tanaka K, Irwin N, Aoki C & Rosenberg PA (2004). The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci, 24, 1136-1148.
20. Chen Z, He Y & Wang ZJ (2012). The beta-lactam antibiotic, ceftriaxone, inhibits the development of opioid-induced hyperalgesia in mice. Neurosci Lett 509, 69-71.
21. Chiechio S, Copani A, Melchiorri D, Canudas AM, Storto M, Calvani M, Nicolai R & Nicoletti F (2004). Metabotropic receptors as targets for drugs of potential use in the treatment of neuropathic pain. J Endocrinol Invest 27, 171-176.
22. Christoph T, Kögel B, Strassburger W & Schug SA (2007). Tramadol has a better potency ratio relative to morphine in neuropathic than in nociceptive pain models. Drugs 8, 51-57.
23. Ciccarelli R, Sureda FX, Casabona G, Di Iorio P, Caruso A, Spinella F, Condorelli DF, Nicoletti F & Caciagli F (1997). Opposite influence of the metabotropic glutamate receptor subtypes mGlu3 and -5 on astrocyte proliferation in culture. Glia 21, 390-398.
24. Danbolt NC (2001). Glutamate uptake. Prog Neurobiol 65, 1-105.
25. Dani JW, Chernjavsky A & Smith SJ (1992). Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8, 429-440.
26. DeLeo JA & Yezierski RP (2001). The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90, 1-6.
27. de Novellis V, Marabese I, Palazzo E, Rossi F, Berrino L, Rodella L, Bianchi R & Maione S (2003). Group I metabotropic glutamate receptors modulate glutamate and γ-aminobutyric acid release in the periaqueductal grey of rats. Eur J Pharmacol 462, 73-81.
28. Devor M (2001). Neuropathic pain: what do we do with all these theories Acta Anaesthesiol Scand 45, 1121-1127.
29. Dingledine R, Borges K, Bowie D & Traynelis SF (1999). The glutamate receptor ion channels. Pharmacol Rev 51, 7-61.
30. Dmitrieva N, Rodríguez-Malaver AJ, Pérez J & Hernández L (2004). Differential release of neurotransmitters from superficial and deep layers of the dorsal horn in response to acute noxious stimulation and inflammation of the rat paw. Eur J Pain 8, 245-252.
31. 5) antagonist, in experimental neuropathic pain in rats. Neurosci Lett 292, 115-118.
32. Dolan S, Kelly JG, Monteiro AM & Nolan AM (2003). Up-regulation of metabotropic glutamate receptor subtypes 3 and 5 in spinal cord in a clinical model of persistent inflammation and hyperalgesia. Pain 106, 501-512.
33. Drew LJ & MacDermott AB (2009). Neuroscience: unbearable lightness of touch. Nature 462, 580-581.
34. Eide K, Stubhaug A, Oye I & Breivik H (1995). Continuous subcutaneous administration of the N-methyl-D-aspartic acid (NMDA) receptor antagonist ketamine in the treatment of post-herpetic neuralgia. Pain 61, 221-228.
35. Ferraguti F, Baldani-Guerra B, Corsi M, Nakanishi S & Corti C (1999). Activation of the extracellular signal-regulated kinase 2 by metabotropic glutamate receptors. Eur J Neurosci 11, 2073-2082.
36. Fisher K & Coderre TJ (1996a). Comparison of nociceptive effects produced by intrathecal administration of mGluR agonists. Neuroreport 7, 2743-2747.
37. Fisher K & Coderre TJ (1996b). The contribution of metabotropic glutamate receptors (mGluRs) to formalin-induced nociception. Pain 68, 255-263.
38. Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA & Edwards RH (2002). The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci U S A 99, 14488-14493.
39. Fundytus ME (2001). Glutamate receptors and nociception: implications for the drug treatment of pain. CNS Drugs 15, 29-58.
40. Fundytus ME, Fisher K, Dray A, Henry JL & Coderre TJ (1998). In vivo antinociceptive activity of anti-rat mGluR1 and mGluR5 antibodies in rats. Neuroreport 9, 731-735.
41. 1) alleviates pain and restores opioid efficacy after nerve injury in rats. Br J Pharmacol 132, 354-367.
42. Gasparini F, Kuhn R & Pin JP (2002). Allosteric modulators of group I metabotropic glutamate receptors: novel subtype-selective ligands and therapeutic perspectives. Curr Opin Pharmacol 2, 43-49.
43. Gerber G, Zhong J, Youn D & Randic M (2000). Group II and group III metabotropic glutamate receptor agonists depress synaptic transmission in the rat spinal cord dorsal horn. Neuroscience 100, 393-406.
44. Glaum SR & Miller RJ (1994). Inhibition of phosphoprotein phosphatases blocks metabotropic glutamate receptor effects in the rat nucleus tractus solitarii. Mol Pharmacol 45, 1221-1226.
45. 2+ signalling in hippocampal neurons. Eur J Neurosci 26, 2481-2495.
46. Goudet C, Chapuy E, Alloui A, Acher F, Pin JP & Eschalier A (2008). Group III metabotropic glutamate receptors inhibit hyperalgesia in animal models of inflammation and neuropathic pain. Pain 137, 112-124.
47. Gras G, Samah B, Hubert A, Léone C, Porcheray F & Rimaniol AC (2012). EAAT expression by macrophages and microglia: still more questions than answers. Amino Acids 42, 221-229.
48. Hanisch UK (2002). Microglia as a source and target of cytokines. Glia 40, 140-155.
49. Herzog E, Bellenchi GC, 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.
50. Hollmann M & Heinemann S (1994). Cloned glutamate receptors. Annu Rev Neurosci 17, 31-108.
51. Hudson LJ, Bevan S, McNair K, Gentry C, Fox A, Kuhn R & Winter J (2002). Metabotropic glutamate receptor 5 upregulation in A-fibers after spinal nerve injury: 2-methyl-6-(phenylethynyl)-pyridine (MPEP) reverses the induced thermal hyperalgesia. J Neurosci 22, 2660-2668.
52. Jensen TS & Baron R (2003). Translation of symptoms and signs into mechanisms in neuropathic pain. Pain 102, 1-8.
53. Jevtovic-Todorovic V, Wozniak DF, Powell S, Nardi A & Olney JW (1998). Clonidine potentiates the neuropathic pain-relieving action of MK-801 while preventing its neurotoxic and hyperactivity side effects. Brain Res 781, 202-211.
54. Ji RR, Baba H, Brenner GJ & Woolf CJ (1999). Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2, 1114-1119.
55. Karim F, Bhave G & Gereau RW 4th (2001). Metabotropic glutamate receptors on peripheral sensory neuron terminals as targets for the development of novel analgesics. Mol Psychiatry 6, 615-617.
56. Kew JN & Kemp JA (2005). Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 179, 4-29.
57. Kozela E, Pilc A & Popik P (2003). Inhibitory effects of MPEP, an mGluR5 antagonist, and memantine, an N-methyl-D-aspartate receptor antagonist, on morphine antinociceptive tolerance in mice. Psychopharmacology (Berl) 165, 245-251.
58. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF & Watkins LR (2005). Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115, 71-83.
59. Leo S, Moechars D, Callaerts-Vegh Z, D'Hooge R & Meert T (2009). Impairment of VGLUT2 but not VGLUT1 signaling reduces neuropathy-induced hypersensitivity. Eur J Pain 13, 1008-1017.
60. Li JL, Fujiyama F, Kaneko T & Mizuno N (2003). 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 457, 236-249.
61. Liberto CM, Albrecht PJ, Herx LM, Yong VW & Levison SW (2004). Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 89, 1092-1100.
62. López-Redondo F, Nakajima K, Honda S & Kohsaka S (2000). Glutamate transporter GLT-1 is highly expressed in activated microglia following facial nerve axotomy. Brain Res Mol Brain Res 76, 429-435.
63. Lorrain DS, Correa L, Anderson J & Varney M (2002). Activation of spinal group I metabotropic glutamate receptors in rats evokes local glutamate release and spontaneous nociceptive behaviors: effects of 2-methyl-6-(phenylethynyl)-pyridine pretreatment. Neurosci Lett 327, 198-202.
64. Mao J, Sung B, Ji RR & Lim G (2002). Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 22, 8312-8323.
65. Marin JC & Goadsby PJ (2010). Glutamatergic fine tuning with ADX-10059: a novel therapeutic approach for migraine Expert Opin Investig Drugs 19, 555-561.
66. Masson J, Sagne C, Hamon M & El Mestikawy S (1999). Neurotransmitter transporters in the central nervous system. Pharmacol Rev 51, 439-464.
67. Masu M, Tanabe Y, Tsuchida K, Shigemoto R & Nakanishi S (1991). Sequence and expression of a metabotropic glutamate receptor. Nature 349, 760-765.
68. Mayer DJ, Mao J & Price DD (1995). The development of morphine tolerance and dependence is associated with translocation of protein kinase C. Pain 61, 365-374.
69. Meldrum BS (2000). Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130, 1007S-1015S.
70. Mika J, Osikowicz M, Makuch W & Przewlocka B (2007). Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur J Pharmacol 560, 142-149.
71. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, Przewlocki R & Przewlocka B (2009). Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol 623, 65-72.
72. Mills CD, Johnson KM & Hulsebosch CE (2002). Role of group II and group III metabotropic glutamate receptors in spinal cord injury. Exp Neurol 173, 153-167.
73. Mills CD, Xu GY, Johnson KM, McAdoo DJ & Hulsebosch CE (2000). AIDA reduces glutamate release and attenuates mechanical allodynia after spinal cord injury. Neuroreport 11, 3067-3070.
74. Mitsukawa K, Yamamoto R, Ofner S, Nozulak J, Pescott O, Lukic S, Stoehr N, Mombereau C, Kuhn R, McAllister KH, van der Putten H, Cryan JF & Flor PJ (2005). A selective metabotropic glutamate receptor 7 agonist: activation of receptor signaling via an allosteric site modulates stress parameters in vivo. Proc Natl Acad Sci U S A 102, 18712-18717.
75. Montana MC, Cavallone LF, Stubbert KK, Stefanescu AD, Kharasch ED & Gereau RWt (2009). The metabotropic glutamate receptor subtype 5 antagonist fenobam is analgesic and has improved in vivo selectivity compared with the prototypical antagonist 2-methyl-6-(phenylethynyl)-pyridine. J Pharmacol Exp Ther 330, 834-843.
76. Moriyama Y & Omote H (2008). Vesicular glutamate transporter acts as a metabolic regulator. Biol Pharm Bull 31, 1844-1846.
77. Moroni F, Cozzi A, Lombardi G, Sourtcheva S, Leonardi P, Carfi M & Pellicciari R (1998). Presynaptic mGlu1 type receptors potentiate transmitter output in the rat cortex. Eur J Pharmacol 347, 189-195.
78. Narita M, Mizoguchi H, Kampine JP & Tseng LF (1996). Role of protein kinase C in desensitization of spinal δ-opioid-mediated antinociception in the mouse. Br J Pharmacol 118, 1829-1835.
79. Narita M, Suzuki M, Niikura K, Nakamura A, Miyatake M, Aoki T, Yajima Y & Suzuki T (2005). Involvement of spinal metabotropic glutamate receptor 5 in the development of tolerance to morphine-induced antinociception. J Neurochem 94, 1297-1305.
80. Neugebauer V (2001). Metabotropic glutamate receptors: novel targets for pain relief. Expert Rev Neurother 1, 207-224.
81. Neugebauer V & Carlton SM (2002). Peripheral metabotropic glutamate receptors as drug targets for pain relief. Expert Opin Ther Targets 6, 349-361.
82. Nichols ML, Lopez Y, Ossipov MH, Bian D & Porreca F (1997). Enhancement of the antiallodynic and antinociceptive efficacy of spinal morphine by antisera to dynorphin A (1-13) or MK-801 in a nerve-ligation model of peripheral neuropathy. Pain 69, 317-322.
83. Ohishi H, Nomura S, Ding YQ, Shigemoto R, Wada E, Kinoshita A, Li JL, Neki A, Nakanishi S & Mizuno N (1995). Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci Lett 202, 85-88.
84. Osikowicz M, Mika J, Makuch W & Przewlocka B (2008). Glutamate receptor ligands attenuate allodynia and hyperalgesia and potentiate morphine effects in a mouse model of neuropathic pain. Pain 139, 117-126.
85. Osikowicz M, Skup M, Mika J, Makuch W, Czarkowska-Bauch J & Przewlocka B (2009). Glial inhibitors influence the mRNA and protein levels of mGlu2/3, 5 and 7 receptors and potentiate the analgesic effects of their ligands in a mouse model of neuropathic pain. Pain 147, 175-186.
86. Ossipov MH, Lopez Y, Nichols ML, Bian D & Porreca F (1995). The loss of antinociceptive efficacy of spinal morphine in rats with nerve ligation injury is prevented by reducing spinal afferent drive. Neurosci Lett 199, 87-90.
87. Parpura V & Haydon PG (2000). Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci U S A 97, 8629-8634.
88. Petralia RS, Wang YX, Niedzielski AS & Wenthold RJ (1996a). The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71, 949-976.
89. Petralia RS, Wang YX, Zhao HM & Wenthold RJ (1996b). Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J Comp Neurol 372, 356-383.
90. Piani D, Frei K, Pfister HW & Fontana A (1993). Glutamate uptake by astrocytes is inhibited by reactive oxygen intermediates but not by other macrophage-derived molecules including cytokines, leukotrienes or platelet-activating factor. J Neuroimmunol 48, 99-104.
91. Pin JP & Duvoisin R (1995). The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 1-26.
92. Pitcher MH, Ribeiro-da-Silva A & Coderre TJ (2007). Effects of inflammation on the ultrastructural localization of spinal cord dorsal horn group I metabotropic glutamate receptors. J Comp Neurol 505, 412-423.
93. Porreca F, Tang QB, Bian D, Riedl M, Elde R & Lai J (1998). Spinal opioid mu receptor expression in lumbar spinal cord of rats following nerve injury. Brain Res 795, 197-203.
94. Ren BX, Gu XP, Zheng YG, Liu CL, Wang D, Sun YE & Ma ZL (2012). Intrathecal injection of metabotropic glutamate receptor subtype 3 and 5 agonist/antagonist attenuates bone cancer pain by inhibition of spinal astrocyte activation in a mouse model. Anesthesiology 116, 122-132.
95. Rossi DJ, Oshima T & Attwell D (2000). Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403, 316-321.
96. Schoepp DD, Jane DE & Monn JA (1999). Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476.
97. Sharpe EF, Kingston AE, Lodge D, Monn JA & Headley PM (2002). Systemic pre-treatment with a group II mGlu agonist, LY379268, reduces hyperalgesia in vivo. Br J Pharmacol 135, 1255-1262.
98. Shen CH, Tsai RY, Tai YH, Lin SL, Chien CC & Wong CS (2011). Intrathecal etanercept partially restores morphine's antinociception in morphine-tolerant rats via attenuation of the glutamatergic transmission. Anesth Analg 113, 184-190.
99. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S & Mizuno N (1997). Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17, 7503-7522.
100. Simmons RM, Webster AA, Kalra AB & Iyengar S (2002). Group II mGluR receptor agonists are effective in persistent and neuropathic pain models in rats. Pharmacol Biochem Behav 73, 419-427.
101. Smith EL, Whedon MB & Bookbinder M (2002). Quality improvement of painful peripheral neuropathy. Semin Oncol Nurs 18, 36-43.
102. Smith GD, Wiseman J, Harrison SM, Elliott PJ & Birch PJ (1994). Pre treatment with MK-801, a non-competitive NMDA antagonist, prevents development of mechanical hyperalgesia in a rat model of chronic neuropathy, but not in a model of chronic inflammation. Neurosci Lett 165, 79-83.
103. Stanfa LC & Dickenson AH (1998). Inflammation alters the effects of mGlu receptor agonists on spinal nociceptive neurones. Eur J Pharmacol 347, 165-172.
104. Sung B, Lim G & Mao J (2003). 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.
105. Sweitzer SM, Schubert P & DeLeo JA (2001). Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther 297, 1210-1217.
106. Tamaru Y, Nomura S, Mizuno N & Shigemoto R (2001). Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106, 481-503.
107. Tapiero H, Mathé G, Couvreur P & Tew KD (2002). II. Glutamine and glutamate. Biomed Pharmacother 56, 446-457.
108. Tawfik VL, Regan MR, Haenggeli C, Lacroix-Fralish ML, Nutile-McMenemy N, Perez N, Rothstein JD & DeLeo JA (2008). Propentofylline-induced astrocyte modulation leads to alterations in glial glutamate promoter activation following spinal nerve transection. Neuroscience 152, 1086-1092.
109. Taylor DL, Diemel LT, Cuzner ML & Pocock JM (2002). Activation of group II metabotropic glutamate receptors underlies microglial reactivity and neurotoxicity following stimulation with chromogranin A, a peptide up-regulated in Alzheimer's disease. J Neurochem 82, 1179-1191.
110. Tzschentke TM (2002). Glutamatergic mechanisms in different disease states: overview and therapeutical implications - an introduction. Amino Acids 23, 147-152.
111. Urban MO, Hama AT, Bradbury M, Anderson J, Varney MA & Bristow L (2003). Role of metabotropic glutamate receptor subtype 5 (mGluR5) in the maintenance of cold hypersensitivity following a peripheral mononeuropathy in the rat. Neuropharmacology 44, 983-993.
112. Walker K, Bowes M, Panesar M, Davis A, Gentry C, Kesingland A, Gasparini F, Spooren W, Stoehr N, Pagano A, Flor PJ, Vranesic I, Lingenhoehl K, Johnson EC, Varney M, Urban L & Kuhn R (2001a). Metabotropic glutamate receptor subtype 5 (mGlu5) and nociceptive function. I. Selective blockade of mGlu5 receptors in models of acute, persistent and chronic pain. Neuropharmacology 40, 1-9.
113. Walker K, Reeve A, Bowes M, Winter J, Wotherspoon G, Davis A, Schmid P, Gasparini F, Kuhn R & Urban L (2001b). mGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurones mediate inflammatory hyperalgesia. Neuropharmacology 40, 10-19.
114. Wen YR, Tan PH, Cheng JK, Liu YC & Ji RR (2011). Microglia: a promising target for treating neuropathic and postoperative pain, and morphine tolerance. J Formos Med Assoc 110, 487-494.
115. Weng HR, Chen JH, Pan ZZ & Nie H (2007). Glial glutamate transporter 1 regulates the spatial and temporal coding of glutamatergic synaptic transmission in spinal lamina II neurons. Neuroscience 149, 898-907.
116. Yamamoto T, Hirasawa S, Wroblewska B, Grajkowska E, Zhou J, Kozikowski A, Wroblewski J & Neale JH (2004). Antinociceptive effects of N-acetylaspartylglutamate (NAAG) peptidase inhibitors ZJ-11, ZJ-17 and ZJ-43 in the rat formalin test and in the rat neuropathic pain model. Eur J Neurosci 20, 483-494.
117. Yang CP, Cherng CH, Wu CT, Huang HY, Tao PL & Wong CS (2011). Intrathecal ultra-low dose naloxone enhances the antinociceptive effect of morphine by enhancing the reuptake of excitatory amino acids from the synaptic cleft in the spinal cord of partial sciatic nerve-transected rats. Anesth Analg 113, 1490-1500.
118. Young MR, Fleetwood-Walker SM, Dickinson T, Blackburn-Munro G, Sparrow H, Birch PJ & Bountra C (1997). Behavioural and electrophysiological evidence supporting a role for group I metabotropic glutamate receptors in the mediation of nociceptive inputs to the rat spinal cord. Brain Res 777, 161-169.
119. Zammataro M, Chiechio S, Montana MC, Traficante A, Copani A, Nicoletti F & Gereau RW 4th (2011). mGlu2 metabotropic glutamate receptors restrain inflammatory pain and mediate the analgesic activity of dual mGlu2/mGlu3 receptor agonists. Mol Pain 7, 6.
120. Zhang H, Yoon SY & Dougherty PM (2012). Evidence that spinal astrocytes but not microglia contribute to the pathogenesis of Paclitaxel-induced painful neuropathy. J Pain 13, 293-303.
121. Zhou S, Komak S, Du J & Carlton SM (2001). Metabotropic glutamate 1α receptors on peripheral primary afferent fibers: their role in nociception. Brain Res 913, 18-26.
122. Zhu CZ, Wilson SG, Mikusa JP, Wismer CT, Gauvin DM, Lynch JJ 3rd, Wade CL, Decker MW & Honore P (2004). Assessing the role of metabotropic glutamate receptor 5 in multiple nociceptive modalities. Eur J Pharmacol 506, 107-118.
123. Zhuang ZY, Gerner P, Woolf CJ & Ji RR (2005). ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114, 149-159.
124. Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T & Carmignoto G (2003). Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553, 407-414.