The glycinergic control of spinal pain processing

Cellular and Molecular Life Sciences

Volumn 62, Issue 18, 2005, Pages 2027-2035

  Zeilhofer, H U ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Dorsal horn; Glycine; Pain; Prostaglandin; Protein kinase A; Spinal cord; Synapse; Synaptic inhibition

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCINE; GLYCINE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN E2;

GABAERGIC TRANSMISSION; HUMAN; HYPERALGESIA; INFLAMMATION; NERVE CELL PLASTICITY; NEUROPATHIC PAIN; NEUROTRANSMISSION; NOCICEPTION; PHOSPHORYLATION; REVIEW; SPINAL CORD; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION;

DINOPROSTONE; HUMANS; HYPERALGESIA; INFLAMMATION; PAIN; POSTERIOR HORN CELLS; RECEPTORS, GLYCINE; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 24744450794     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-005-5107-2     Document Type: Review

References (71)

1. Sherrington C. S. (1908) The integrative actions of the nervous system, Archibald Constable
2. Taal W. and Holstege J. C. (1994) GABA and glycine frequently colocalize in terminals on cat spinal motoneurons. Neuroreport 5: 2225-2228
3. Popratiloff A., Valtschanoff J. G., Rustioni A. and Weinberg R. J. (1996) Colocalization of GABA and glycine in the rat dorsal column nuclei. Brain Res. 706: 308-312
4. Todd A. J., Watt C., Spike R. C. and Sieghart W. (1996) Colocalization of GABA, glycine and their receptors at synapses in the rat spinal cord. J. Neurosci. 16: 974-982
5. Jonas P., Bischofberger J. and Sandkühler J. (1998) Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424
6. Keller A. F., Coull J. A., Chery N., Poisbeau P. and de Koninck Y. (2001) Region-specific developmental specialization of GABA-glycine cosynapses in laminas I-II of the rat spinal dorsal horn. J. Neurosci. 21: 7871-7880
7. A receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J. Neurosci. 19: 7342-7355
8. Lynch J. W. (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol. Rev. 84: 1051-1095
9. Legendre P. (2001) The glycinergic inhibitory synapse. Cell. Mol. Life Sci. 58: 760-793
10. Pfeiffer F., Simler R., Grenningloh G. and Betz H. (1984) Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc. Natl. Acad. Sci. USA. 81: 7224-7227
11. Zeilhofer H. U., Studler B., Arabadzisz D., Schweizer C., Ahmadi S., Layh B. et al. (2005) Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J. Comp. Neurol. 482: 123-141
12. Mackie M., Hughes D. L., Maxwell D. J., Tillakaratne N. J. and Todd A. J. (2003) Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 119: 461-472
13. A-receptor subtypes in the spinal cord: an immunohistochemical study. J. Neurosci. 16: 283-297
14. Powell J. J. and Todd A. J. (1992) Light and electron microscope study of GABA-immunoreactive neurones in lamina III of rat spinal cord. J. Comp. Neurol. 315: 125-136
15. Narikawa K., Furue H., Kumamoto E. and Yoshimura M. (2000) In vivo patch-clamp analysis of IPSCs evoked in rat substantia gelatinosa neurons by cutaneous mechanical stimulation. J. Neurophysiol. 84: 2171-2174
16. A and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J. Neurophysiol. 72: 169-179
17. Sherman S. E., Luo L. and Dostrovsky J. O. (1997) Spinal strychnine alters response properties of nociceptive-specific neurons in rat medial thalamus. J. Neurophysiol. 78: 628-637
18. Sorkin L. S., Puig S. and Jones D. L. (1998) Spinal bicuculline produces hypersensitivity of dorsal horn neurons: effects of excitatory amino acid antagonists. Pain 77: 181-190
19. Loomis C. W., Khandwala H., Osmond G. and Hefferan M. P. (2001) Coadministration of intrathecal strychnine and bicuculline effects synergistic allodynia in the rat: an isobolographic analysis. J. Pharmacol. Exp. Ther. 296: 756-761
20. A- and glycine-receptor mediated tonic inhibition in the dorsal horn of the rat lumbar spinal cord: effects of picrotoxin and strychnine on expression of Fos-like immunoreactivity. Pain 112: 156-163
21. O'Banion M. K. (1999) Cyclooxygenase-2: molecular biology, pharmacology and neurobiology. Crit. Rev. Neurobiol. 13: 45-82
22. Narumiya, S., Sugimoto Y. and Ushikubi F. (1999) Prostanoid receptors: structures, properties and functions. Physiol. Rev. 79: 1193-1226
23. Moriyama T., Higashi T., Togashi K., Iida T., Segi E., Sugimoto Y. et al. (2005) Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol. Pain 1: 3 doi:10.1186/1744-8069-1-3
24. Caterina M. J., Schumacher M. A., Tominaga M., Rosen T. A., Levine J. D. and Julius D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824
25. Tominaga M., Caterina M. J., Malmberg A. B., Rosen T. A., Gilbert H., Skinner K. et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543
26. 2-mediated sensitization of the capsaicin response in rat sensory neurons. J. Neurophysiol. 78: 3154-3164
27. England S., Bevan S., and Docherty R. J. (1996) PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J. Physiol 495: 429-440
28. Gold M. S., Reichling D. B., Shuster M. J., and Levine J. D. (1996) Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc. Natl. Acad. Sci. USA 93: 1108-1112
29. Akopian A. N., Souslova V., England S., Okuse K., Ogata N., Ure J. et al. (1999) The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 2: 541-548
30. Beiche F., Scheuerer S., Brune K., Geisslinger G. and Goppelt-Struebe M. (1996) Up-regulation of cyclooxygenase-2 mRNA in the rat spinal cord following peripheral inflammation. FEBS Lett. 390: 165-169
31. Samad T. A., Moore K. A., Sapirstein A., Billet S., Allchorne A., Poole S. et al. (2001) Interleukin-1 beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410: 471-475
32. Vasquez E., Bär K. J., Ebersberger A., Klein B., Vanegas H. and Schaible H. G. (2001) Spinal prostaglandins are involved in the development but not the maintenance of inflammation-induced spinal hyperexcitability. J. Neurosci. 21: 9001-9008
33. Minami T., Okuda-Ashitaka E., Hori Y., Sakuma S., Sugimoto T., Sakimura K. et al. (1999) Involvement of primary afferent C-fibres in touch-evoked pain (allodynia) induced by prostaglandin E2. Eur. J. Neurosci. 11: 1849-1856
34. Baba H., Kohno T., Moore K. A. and Woolf C. J. (2001) Direct activation of rat spinal dorsal horn neurons by prostaglandin E2. J. Neurosci. 21: 1750-1756
35. 2 selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat. Neurosci. 5: 34-40
36. Malmberg A. B., Brandon E. P., Idzerda R. L., Liu H., McKnight G. S. and Basbaum A. I. (1997) Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J. Neurosci. 17: 7462-7470
37. Harvey R. J., Depner U. B., Wässle H., Ahmadi S., Heindl C., Reinold H. et al. (2004) GlyR α3: an essential target for spinal inflammatory pain sensitization. Science 304: 884-887
38. Findlay G. S., Phelan R., Roberts M. T., Homanics G. E., Bergeson S. E., Lopreato G. F. et al. (2003) Glycine receptor knock-in mice and hyperekplexia-like phenotypes: comparisons with the null mutant. J. Neurosci. 23: 8051-8059
39. Meller S. T. and Gebhart G. F. (1997) Intraplantar zymosan as a reliable, quantifiable model of thermal and mechanical hyperalgesia in the rat. Eur. J. Pain 1: 43-52
40. Reinold H., Ahmadi S., Depner U. B., Layh B., Heindl C., Hamza M. et al. (2005) Spinal inflammatory hyperalgesia is mediated by spinal prostaglandin E receptors of the EP2 subtype. J. Clin. Invest. 115: 673-679
41. 2. J. Neurosci. 21: 1750-1756
42. Tambeli C. H., Quang P., Levine J. D. and Gear R. W. (2003) Contribution of spinal inhibitory receptors in heterosegmental antinociception induced by noxious stimulation.Eur J Neurosci. 18: 2999-3006
43. A antagonists reduce the inhibition of primate spinothalamic tract neurons produced by stimulation in periaqueductal gray. Brain Res. 654: 286-302
44. Antal M., Petko M., Polgar E., Heizmann C. W. and Storm-Mathisen J. (1996) Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience 73: 509-518
45. Hefferan M. P., Carter P., Haley M. and Loomis C. W. (2003) Spinal nerve injury activates prostaglandin synthesis in the spinal cord that contributes to early maintenance of tactile allodynia. Pain 101: 139-147
46. Zhu X. and Eisenach J. C. (2003) Cyclooxygenase-1 in the spinal cord is altered after peripheral nerve injury. Anesthesiology 99: 1175-1179
47. Broom D. C., Samad T. A., Kohno T., Tegeder I., Geisslinger G. and Woolf C. J. (2004) Cyclooxygenase 2 expression in the spared nerve injury model of neuropathic pain. Neuroscience 124: 891-900
48. Okuda-Ashitaka E., Minami T., Tachibana S., Yoshihara Y., Nishiuchi Y., Kimura T. et al. (1998) Nocistatin, a peptide that blocks nociceptin action in pain transmission. Nature 392: 286-289
49. Zeilhofer H. U., Muth-Selbach U., Guhring H., Erb K. and Ahmadi S. (2000) Selective suppression of inhibitory synaptic transmission by nocistatin in the rat spinal cord dorsal horn. J. Neurosci. 20: 4922-4999
50. Muth-Selbach U., Dybek E., Kollosche K., Stegmann J. U., Holthusen H., Lipfert P. et al. (2004) The spinal antinociceptive effect of nocistatin in neuropathic rats is blocked by D-serine. Anesthesiology 101: 753-758
51. Lee T. L., Fung F. M., Chen F. G., Chou N., Okuda-Ashitaka E., Ito S. et al. (1999) Identification of human, rat and mouse nocistatin in brain and human nocistatin in brain and human cerebrospinal fluid. Neuroreport 10: 1537-1541
52. Depner U. B., Reinscheid R. K., Takeshima H., Brune K. and Zeilhofer H. U. (2003) Normal sensitivity of acute pain, but increased inflammatory hyperalgesia in mice lacking the nociceptin precursor polypeptide or the nociceptin receptor. Eur. J. Neurosci. 17: 2381-2387
53. Yang K., Fujita T. and Kumamoto E. (2004) Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J. Neurophysiol. 92: 2867-2877
54. Hugel S. and Schlichter R. (2003) Convergent control of synaptic GABA release from rat dorsal horn neurones by adenosine and GABA autoreceptors. J. Physiol. 551: 479-489
55. Coull J. A., Boudreau D., Bachand K., Prescott S. A., Nault F., Sik A. et al. (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424: 938-942
56. Moore K. A., Kohno T., Karchewski E. A., Scholz J., Baba H. and Woolf C. J. (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
57. Polgar E., Hughes D. I., Riddell J. S., Maxwell D. J., Puskar Z. and Todd A. J. (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
58. Polgar E., Gray S., Riddell J. S. and Todd A. J. (2004) Lack of evidence for significant neuronal loss in laminae I-III of the spinal dorsal horn of the rat in the chronic constriction injury model. Pain 111: 144-150
59. Jang I. S., Rhee J. S., Kubota H. and Akaike N. (2001) Developmental changes in P2X purinoceptors on glycinergic presynaptic nerve terminals projecting to rat substantia gelatinosa neurones. J. Physiol. 536: 505-519
60. Rhee J. S., Wang Z. M., Nabekura J., Inoue K. and Akaike N. (2000) ATP facilitates spontaneous glycinergic IPSC frequency at dissociated rat dorsal horn interneuron synapses. J. Physiol. 524: 471-483
61. Baba H., Shimoji K. and Yoshimura M. (2000) Norepinephrine facilitates inhibitory transmission in substantia gelatinosa of adult rat spinal cord (part 1): effects on axon terminals of GABAergic and glycinergic neurons. Anesthesiology 92: 473-484
62. Baba H., Goldstein P. A., Okamoto M., Kohno T., Ataka T., Yoshimura M. et al. (2000) Norepinephrine facilitates inhibitory transmission in substantia gelatinosa of adult rat spinal cord (part 2): effects on somatodendritic sites of GABAergic neurons. Anesthesiology 92: 485-492
63. Nabekura J., Xu T. L., Rhee J. S., Li J. S. and Akaike N. (1999) Alpha2-adrenoceptor-mediated enhancement of glycine response in rat sacral dorsal commissural neurons. Neuroscience 9: 29-41
64. Breitinger H. G. and Becker C. M. (1998) The inhibitory glycine receptor: prospects for a therapeutic orphan? Curr. Pharm. Des. 4: 315-334
65. Laube B., Maksay G., Schemm R. and Betz H. (2002) Modulation of glycine receptor function: a novel approach for therapeutic intervention at inhibitory synapses? Trends Pharmacol. Sci. 23: 519-527
66. A agonists and partial agonists: THIP (Gaboxadol) as a non-opioid analgesic and a novel type of hypnotic. Biochem. Pharmacol. 68: 1573-1580
67. Jasmin L., Wu M. V. and Ohara P. T. (2004) GABA puts a stop to pain. Curr. Drug. Targets CNS Neurol. Disord. 3: 487-505
68. A receptors at supraspinal level. Eur. J. Pharmacol. 370: 9-15
69. A receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu. Rev. Pharmacol. Toxicol. 44: 475-498
70. Löw K., Crestani F., Keist R., Benke D., Brünig I., Benson J. A. et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290: 131-134
71. A receptor alphal subtype. Nat. Neurosci. 3: 587-592