Neurotensin inhibits background K + channels and facilitates glutamatergic transmission in rat spinal cord dorsal horn

European Journal of Neuroscience

Volumn 34, Issue 8, 2011, Pages 1230-1240

  Kadiri, Nabila ^a   Rodeau, Jean Luc ^a   Schlichter, Rémy ^a   Hugel, Sylvain ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Excitatory synaptic transmission; K2P channels; Neuropeptide; Spinal cord dorsal horn

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [5 (2,6 DIMETHOXYPHENYL) 1 [4 [N (3 DIMETHYLAMINOPROPYL) N METHYLCARBAMOYL] 2 ISOPROPYLPHENYL] 1H PYRAZOL 3 YLCARBONYLAMINO]ADAMANTANE 2 CARBOXYLIC ACID; BARIUM ION; CALCIUM ACTIVATED POTASSIUM CHANNEL; CHELERYTHRINE; GLUTAMIC ACID; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; LEVOCABASTINE; MECLINERTANT; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUROTENSIN; NEUROTENSIN RECEPTOR; PERTUSSIS TOXIN; POTASSIUM CHANNEL; PROTEIN KINASE C; ZINC ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME RELEASE; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; INHIBITION KINETICS; NERVE CELL CULTURE; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROTRANSMISSION; NEWBORN; NONHUMAN; POTASSIUM CONDUCTANCE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; SIGNAL TRANSDUCTION; SOMATOSENSORY SYSTEM; SPINAL CORD DORSAL HORN;

ANIMALS; BENZOPHENANTHRIDINES; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; NEUROTENSIN; OLIGOPEPTIDES; PATCH-CLAMP TECHNIQUES; PERTUSSIS TOXIN; PIPERIDINES; POSTERIOR HORN CELLS; POTASSIUM CHANNELS; PYRAZOLES; QUINOLINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROTENSIN; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 80054707792     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07846.x     Document Type: Article

References (55)

1. Audinat, E., Hermel, J.M. & Crepel, F. (1989) Neurotensin-induced excitation of neurons of the rat's frontal cortex studied intracellularly in vitro. Exp. Brain Res., 78, 358-368.
2. Breton, J.D., Veinante, P., Uhl-Bronner, S., Vergnano, A.M., Freund-Mercier, M.J., Schlichter, R. & Poisbeau, P. (2008) Oxytocin-induced antinociception in the spinal cord is mediated by a subpopulation of glutamatergic neurons in lamina I-II which amplify GABAergic inhibition. Mol. Pain., 4, 19.
3. Carraway, R. & Leeman, S.E. (1973) The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J. Biol. Chem., 248, 6854-6861.
4. Chen, L., Yung, K.K. & Yung, W.H. (2004) Neurotensin depolarizes globus pallidus neurons in rats via neurotensin type-1 receptor. Neuroscience, 125, 853-859.
5. Clarke, C.E., Veale, E.L., Wyse, K., Vandenberg, J.I. & Mathie, A. (2008) The M1P1 loop of TASK3 K2P channels apposes the selectivity filter and influences channel function. J. Biol. Chem., 283, 16985-16992.
6. + channels. Mol. Pharmacol., 69, 1024-1032.
7. Difiglia, M., Aronin, N. & Leeman, S.E. (1984) Ultrastructural localization of immunoreactive neurotensin in the monkey superficial dorsal horn. J. Comp. Neurol., 225, 1-12.
8. Dobner, P.R. (2006) Neurotensin and pain modulation. Peptides, 27, 2405-2414.
9. Elde, R., Schalling, M., Ceccatelli, S., Nakanishi, S. & Hokfelt, T. (1990) Localization of neuropeptide receptor mRNA in rat brain: initial observations using probes for neurotensin and substance P receptors. Neurosci. Lett., 120, 134-138.
10. + currents: two-pore domain potassium channels. Physiol. Rev., 90, 559-605.
11. Farkas, R.H., Nakajima, S. & Nakajima, Y. (1994) Neurotensin excites basal forebrain cholinergic neurons: ionic and signal-transduction mechanisms. Proc. Natl. Acad. Sci. USA, 91, 2853-2857.
12. Fields, H. (2004) State-dependent opioid control of pain. Nat. Rev. Neurosci., 5, 565-575.
13. Goldstein, S.A., Bayliss, D.A., Kim, D., Lesage, F., Plant, L.D. & Rajan, S. (2005) International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol. Rev., 57, 527-540.
14. Hibino, H., Inanobe, A., Furutani, K., Murakami, S., Findlay, I. & Kurachi, Y. (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev., 90, 291-366.
15. Hu, H.J. & Gereau, R.W. 4th (2003) ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J. Neurophysiol., 90, 1680-1688.
16. + currents. J. Neurophysiol., 90, 1671-1679.
17. Hu, H.J., Alter, B.J., Carrasquillo, Y., Qiu, C.S. & Gereau, R.W. 4th (2007) Metabotropic glutamate receptor 5 modulates nociceptive plasticity via extracellular signal-regulated kinase-Kv4.2 signaling in spinal cord dorsal horn neurons. J. Neurosci., 27, 13181-13191.
18. Hugel, S. & Schlichter, R. (2000) Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J. Neurosci., 20, 2121-2130.
19. Hunt, S.P., Kelly, J.S., Emson, P.C., Kimmel, J.R., Miller, R.J. & Wu, J.Y. (1981) An immunohistochemical study of neuronal populations containing neuropeptides or gamma-aminobutyrate within the superficial layers of the rat dorsal horn. Neuroscience, 6, 1883-1898.
20. Inquimbert, P., Rodeau, J.L. & Schlichter, R. (2007) Differential contribution of GABAergic and glycinergic components to inhibitory synaptic transmission in lamina II and laminae III-IV of the young rat spinal cord. Eur. J. Neurosci., 26, 2940-2949.
21. Jiang, Z.G., Pessia, M. & North, R.A. (1994) Neurotensin excitation of rat ventral tegmental neurones. J. Physiol., 474, 119-129.
22. Jo, Y.H., Stoeckel, M.E., Freund-Mercier, M.J. & Schlichter, R. (1998a) Oxytocin modulates glutamatergic synaptic transmission between cultured neonatal spinal cord dorsal horn neurons. J. Neurosci., 18, 2377-2386.
23. Jo, Y.H., Stoeckel, M.E. & Schlichter, R. (1998b) Electrophysiological properties of cultured neonatal rat dorsal horn neurons containing GABA and met-enkephalin-like immunoreactivity. J. Neurophysiol., 79, 1583-1586.
24. Jolas, T. & Aghajanian, G.K. (1996) Neurotensin excitation of serotonergic neurons in the dorsal raphe nucleus of the rat in vitro. Eur. J. Neurosci., 8, 153-161.
25. Kindler, C.H., Yost, C.S. & Gray, A.T. (1999) Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology, 90, 1092-1102.
26. Kirkpatrick, K. & Bourque, C.W. (1995) Effects of neurotensin on rat supraoptic nucleus neurones in vitro. J. Physiol., 482 (Pt 2) 373-381.
27. Kitabgi, P. (2006) Functional domains of the subtype 1 neurotensin receptor (NTS1). Peptides, 27, 2461-2468.
28. Le Bars, D. (2002) The whole body receptive field of dorsal horn multireceptive neurones. Brain Res. Brain Res. Rev., 40, 29-44.
29. Legault, M., Congar, P., Michel, F.J. & Trudeau, L.E. (2002) Presynaptic action of neurotensin on cultured ventral tegmental area dopaminergic neurones. Neuroscience, 111, 177-187.
30. Lepee-Lorgeoux, I., Betancur, C., Rostene, W. & Pelaprat, D. (1999) Differential ontogenetic patterns of levocabastine-sensitive neurotensin NT2 receptors and of NT1 receptors in the rat brain revealed by in situ hybridization. Brain Res. Dev. Brain Res., 113, 115-131.
31. Lesage, F. (2003) Pharmacology of neuronal background potassium channels. Neuropharmacology, 44, 1-7.
32. Mazella, J. (2001) Sortilin/neurotensin receptor-3: a new tool to investigate neurotensin signaling and cellular trafficking? Cell. Signal., 13, 1-6.
33. Mazella, J. & Vincent, J.P. (2006) Functional roles of the NTS2 and NTS3 receptors. Peptides, 27, 2469-2475.
34. Mazella, J., Botto, J.M., Guillemare, E., Coppola, T., Sarret, P. & Vincent, J.P. (1996) Structure, functional expression, and cerebral localization of the levocabastine-sensitive neurotensin/neuromedin N receptor from mouse brain. J. Neurosci., 16, 5613-5620.
35. Miletic, V. & Randic, M. (1979) Neurotensin excites cat spinal neurones located in laminae I-III. Brain Res., 169, 600-604.
36. Mitchell, V.A., Kawahara, H. & Vaughan, C.W. (2009) Neurotensin inhibition of GABAergic transmission via mGluR-induced endocannabinoid signalling in rat periaqueductal grey. J. Physiol., 587, 2511-2520.
37. Ninkovic, M., Hunt, S.P. & Kelly, J.S. (1981) Effect of dorsal rhizotomy on the autoradiographic distribution of opiate and neurotensin receptors and neurotensin-like immunoreactivity within the rat spinal cord. Brain Res., 230, 111-119.
38. Ogawa, W.N., Baptista, V., Aguiar, J.F. & Varanda, W.A. (2005) Neurotensin modulates synaptic transmission in the nucleus of the solitary tract of the rat. Neuroscience, 130, 309-315.
39. Pottosin, I.I., Bonales-Alatorre, E., Valencia-Cruz, G., Mendoza-Magana, M.L. & Dobrovinskaya, O.R. (2008) TRESK-like potassium channels in leukemic T cells. Pflugers Arch., 456, 1037-1048.
40. Roussy, G., Dansereau, M.A., Dore-Savard, L., Belleville, K., Beaudet, N., Richelson, E. & Sarret, P. (2008) Spinal NTS1 receptors regulate nociceptive signaling in a rat formalin tonic pain model. J. Neurochem., 105, 1100-1114.
41. + channel, TRESK, is localized in the spinal cord. J. Biol. Chem., 278, 27406-27412.
42. Sarret, P., Beaudet, A., Vincent, J.P. & Mazella, J. (1998) Regional and cellular distribution of low affinity neurotensin receptor mRNA in adult and developing mouse brain. J. Comp. Neurol., 394, 344-356.
43. Sarret, P., Esdaile, M.J., Perron, A., Martinez, J., Stroh, T. & Beaudet, A. (2005) Potent spinal analgesia elicited through stimulation of NTS2 neurotensin receptors. J. Neurosci., 25, 8188-8196.
44. Stanzione, P. & Zieglgansberger, W. (1983) Action of neurotensin on spinal cord neurons in the rat. Brain Res., 268, 111-118.
45. Takeda, A., Minami, A., Seki, Y. & Oku, N. (2004) Differential effects of zinc on glutamatergic and GABAergic neurotransmitter systems in the hippocampus. J. Neurosci. Res., 75, 225-229.
46. Talley, E.M., Solorzano, G., Lei, Q., Kim, D. & Bayliss, D.A. (2001) Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. J. Neurosci., 21, 7491-7505.
47. Todd, A.J., Spike, R.C., Price, R.F. & Neilson, M. (1994) Immunocytochemical evidence that neurotensin is present in glutamatergic neurons in the superficial dorsal horn of the rat. J. Neurosci., 14, 774-784.
48. Uhl, G.R., Bennett, J.P. Jr & Snyder, S.H. (1977a) Neurotensin, a central nervous system peptide: apparent receptor binding in brain membranes. Brain Res., 130, 299-313.
49. Uhl, G.R., Kuhar, M.J. & Snyder, S.H. (1977b) Neurotensin: immunohistochemical localization in rat central nervous system. Proc. Natl. Acad. Sci. USA, 74, 4059-4063.
50. Urban, M.O. & Gebhart, G.F. (1997) Characterization of biphasic modulation of spinal nociceptive transmission by neurotensin in the rat rostral ventromedial medulla. J. Neurophysiol., 78, 1550-1562.
51. Vega-Saenz de Miera, E., Lau, D.H., Zhadina, M., Pountney, D., Coetzee, W.A. & Rudy, B. (2001) KT3.2 and KT3.3, two novel human two-pore K(+) channels closely related to TASK-1. J. Neurophysiol., 86, 130-142.
52. Vergnano, A.M., Schlichter, R. & Poisbeau, P. (2007) PKC activation sets an upper limit to the functional plasticity of GABAergic transmission induced by endogenous neurosteroids. Eur. J. Neurosci., 26, 1173-1182.
53. Vincent, J.P., Mazella, J. & Kitabgi, P. (1999) Neurotensin and neurotensin receptors. Trends Pharmacol. Sci., 20, 302-309.
54. Yoo, S., Liu, J., Sabbadini, M., Au, P., Xie, G.X. & Yost, C.S. (2009) Regional expression of the anesthetic-activated potassium channel TRESK in the rat nervous system. Neurosci. Lett., 465, 79-84.
55. Zhang, X., Bao, L., Xu, Z.Q., Diez, M., Frey, P. & Hokfelt, T. (1996) Peripheral axotomy induces increased expression of neurotensin in large neurons in rat lumbar dorsal root ganglia. Neurosci. Res., 25, 359-369.