Functional plasticity of group II metabotropic glutamate receptors in regulating spinal excitatory and inhibitory synaptic input in neuropathic pain

Journal of Pharmacology and Experimental Therapeutics

Volumn 336, Issue 1, 2011, Pages 254-264

  Zhou, Hong Yi ^a   Chen, Shao Rui ^a   Chen, Hong ^a   Pan, Hui Lin ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; ALPHA ETHYLGLUTAMIC ACID; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG DEPENDENCE; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPERALGESIA; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE CELL PLASTICITY; NERVE INJURY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; NEURAL INHIBITION; NEURALGIA; NEURONAL PLASTICITY; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SPINAL CORD; SYNAPSES;

EID: 78650797715     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.110.173112     Document Type: Article

References (57)

1. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29:83-120.
2. Breakwell NA, Huang L, Rowan MJ, and Anwyl R (1997) DCG-IV inhibits synaptic transmission by activation of NMDA receptors in area CA1 of rat hippocampus. Eur J Pharmacol 322:173-178.
3. Carlton SM, Hargett GL, and Coggeshall RE (2001) Localization of metabotropic glutamate receptors 2/3 on primary afferent axons in the rat. Neuroscience 105: 957-969.
4. Castro-Lopes JM, Tavares I, and Coimbra A (1993) GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res 620:287-291.
5. Cervero F and Iggo A (1980) The substantia gelatinosa of the spinal cord: a critical review. Brain 103:717-772.
6. Chaplan SR, Malmberg AB, and Yaksh TL (1997) Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 280:829-838.
7. Chen SR and Pan HL (2005) Distinct roles of group III metabotropic glutamate receptors in control of nociception and dorsal horn neurons in normal and nerveinjured Rats. J Pharmacol Exp Ther 312:120-126.
8. Chen SR and Pan HL (2006) Loss of TRPV1-expressing sensory neurons reduces spinal mu opioid receptors but paradoxically potentiates opioid analgesia. J Neurophysiol 95:3086-3096.
9. Chen SR, Cai YQ, and Pan HL (2009a) Plasticity and emerging role of BKCa channels in nociceptive control in neuropathic pain. J Neurochem 110:352-362.
10. Chen SR, Eisenach JC, McCaslin PP, and Pan HL (2000) Synergistic effect between intrathecal non-NMDA antagonist and gabapentin on allodynia induced by spinal nerve ligation in rats. Anesthesiology 92:500-506.
11. Chen SR, Samoriski G, and Pan HL (2009b) Antinociceptive effects of chronic administration of uncompetitive NMDA receptor antagonists in a rat model of diabetic neuropathic pain. Neuropharmacology 57:121-126.
12. Conn PJ and Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
13. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, and De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017-1021.
14. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sîk A, De Koninck P, and De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424:938-942.
15. Everill B and Kocsis JD (1999) Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J Neurophysiol 82: 700-708.
16. Fisher K, Lefebvre C, and Coderre TJ (2002) Antinociceptive effects following intrathecal pretreatment with selective metabotropic glutamate receptor compounds in a rat model of neuropathic pain. Pharmacol Biochem Behav 73:411-418.
17. Gerber G, Zhong J, Youn D, and 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.
18. Gracely RH, Lynch SA, and Bennett GJ (1992) Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51:175-194.
19. Hayashi Y, Sekiyama N, Nakanishi S, Jane DE, Sunter DC, Birse EF, Udvarhelyi PM, and Watkins JC (1994) Analysis of agonist and antagonist activities of phenylglycine derivatives for different cloned metabotropic glutamate receptor subtypes. J Neurosci 14:3370-3377.
20. Heinke B and Sandkühler J (2007) Group I metabotropic glutamate receptor-induced Ca(2+)-gradients in rat superficial spinal dorsal horn neurons. Neuropharmacology 52:1015-1023.
21. Hermanns H, Muth-Selbach U, Lipfert P, Braun S, Werdehausen R, and Bauer I (2009) Loss of spinal glycinergic neurons is not necessary for development of neuropathic pain in transgenic mice expressing enhanced green fluorescent protein in glycinergic neurons. Neuroscience 159:1148-1153.
22. Ibuki T, Hama AT, Wang XT, Pappas GD, and Sagen J (1997) Loss of GABAimmunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 76:845-858.
23. Ishida M, Saitoh T, and Shinozaki H (1993a) A new metabotropic glutamate receptor agonist: developmental change of its sensitivity to receptors in the newborn rat spinal cord. Neurosci Lett 160:156-158.
24. Ishida M, Saitoh T, Shimamoto K, Ohfune Y, and Shinozaki H (1993b) A novel metabotropic glutamate receptor agonist: marked depression of monosynaptic excitation in the newborn rat isolated spinal cord. Br J Pharmacol 109:1169-1177. (Pubitemid 23216788)
25. Jane DE, Thomas NK, Tse HW, and Watkins JC (1996) Potent antagonists at the L-AP4- and (1S,3S)-ACPD-sensitive presynaptic metabotropic glutamate receptors in the neonatal rat spinal cord. Neuropharmacology 35:1029-1035.
26. Jia H, Rustioni A, and Valtschanoff JG (1999) Metabotropic glutamate receptors in superficial laminae of the rat dorsal horn. J Comp Neurol 410:627-642.
27. Kim DS, Choi JO, Rim HD, and Cho HJ (2002) Down-regulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res Mol Brain Res 105:146-152.
28. Kim SH and Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
29. Kohno T, Moore KA, Baba H, and Woolf CJ (2003) Peripheral nerve injury alters excitatory synaptic transmission in lamina II of the rat dorsal horn. J Physiol 548:131-138.
30. Kumar N, Laferriere A, Yu JS, Poon T, and Coderre TJ (2010) Metabotropic glutamate receptors (mGluRs) regulate noxious stimulus-induced glutamate release in the spinal cord dorsal horn of rats with neuropathic and inflammatory pain. J Neurochem 114:281-290.
31. Li JQ, Chen SR, Chen H, Cai YQ, and Pan HL (2010) Regulation of increased glutamatergic input to spinal dorsal horn neurons by mGluR5 in diabetic neuropathic pain. J Neurochem 112:162-172.
32. Liu H, Mantyh PW, and Basbaum AI (1997) NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature 386:721-724.
33. Lu Y and Perl ER (2003) A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 23:8752-8758.
34. Matzner O and Devor M (1994) Hyperexcitability at sites of nerve injury depends on voltage-sensitive Na+ channels. J Neurophysiol 72:349-359.
35. Monn JA, Valli MJ, Massey SM, Hansen MM, Kress TJ, Wepsiec JP, Harkness AR, Grutsch JL Jr, Wright RA, Johnson BG, et al. (1999) Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0]hexane-2,6-dicarboxylic acid (LY354740): identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors. J Med Chem 42:1027-1040.
36. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, and Woolf CJ (2002) Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 22:6724-6731.
37. Polgár E, Hughes DI, Arham AZ, and Todd AJ (2005) Loss of neurons from laminas I-III of the spinal dorsal horn is not required for development of tactile allodynia in the spared nerve injury model of neuropathic pain. J Neurosci 25:6658-6666.
38. Polgár E, Hughes DI, Riddell JS, Maxwell DJ, Puskár Z, and Todd AJ (2003) Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 104:229-239.
39. Santos SF, Rebelo S, Derkach VA, and Safronov BV (2007) Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J Physiol 581:241-254.
40. Sarantopoulos CD, McCallum JB, Rigaud M, Fuchs A, Kwok WM, and Hogan QH (2007) Opposing effects of spinal nerve ligation on calcium-activated potassium currents in axotomized and adjacent mammalian primary afferent neurons. Brain Res 1132:84-99.
41. Schoepp DD, Jane DE, and Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38:1431-1476.
42. Schoppa NE and Westbrook GL (1997) Modulation of mEPSCs in olfactory bulb mitral cells by metabotropic glutamate receptors. J Neurophysiol 78:1468-1475.
43. Simmons RM, Webster AA, Kalra AB, and Iyengar S (2002) Group II mGluR receptor agonists are effective in persistent and neuropathic pain models in rats. Pharmacol Biochem Behav 73:419-427.
44. Sorkin LS, Puig S, and Jones DL (1998) Spinal bicuculline produces hypersensitivity of dorsal horn neurons: effects of excitatory amino acid antagonists. Pain 77:181-190.
45. Todd AJ (1996) GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur J Neurosci 8:2492-2498.
46. Todd AJ and Sullivan AC (1990) Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496-505.
47. Wang XL, Zhang HM, Chen SR, and Pan HL (2007) Altered synaptic input and GABAB receptor function in spinal superficial dorsal horn neurons in rats with diabetic neuropathy. J Physiol 579:849-861.
48. Wang XL, Zhang HM, Li DP, Chen SR, and Pan HL (2006) Dynamic regulation of glycinergic input to spinal dorsal horn neurones by muscarinic receptor subtypes in rats. J Physiol 571:403-413.
49. Wu S, Wright RA, Rockey PK, Burgett SG, Arnold JS, Rosteck PR Jr, Johnson BG, Schoepp DD, and Belagaje RM (1998) Group III human metabotropic glutamate receptors 4, 7 and 8: molecular cloning, functional expression, and comparison of pharmacological properties in RGT cells. Brain Res Mol Brain Res 53:88-97.
50. Yaksh TL (1989) Behavioral and autonomic correlates of the tactile evoked allodynia produced by spinal glycine inhibition: effects of modulatory receptor systems and excitatory amino acid antagonists. Pain 37:111-123.
51. Zhang HM, Chen SR, and Pan HL (2009) Effects of activation of group III metabotropic glutamate receptors on spinal synaptic transmission in a rat model of neuropathic pain. Neuroscience 158:875-884.
52. Zhang HM, Li DP, Chen SR, and Pan HL (2005) M2, M3, and M4 receptor subtypes contribute to muscarinic potentiation of GABAergic inputs to spinal dorsal horn neurons. J Pharmacol Exp Ther 313:697-704.
53. Zhou HY, Chen SR, Chen H, and Pan HL (2008a) Sustained inhibition of neurotransmitter release from nontransient receptor potential vanilloid type 1-expressing primary afferents by mu-opioid receptor activation-enkephalin in the spinal cord. J Pharmacol Exp Ther 327:375-382.
54. Zhou HY, Chen SR, Chen H, and Pan HL (2009) The glutamatergic nature of TRPV1-expressing neurons in the spinal dorsal horn. J Neurochem 108:305-318.
55. Zhou HY, Chen SR, Chen H, and Pan HL (2010) Opioid-induced long-term potentiation in the spinal cord is a presynaptic event. J Neurosci 30:4460-4466.
56. Zhou HY, Zhang HM, Chen SR, and Pan HL (2007) Increased nociceptive input rapidly modulates spinal GABAergic transmission through endogenously released glutamate. J Neurophysiol 97:871-882.
57. Zhou HY, Zhang HM, Chen SR, and Pan HL (2008b) Increased C-fiber nociceptive input potentiates inhibitory glycinergic transmission in the spinal dorsal horn. J Pharmacol Exp Ther 324:1000-1010.