The Journal of Pain
Volume 11, Issue 4 , Pages 321-329 , April 2010

Differential Roles of Peripheral Metabotropic Glutamate Receptors in Bee Venom-Induced Nociception and Inflammation in Conscious Rats

Received 22 December 2008 ,Revised 3 June 2009 ,Accepted 30 July 2009.

References 

  1. Adwanikar H, Karim F, Gereau RW. Inflammation persistently enhances nocifensive behaviors mediated by spinal group I mGluRs through sustained ERK activation. Pain. 2004;111:125–135
  2. Ahn DK, Kim KH, Jung CY, Choi HS, Lim EJ, Youn DH, et al. Role of peripheral group I and II metabotropic glutamate receptors in IL-1beta-induced mechanical allodynia in the orofacial area of conscious rats. Pain. 2005;118:53–60
  3. Bhave G, Karim F, Carlton SM, Gereau RW. Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci. 2001;4:417–423
  4. Carlton SM. Peripheral excitatory amino acids. Curr Opin Pharmacol. 2001;1:52–56
  5. Carlton SM, Hargett GL. Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells. J Comp Neurol. 2007;501:780–789
  6. Carlton SM, Hargett GL, Coggeshall RE. Localization of metabotropic glutamate receptors 2/3 on primary afferent axons in the rat. Neuroscience. 2001;105:957–969
  7. Chen HS, He X, Qu F, Kang SM, Yu Y, Liao D, et al. Differential roles of peripheral MAPK signal transduction pathways in bee venom-induced nociception and inflammation in conscious rats. J Pain. 2009;10:201–207
  8. Chen HS, He X, Wang Y, Wen WW, You HJ, Arendt-Nielsen L. Roles of capsaicin-sensitive primary afferents in differential rat models of inflammatory pain: A systematic comparative study in conscious rats. Experimental Neurology. 2007;204:244–251
  9. Chen HS, Lei J, He X, Qu F, Wang Y, Wen WW, et al. Peripheral involvement of PKA and PKC in subcutaneous bee venom-induced persistent nociception, mechanical hyperalgesia, and inflammation in rats. Pain. 2008;135:31–36
  10. Chen HS, Lei J, He X, Wang Y, Wen WW, Wei XZ, et al. Pivotal involvement of neurogenic mechanism in subcutaneous bee venom induced inflammation and allodynia in unanesthetized conscious rats. Experimental Neurology. 2006;200:386–391
  11. Chen HS, Li MM, Shi J, Chen J. Supraspinal contribution to development of both tonic nociception and referred mirror hyperalgesia: A comparative study between formalin test and bee venom test in the rat. Anesthesiology. 2003;98:1231–1236
  12. Chen J, Li HL, Luo C, Li Z, Zheng J. Involvement of peripheral NMDA and non-NMDA receptors in development of persistent firing of spinal wide-dynamic-range neurons induced by subcutaneous bee venom injection in the cat. Brain Res. 1999;844:98–105
  13. Chiechio S, Copani A, Melchiorri D, Canudas AM, Storto M, Calvani M, et al. Metabotropic receptors as targets for drugs of potential use in the treatment of neuropathic pain. J Endocrinol Invest. 2004;27:171–176
  14. Conn PJ, Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol. 1997;37:205–237
  15. Dogrul A, Ossipov MH, Lai J, Malan TP, Porreca F. Peripheral and spinal antihyperalgesic activity of SIB-1757, a metabotropic glutamate receptor (mGLUR(5)) antagonist, in experimental neuropathic pain in rats. Neurosci Lett. 2000;292:115–118
  16. Dolan S, Nolan AM. Behavioral evidence supporting a differential role for spinal group I and II metabotropic glutamate receptors in inflammatory hyperalgesia in sheep. Neuropharmacology. 2002;43:319–326
  17. Du J, Zhou S, Carlton SM. Group II metabotropic glutamate receptor activation attenuates peripheral sensitization in inflammatory states. Neuroscience. 2008;154:754–766
  18. El-Kouhen O, Lehto SG, Pan JB, Chang R, Baker SJ, Zhong C, et al. Blockade of mGluR1 receptor results in analgesia and disruption of motor and cognitive performances: Effects of A-841720, a novel non-competitive mGluR1 receptor antagonist. Br J Pharmacol. 2006;149:761–774
  19. Fisher K, Coderre TJ. The contribution of metabotropic glutamate receptors (mGluRs) to formalin-induced nociception. Pain. 1996;68:255–263
  20. Fisher K, Fundytus ME, Cahill CM, Coderre TJ. Intrathecal administration of the mGluR compound, (S)-4CPG, attenuates hyperalgesia and allodynia associated with sciatic nerve constriction injury in rats. Pain. 1998;77:59–66
  21. Fisher K, Lefebvre C, Coderre TJ. Antinociceptive effects following intrathecal pretreatment with selective metabotropic glutamate receptor compounds in a rat model of neuropathic pain. Pharmacol Biochem Behav. 2002;73:411–418
  22. Fundytus ME. Glutamate receptors and nociception: Implications for the drug treatment of pain. CNS Drugs. 2001;15:29–58
  23. Goudet C, Chapuy E, Alloui A, Acher F, Pin JP, Eschalier A. Group III metabotropic glutamate receptors inhibit hyperalgesia in animal models of inflammation and neuropathic pain. Pain. 2008;137:112–124
  24. Hama AT. Acute activation of the spinal cord metabotropic glutamate subtype-5 receptor leads to cold hypersensitivity in the rat. Neuropharmacology. 2003;44:423–430
  25. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron. 2002;36:57–68
  26. Jones CK, Eberle EL, Peters SC, Monn JA, Shannon HE, Fisher K, et al. The contribution of metabotropic glutamate receptors (mGluRs) to formalin-induced nociception. NeuroReport. 1996;7:2743–2747
  27. Jones CK, Eberle EL, Peters SC, Monn JA, Shannon HE. Analgesic effects of the selective group II (mGlu2/3) metabotropic glutamate receptor agonists LY379268 and LY389795 in persistent and inflammatory pain models after acute and repeated dosing. Neuropharmacology. 2005;49:206–218
  28. Jung CY, Choi HS, Ju JS, Park HS, Kwon TG, Bae YC, et al. Central metabotropic glutamate receptors differentially participate in interleukin-1beta-induced mechanical allodynia in the orofacial area of conscious rats. J Pain. 2006;7:747–756
  29. Jung CY, Lee SY, Choi HS, Lim EJ, Lee MK, Yang GY, et al. Participation of peripheral group I and II metabotropic glutamate receptors in the development or maintenance of IL-1beta-induced mechanical allodynia in the orofacial area of conscious rats. Neurosci Lett. 2006;409:173–178
  30. Kohara A, Nagakura Y, Kiso T, Toya T, Watabiki T, Tamura S, et al. Antinociceptive profile of a selective metabotropic glutamate receptor 1 antagonist YM-230888 in chronic pain rodent models. Eur J Pharmacol. 2007;571:8–16
  31. Lee HJ, Choi HS, Ju JS, Bae YC, Kim SK, Yoon YW, et al. Peripheral mGluR5 antagonist attenuated craniofacial muscle pain and inflammation but not mGluR1 antagonist in lightly anesthetized rats. Brain Res Bull. 2006;70:378–385
  32. Lee MK, Choi BY, Yang GY, Jeon HJ, Kyung HM, Kwon OW, et al. Low doses of cannabinoids enhance the antinociceptive effects of intracisternally administered mGluRs groups II and III agonists in formalin-induced TMJ nociception in rats. Pain. 2008;139:367–375
  33. Lee KS, Kim J, Yoon YW, Lee MG, Hong SK, Han HC. The peripheral role of group I metabotropic glutamate receptors on nociceptive behaviors in rats with knee joint inflammation. Neurosci Lett. 2007;416:123–127
  34. Lee JS, Ro JY. Peripheral metabotropic glutamate receptor 5 mediates mechanical hypersensitivity in craniofacial muscle via protein kinase C dependent mechanisms. Neuroscience. 2007;146:375–383
  35. Li H, Ohishi H, Kinoshita A, Shigemoto R, Nomura S, Mizuno N. Localization of a metabotropic glutamate receptor, mGluR7, in axon terminals of presumed nociceptive, primary afferent fibers in the superficial layers of the spinal dorsal horn: An electron microscope study in the rat. Neurosci Lett. 1997;223:153–156
  36. Li JL, Ohishi H, Kaneko T, Shigemoto R, Neki A, Nakanishi S, et al. Immunohistochemical localization of a metabotropic glutamate receptor, mGluR7, in ganglion neurons of the rat; with special reference to the presence in glutamatergic ganglion neurons. Neurosci Lett. 1996;204:9–12
  37. Marabese I, de Novellis V, Palazzo E, Scafuro MA, Vita D, Rossi F, et al. Effects of (S)-3,4-DCPG, an mGlu8 receptor agonist, on inflammatory and neuropathic pain in mice. Neuropharmacology. 2007;52:253–262
  38. Nagy I, Santha P, Jancso G, Urban L. The role of the vanilloid (capsaicin) receptor (TRPV1) in physiology and pathology. Eur J Pharmacol. 2004;500:351–369
  39. Neugebauer V. Glutamate receptor ligands. Handb Exp Pharmacol. 2007;177:217–249
  40. Neugebauer V, Chen PS, Willis WD. Groups II and III metabotropic glutamate receptors differentially modulate brief and prolonged nociception in primate STT cells. J Neurophysiol. 2000;84:2998–3009
  41. Neugebauer V, Chen PS, Willis WD. Role of metabotropic glutamate receptor subtype mGluR1 in brief nociception and central sensitization of primate STT cells. J Neurophysiol. 1999;82:272–282
  42. Ohishi H, Nomura S, Ding YQ, Shigemoto R, Wada E, Kinoshita A, et al. Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: An immunohistochemical study in the rat. Neurosci Lett. 1995;202:85–88
  43. Sevostianova N, Danysz W. Analgesic effects of mGlu1 and mGlu5 receptor antagonists in the rat formalin test. Neuropharmacology. 2006;51:623–630
  44. Scotland PE, Coderre TJ. Enhanced 3,5-dihydroxyphenylglycine-induced sustained nociceptive behaviors in rats with neuropathy or chronic inflammation. Behav Brain Res. 2007;184:150–156
  45. Simmons RMA, Webster AA, Kalra AB, Iyengar S. Group II mGluR receptor agonists are effective in persistent and neuropathic pain models in rats. Pharmacol Biochem Behav. 2002;73:419–427
  46. Soliman AC, Yu JS, Coderre TJ. mGlu and NMDA receptor contributions to capsaicin-induced thermal and mechanical hypersensitivity. Neuropharmacology. 2005;48:325–332
  47. Stanfa LC, Dickenson AH. Inflammation alters the effects of mGlu receptor agonists on spinal nociceptive neurones. Eur J Pharmaco. 1998;347:165–172
  48. Tominaga M, Tominaga T. Structure and function of TRPV1. Pflugers Arch. 2005;451:143–150
  49. Valerio A, Rizzonelli P, Paterlin M, Moretto G, Knopfel T, Kuhn R, et al. mGluR5 metabotropic glutamate receptor distribution in rat and human spinal cord: A developmental study. Neuroscience Research. 1997;28:49–57
  50. Varney MA, Gereau RW. Metabotropic glutamate receptor involvement in models of acute and persistent pain: Prospects for the development of novel analgesics. Current Drug Targets. 2002;1:215–225
  51. Walker K, Bowes M, Panesar M, Davis A, Gentry C, Kesingland A, et al. Metabotropic glutamate receptor subtype 5 (mGlu5) and nociceptive function. I. Selective blockade of mGlu5 receptors in models of acute, persistent and chronic pain. Neuropharmacology. 2001;40:1–9
  52. Walker K, Reeve A, Bowes M, Winter J, Wotherspoon G, Davis A, et al. mGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurones mediate inflammatory hyperalgesia. Neuropharmacology. 2001;40:10–19
  53. Yang D, Gereau RW. Peripheral group II metabotropic glutamate receptors (mGluR2/3) regulate prostaglandin E2-mediated sensitization of capsaicin responses and thermal nociception. J Neurosci. 2002;22:6388–6393
  54. Yang D, Gereau RW. Peripheral group II metabotropic glutamate receptors mediate endogenous anti-allodynia in inflammation. Pain. 2003;106:411–417
  55. Yashpal K, Fisher K, Chabot JG, Coderre TJ. Differential effects of NMDA and group I mGluR antagonists on both nociception and spinal cord protein kinase C translocation in the formalin test and a model of neuropathic pain in rats. Pain. 2001;94:17–29
  56. You HJ, Chen J, Morch CD, Arendt-Nielsen L. Differential effect of peripheral glutamate (NMDA, non-NMDA) receptor antagonists on bee venom-induced spontaneous nociception and sensitization. Brain Res Bull. 2002;58:561–567
  57. Young MR, Fleetwood-Walker SM, Dickinson T, Blackburn-Munro G, Sparrow H, Birch PJ, et al. 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. 1997;777:161–169
  58. Zhang L, Lu Y, Chen Y, Westlund KN. Group I metabotropic glutamate receptor antagonists block secondary thermal hyperalgesia in rats with knee joint inflammation. J Pharmacol Exp Ther. 2002;300:149–156
  59. Zhang T, Zhang J, Shi J, Feng Y, Sun ZS, Li H. Antinociceptive synergistic effect of spinal mGluR2/3 antagonist and glial cells inhibitor on peripheral inflammation-induced mechanical hypersensitivity. Brain Res Bull. 2009;79:219–223
  60. Zhou S, Komak S, Du J, Carlton SM. Metabotropic glutamate 1alpha receptors on peripheral primary afferent fibers: Their role in nociception. Brain Res. 2001;913:18–26
  61. Zhu CZ, Baker S, Ei-Kouhen O, Lehto SG, Hollingsworth PR, Gauvin DM, et al. Analgesic activity of metabotropic glutamate receptor 1 antagonists on spontaneous post-operative pain in rats. Eur J Pharmacol. 2008;580:314–321
  62. Zhu CZ, Hsieh G, Ei-Kouhen O, Wilson SG, Mikusa JP, Hollingsworth PR, et al. Role of central and peripheral mGluR5 receptors in post-operative pain in rats. Pain. 2005;114:195–202
  63. Zhu CZ, Wilson SG, Mikusa JP, Wismer CT, Gauvin DM, Lynch JJ, et al. Assessing the role of metabotropic glutamate receptor 5 in multiple nociceptive modalities. Eur J Pharmacol. 2004;506:107–118
  64. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16:109–110

 Supported by grants from the National Natural Science Foundation of China (30471667) and Postdoctoral Science Foundation of P. R. China (2005037760; both to H.S.C.).

PII: S1526-5900(09)00664-6

doi: 10.1016/j.jpain.2009.07.013

The Journal of Pain
Volume 11, Issue 4 , Pages 321-329 , April 2010