Modulation of inhibitory neurotransmission by the vanilloid receptor type 1 (TRPV1) in organotypically cultured mouse substantia gelatinosa neurons

Pain

Volumn 150, Issue 1, 2010, Pages 128-140

  Ferrini, Francesco ^a   Salio, Chiara ^a   Lossi, Laura ^a,b   Gambino, Graziana ^a   Merighi, Adalberto ^a,b  

^a Department of Veterinary Morphophysiology ^*  (Italy)

^b Istituto Nazionale di Neuroscienze   (Italy)

Author keywords

Capsaicin; Endovanilloids; Inhibitory post synaptic currents; Organotypic cultures; Substantia gelatinosa; TRPV1 receptor

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; CAPSAICIN; IODORESINIFERATOXIN; MESSENGER RNA; N ARACHIDONOYLDOPAMINE; N PALMITOYLDOPAMINE; N STEAROYLDOPAMINE; TETRODOTOXIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR AGONIST; VANILLOID RECEPTOR ANTAGONIST;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL CULTURE; CONTROLLED STUDY; EXPERIMENTAL MOUSE; FEMALE; FREQUENCY MODULATION; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PERINATAL PERIOD; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SUBSTANTIA GELATINOSA; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CAPSAICIN; CELLS, CULTURED; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STATISTICS, NONPARAMETRIC; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION; TRPV CATION CHANNELS;

EID: 77953025205     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2010.04.016     Document Type: Article

References (51)

1. Baccei M.L., Bardoni R., and Fitzgerald M. Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. J Physiol 549 (2003) 231-242
2. Ballerini L., and Galante M. Network bursting by organotypic spinal slice cultures in the presence of bicuculline and/or strychnine is developmentally regulated. Eur J Neurosci 10 (1998) 2871-2879
3. Bhave G., Zhu W., Wang H., Brasier D.J., and Oxford G.S. Gereau RW cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35 (2002) 721-731
4. Bolcskei K., Helyes Z., Szabo A., Sandor K., Elekes K., Nemeth J., Almasi R., Pinter E., Petho G., and Szolcsanyi J. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 117 (2005) 368-376
5. Bracci E., Ballerini L., and Nistri A. Localization of rhythmogenic networks responsible for spontaneous bursts induced by strychnine and bicuculline in the rat isolated spinal cord. J Neurosci 16 (1996) 7063-7076
6. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
7. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
8. Cavanaugh D.J., Lee H., Lo L., Shields S.D., Zylka M.J., Basbaum A.I., and Anderson D.J. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci USA 106 (2009) 9075-9080
9. Christoph T., Gillen C., Mika J., Grunweller A., Schafer M.K., Schiene K., Frank R., Jostock R., Bahrenberg G., Weihe E., Erdmann V.A., and Kurreck J. Antinociceptive effect of antisense oligonucleotides against the vanilloid receptor VR1/TRPV1. Neurochem Int 50 (2007) 281-290
10. Chu C.J., Huang S.M., De Petrocellis L., Bisogno T., Ewing S.A., Miller J.D., Zipkin R.E., Daddario N., Appendino G., Di Marzo V., and Walker J.M. N-Oleoyldopamine, a novel endogenous capsaicin-like lipid that produces hyperalgesia. J Biol Chem 278 (2003) 13633-13639
11. Conway S.J. TRPing the switch on pain: an introduction to the chemistry and biology of capsaicin and TRPV1. Chem Soc Rev 37 (2008) 1530-1545
12. Cruz C.D., Charrua A., Vieira E., Valente J., Avelino A., and Cruz F. Intrathecal delivery of resiniferatoxin (RTX) reduces detrusor overactivity and spinal expression of TRPV1 in spinal cord injured animals. Exp Neurol 214 (2008) 301-308
13. Cui J.G., Zhang X., Zhao Y.H., Chen C., and Bazan N. Allodynia and hyperalgesia suppression by a novel analgesic in experimental neuropathic pain. Biochem Biophys Res Commun 350 (2006) 358-363
14. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A., and Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
15. De Petrocellis L., Chu C.J., Moriello A.S., Kellner J.C., Walker J.M., and Di Marzo V. Actions of two naturally occurring saturated N-acyldopamines on transient receptor potential vanilloid 1 (TRPV1) channels. Br J Pharmacol 143 (2004) 251-256
16. De Simoni A., Griesinger C.B., and Edwards F.A. Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 550 (2003) 135-147
17. Delfs J., Friend J., Ishimoto S., and Saroff D. Ventral and dorsal horn acetylcholinesterase neurons are maintained in organotypic cultures of postnatal rat spinal cord explants. Brain Res 488 (1989) 31-42
18. Doly S., Fischer J., and Conrath M. The vanilloid receptor-1 (TRPV1) is expressed in some rat dorsal horn NK1 cells. Brain Res 1004 (2004) 203-207
19. Ferrini F., Salio C., Vergnano A.M., and Merighi A. Vanilloid receptor-1 (TRPV1)-dependent activation of inhibitory neurotransmission in spinal substantia gelatinosa neurons of mouse. Pain 129 (2007) 195-209
20. Grudt T.J., and Perl E.R. Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540 (2002) 189-207
21. Guo A., Simone D.A., Stone L.S., Fairbanks C.A., Wang J., and Elde R. Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. Eur J Neurosci 14 (2001) 293-304
22. Guo A., Vulchanova L., Wang J., Li X., and Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11 (1999) 946-958
23. Heinke B., Ruscheweyh R., Forsthuber L., Wunderbaldinger G., and Sandkuhler J. Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice. J Physiol 560 (2004) 249-266
24. Hilton K.J., Bateson A.N., and King A.E. A model of organotypic rat spinal slice culture and biolistic transfection to elucidate factors that drive the preprotachykinin-A promoter. Brain Res Brain Res Rev 46 (2004) 191-203
25. Huang S.M., Bisogno T., Trevisani M., Al Hayani A., De Petrocellis L., Fezza F., Tognetto M., Petros T.J., Krey J.F., Chu C.J., Miller J.D., Davies S.N., Geppetti P., Walker J.M., and Di Marzo V. An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci USA 99 (2002) 8400-8405
26. Huang S.M., and Walker J.M. Enhancement of spontaneous and heat-evoked activity in spinal nociceptive neurons by the endovanilloid/endocannabinoid N-arachidonoyldopamine (NADA). J Neurophysiol 95 (2006) 1207-1212
27. Hulsebosch C.E., and Coggeshall R.E. Sprouting of dorsal root axons. Brain Res 224 (1981) 170-174
28. Hwang S.J., Burette A., and Valtschanoff J.G. VR1-positive primary afferents contact NK1-positive spinoparabrachial neurons. J Comp Neurol 460 (2003) 255-265
29. Keller A.F., Coull J.A., Chery N., Poisbeau P., and de Koninck Y. Region-specific developmental specialization of GABA-glycine cosynapses in laminas I-II of the rat spinal dorsal horn. J Neurosci 21 (2001) 7871-7880
30. Koplas P.A., Rosenberg R.L., and Oxford G.S. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17 (1997) 3525-3537
31. Labrakakis C., and MacDermott A.B. Neurokinin receptor 1-expressing spinal cord neurons in lamina I and III/IV of postnatal rats receive inputs from capsaicin sensitive fibers. Neurosci Lett 352 (2003) 121-124
32. Lao L.J., Song B., and Marvizon J.C. Neurokinin release produced by capsaicin acting on the central terminals and axons of primary afferents: relationship with N-methyl-d-aspartate and GABA(B) receptors. Neuroscience 121 (2003) 667-680
33. Lossi L., Alasia S., Salio C., and Merighi A. Cell death and proliferation in acute slices and organotypic cultures of mammalian CNS. Prog Neurobiol (2009). http://dx.doi.org/10.1016/j.pneurobio.2009.01.002
34. Lu V.B., Moran T.D., Balasubramanyan S., Alier K.A., Dryden W.F., Colmers W.F., and Smith P.A. Substantia Gelatinosa neurons in defined-medium organotypic slice culture are similar to those in acute slices from young adult rats. Pain 121 (2006) 261-275
35. Michael G.J., and Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 19 (1999) 1844-1854
36. Nakatsuka T., Chen M., Takeda D., King C., Ling J., Xing H., Ataka T., Vierck C., Yezierski R., and Gu J.G. Substance P-driven feed-forward inhibitory activity in the mammalian spinal cord. Mol Pain 20 (2005) 20
37. Nakatsuka T., Furue H., Yoshimura M., and Gu J.G. Activation of central terminal vanilloid receptor-1 receptors and alpha beta-methylene-ATP-sensitive P2X receptors reveals a converged synaptic activity onto the deep dorsal horn neurons of the spinal cord. J Neurosci 22 (2002) 1228-1237
38. Premkumar L.S., Qi Z.H., Van Buren J., and Raisinghani M. Enhancement of potency and efficacy of NADA by PKC-mediated phosphorylation of vanilloid receptor. J Neurophysiol 91 (2004) 1442-1449
39. Roberts L.A., and Connor M. TRPV1 antagonists as a potential treatment for hyperalgesia. Recent Pat CNS Drug Discov 1 (2006) 65-76
40. Ruscheweyh R., and Sandkuhler J. Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro. J Physiol 541 (2002) 231-244
41. Sagar D.R., Smith P.A., Millns P.J., Smart D., Kendall D.A., and Chapman V. TRPV1 and CB(1) receptor-mediated effects of the endovanilloid/endocannabinoid N-arachidonoyl-dopamine on primary afferent fibre and spinal cord neuronal responses in the rat. Eur J Neurosci 20 (2004) 175-184
42. Salio C., Fischer J., Franzoni M.F., and Conrath M. Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience 110 (2002) 755-764
43. Salio C., Fischer J., Franzoni M.F., Mackie K., Kaneko T., and Conrath M. CB1-cannabinoid and mu-opioid receptor co-localization on postsynaptic target in the rat dorsal horn. Neuroreport 12 (2001) 3689-3692
44. Starowicz K., Cristino L., and Di Marzo V. TRPV1 receptors in the central nervous system: potential for previously unforeseen therapeutic applications. Curr Pharm Des 14 (2008) 42-54
45. Sugimoto T., Funahashi M., Xiao C., Adachi A., and Ichikawa H. Exaggerated C-fiber activation prevents peripheral nerve injury-induced hyperinducibility of c-Fos in partially deafferented spinal dorsal horn. Neurosci Res 27 (1997) 161-167
46. Toth A., Kedei N., Wang Y., and Blumberg P.M. Arachidonyl dopamine as a ligand for the vanilloid receptor VR1 of the rat. Life Sci 73 (2003) 487-498
47. Urban L., and Dray A. Synaptic activation of dorsal horn neurons by selective C-fibre excitation with capsaicin in the mouse spinal cord in vitro. Neuroscience 47 (1992) 693-702
48. Valtschanoff J.G., Rustioni A., Guo A., and Hwang S.J. Vanilloid receptor VR1 is both presynaptic and postsynaptic in the superficial laminae of the rat dorsal horn. J Comp Neurol 436 (2001) 225-235
49. Van Der Stelt M., and Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 271 (2004) 1827-1834
50. Yang K., Kumamoto E., Furue H., and Yoshimura M. Capsaicin facilitates excitatory but not inhibitory synaptic transmission in substantia gelatinosa of the rat spinal cord. Neurosci Lett 255 (1998) 135-138
51. Zhou H.Y., Chen S.R., Chen H., and Pan H.L. The glutamatergic nature of TRPV1-expressing neurons in the spinal dorsal horn. J Neurochem 108 (2009) 305-318