Neurokinin 1 receptor activates transient receptor potential-like currents in noradrenergic A7 neurons in rats

Molecular and Cellular Neuroscience

Volumn 42, Issue 1, 2009, Pages 56-65

  Min, Ming Yuan ^a   Shih, Pei Yu ^a   Wu, Yu Wei ^a   Lu, Hsin Wei ^a   Lee, Meng Larn ^b   Yang, Hsiu Wen ^b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Noradrenergic; Pain; Substance P; Tachykinin; TRPC; Ventromedial medulla

Indexed keywords

GLYCEROL 2 ACETATE 1 OLEATE; NEUROKININ 1 RECEPTOR; NEUROKININ 1 RECEPTOR ANTAGONIST; PROTEIN KINASE C; SUBSTANCE P; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; IMMUNOHISTOCHEMISTRY; NEUROMODULATION; NONHUMAN; NORADRENERGIC NERVE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR POTENTIAL; REGULATORY MECHANISM; SLOW INWARD CURRENT;

ANIMALS; ANIMALS, NEWBORN; ANTINEOPLASTIC AGENTS; DOPAMINE BETA-HYDROXYLASE; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; ESTRENES; EXCITATORY AMINO ACID ANTAGONISTS; ISOINDOLES; LYSINE; MEMBRANE POTENTIALS; NEURONS; NEUROTRANSMITTER AGENTS; NOREPINEPHRINE; PATCH-CLAMP TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; PYRROLIDINONES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; SPINAL CORD; SUBSTANCE P; SURAMIN; TRPC CATION CHANNELS;

RATTUS;

EID: 67650986121     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.05.006     Document Type: Article

References (58)

1. Alter B.J., and Gereau R.W. Hotheaded: TRPV1 as mediator of hippocampal synaptic plasticity. Neuron 57 (2008) 629-631
2. Amaral M.D., and Pozzo-Miller L. TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J. Neurosci. 27 (2007) 5179-5189
3. Bajic D., Van Bockstaele E.J., and Proudfit H.K. Ultrastructure analysis of ventro-lateral periaqueductal gray projections to the A7 catecholamine cell group. Neuroscience 104 (2001) 181-197
4. Barbaro N.M., Hammond D.L., and Fields H.L. Effects of intrathecally administered methysergide and yohimbine on microstimulation-produced antinociception in the rat. Brain Res. 343 (1985) 223-229
5. Bengtson C.P., Tozzi A., Bernardi G., and Mercuri N.B. Transient receptor potential-like channel mediate metaotropic glutamate receptor EPSCs in rat dopamine neruones. J. Physiol. 555 (2004) 323-330
6. Berg A.P., Sen N., and Bayliss D.A. TrpC3/C7 and Slo2.1 are molecular targets for metabotropic glutamate receptor signaling in rat striatal cholinergic interneurons. J. Neurosci. 27 (2007) 8845-8856
7. Carlsson A., Falck B., Fuxe K., and Hillarp N.A. Cellular localization of monoamines in the spinal cord. Acta PhysiolScand. 60 (1964) 112-119
8. Chen L.-W., Wei L.C., Liu H.-L., and Rao Z.R. Noradrenergic neurons expressing substance P receptor (NK1) in the locus coeruleus complex: a double immunofluorescent study in the rat. Brain Res. 873 (2000) 155-159
9. Clapham D.E. TRP channels as cellular sensors. Nature 426 (2003) 517-524
10. Clark F.M., and Proudfit H.K. The projection of noradrenergic neurons in A7 catecholamine cell group to the spinal cord in rat demonstrated by antrograde tracing combined immunohistochemistry. Brain Res. 547 (1991) 279-288
11. Clark F.M., and Proudfit H.K. Projection of neurons in the ventromedial medulla to pontine catecholamine cell groups involved in the modulation of nociception. Brain Res. 540 (1991) 105-111
12. Dahlsötrm A., and Fuse K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta. Physiol. Scand. 62 Suppl. 232 (1964) 1-55
13. Drew G.M., Michell V.A., and Vauhan C.W. Postsynaptic action of Substance P on rat periaqueductal grey neurons in vitro. Neuropharmacol. 49 (2005) 587-595
14. Estacion M., Li S., Sinkins W.G., Gosling M., Bahra P., Poll C., Westwick J., and Schilling W.P. Activation of human TRPC6 channels by receptor stimulation. J. Biol. Chem. 279 (2004) 22047-22056
15. Gee C.E., Benquet P., and Gerber U. Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J. Physiol. 254 (2003) 655-664
16. Gibson H.E., Edwards J.G., Page R.S., Van Hook M.J., and Kauer J.A. TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57 (2008) 746-759
17. Hodge C.J., Apkarian A.V., and Stevens R.T. Inhibition of dorsal horn cell response by stimulation of the Kölliker-Fuse nucleus. J. Neurosurg. 65 (1986) 825-833
18. Hofmann T., Obukhov A.G., Schaefer M., Hartenc K.C., Gudermann T., and Schultz G. Direct stimulation of Human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397 (1999) 259-263
19. Holden J.E., and Pizzi J.A. The challenge of chronic pain. Adv. Drug Deliv. Rev. 55 (2003) 935-948
20. Holden J.E., and Proudfit H.K. Enkephalin neurons that project to the A7 catecholamine cell group are located in brainstem nuclei that modulate nociception: ventromedial medulla. Neuroscience 83 (1998) 929-947
21. Holden J.E., Schwartz E.J., and Proudfit H.K. Microinjection of morphine in the A7 catecholamine cell group produces opposing effects on nociception that are mediated by alpha1- and alpha2-adrenoceptors. Neuroscience 83 (1999) 979-990
22. Holden J.E., Van Poppel A.Y., and Thomas S. Antinociception from lateral hypothalamic stimulation may be mediated by NK1 receptors in the A7 catecholamine cell group in rat. Brain Res. 953 (2002) 195-204
23. Jones S.L. Descending noradrenergic influences on pain. Prog. Brain Res. 88 (1991) 381-394
24. Jung S., Muhle A., Schaefer M., Schultz G., and Plant T.D. Lanthanides potentiate TRPC5 currents by an action at extracellular sites close to the pore mouth. J. Biol. Chem. 278 (2003) 3562-3571
25. Kwiat G.C., and Basbaum A.I. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens. Mot. Res. 9 (1992) 157-173
26. Koyano K., Velimirovic B.M., Grigg J.J., Nakajima S., and Nakajima Y. Two signal transduction mechanisms of substance P-induced depolarization in locus coeruleus neurons. Eur. J. Neurosci. 5 (1993) 1189-1197
27. Ljungdahl A., Hökfelt T., Nilsson G., and Goldstein M. Distribution of Substance P-like immunoreactivity in the central nervous system in the rat. II. Light microscopic localization in relation to catecholamine-containing neurons. Neuroscience 3 (1978) 945-976
28. Marvizón J.C.G., Matinez V., Grady E.F., Bunnett N.W., and Mayer E.A. Neurokinin 1 receptor internalization in spinal cord slices induced by dorsal root stimulation is mediated by NMDA receptors. J. Neurosci. 17 (1997) 8129-8136
29. Meis S., Munsch T., Sosulina L., and Pape H.C. Postsynaptic mechanisms underlying responsiveness of amygdaloid neurons to cholecystokinin are mediated by a transient receptor potential-like current. Mol. Cell Neurosci. 35 (2007) 356-367
30. Min M.-Y., Hsu P.-C., and Yang H.-W. The physiological and morphological characteristics of interneurons caudal to the trigeminal motor nucleus in rats. Eur. J. Neurosci. 18 (2003) 2981-2998
31. Min M.-Y., Hsu P.-C., Lu H.-W., Lin C.-J., and Yang H.-W. Postnatal development of noradrenergic terminals in the rat trigeminal motor nucleus: a light and electron microscopic immunocytochemical analysis. Anat. Rec. 290 (2007) 96-107
32. Min M.-Y., Wu Y.-W., Shih P.-Y., Lu H.-W., Lin C.-C., Wu Y., Li M.-J., and Yang H.-W. Physiological and morphological properties of, and effect of substance P on, neurons in the A7 catecholamine cell group in rats. Neuroscience 153 (2008) 1020-1033
33. Moran M.M., Xu H., and Clapham D.E. TRP ion channels in the nervous system. Curr. Opin. Neurobiol. 14 (2004) 362-369
34. Nuseir K., and Proudfit H.K. Bidirectional modulation of nociception by GABA neurons in the dorsolateral pontine tegmentum that tonically inhibit spinally projecting noradrenergic A7 neurons. Neuroscience 96 4 (2000) 773-783
35. Oh E.J., Gover T.D., Cordoba-Rodriguez R., et al. Substance P evokes cation currents through TRP channels in HEK393 cells. J. Neurophysiol. 90 (2003) 2069-2073
36. Patterson R.L., van Rossum D.B., Nikolaidis N., and Weinreich D. Phospholipase C-gamma: diverse roles in receptor-mediated calcium signalling. Trends Biochem. Sci. 30 (2005) 688-697
37. Pertovaara A. Noradrenergic pain modulation. Prog. Neurobiol. 80 (2006) 53-83
38. Ramsey I.S., Delling M., and Clapham D.E. An introduction to TRP channels. Annu. Rev. Physiol. 68 (2006) 619-647
39. Roosterman D., Cottrell G.S., Schmidlin F., Steinhoff M., and Bunnett N.W. Recycling and resensitization of the Neurokinin 1 receptor. J. Biol. Chem. 279 (2004) 30670-30679
40. Sagen J., and Proudfit H.K. Hypoalgesia induced by blockade of noradrenergic projections to the raphe magnus: reversal by blockade of noradrenergic projections to the spinal cord. Brain Res. 223 (1981) 391-396
41. Sakakibara M., Inoue H., and Yoshioka T. Evidence for the involvement of inositol trisphosphate but not cyclic nucleotides in visual transduction in Hermissenda eye. J. Biol. Chem. 273 (1998) 20795-20801
42. Satoh M., Oku R., and Akaike A. Analgesia produced by microinjection of l-glutamate into the rostral ventromedial bulbar nuclei of rats and its inhibition by intrathecal adrenergic blocking agents. Brain Res. 261 (1983) 361-364
43. Schaefer M., Plant T.D., Obukhov A.G., Hofmann T., Gudermann T., and Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275 (2000) 17517-17526
44. Schaefer M., Plant T.D., Stresow N., Albrecht N., and Schultz G. Functional differences between TRPC4 splice variants. J. Biol. Chem. 277 (2002) 3752-3759
45. Sekaran S., Lall G.S., Ralphs K.L., Wolsenholme A.J., Lucas R.J., Foster R.G., and Hankins M.W. 2-aminoethoxydiphenylborane is an acute inhibitor of directly photosensitive retinal ganglion cell activity in vitro and in vivo. J. Neurosci. 27 (2007) 3981-3986
46. Shen K.Z., and North R.A. Substance P opens cation channels and closes potassium channels in rat locus coeruleus neurons. Neuroscience 50 (1992) 345-353
47. Shih, P.-W., Wu, Y.-W., Yang, H.-W., Min, M.-Y., 2006. Substance P acting on NK1 receptor increases excitability of neurons in A7 catecholamine cell group in rats. Program no. 547.15. Soci. Neurosci. (http://www.snf.org).
48. Shults C.W., Quirion R., Chronwall B., Chase T.N., and O'Donohue T.L. A comparison of the anatomical distribution of substance P and substance P receptors in the rat central nervous system. Peptides 5 6 (1984) 1097-1128
49. Strübing C., Krapivinsky G., Krapivinsky L., and Clapham D.E. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29 (2001) 645-655
50. Tozzi A., Bengtson C.P., Longone P., Carignani C., Fusco F.R., Bernardi G., and Mercuri N.B. Involvement of transient receptor potential-like channels in responses to mGluR-I activation in midbrain dopamine neurons. Eur. J. Neurosci. 18 (2003) 2133-2145
51. Velimirovic B.M., Koyano K., Nakajima S., and Nakajima Y. Opposing mechanisms of regulation of a G-protein-coupled inward rectifier K+ channel in rat brain neurons. Proc. Natl. Acad. Sci U. S. A. 92 (1995) 1590-1594
52. Venkatachalam K., Zheng F., and Gill D.L. Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem. 278 (2003) 29031-29040
53. Yasuda K., Robinson D.M., Selvaratnam S.R., Walsh C.W., McMorland A.J., and Funk G.D. Modulation of hypoglossal motoneuron excitability by NK 1 receptor activation in neonatal mice in vitro. J. Physiol. 534 (2001) 447-464
54. Yeomans D.C., Clark F.M., Paice J.A., and Proudfit H.K. Antinociception induced by electrical stimulation of spinally-projecting neurons in A7 catecholamine cell group of the rat. Pain 48 (1992) 449-461
55. Yeomans D.C., and Proudfit H.K. Projection of substance P-immunoreactive neurons located in the ventromedial medulla to the A7 noradrenergic nucleus of the rat demonstrated using retrograde tracing combined with immunohistochemistry. Brain Res. 532 (1990) 329-332
56. Yeomans D.C., and Proudfit H.K. Antinociception induced by microinjection of substance P into the A7 catecholamine cell group in the rat. Neuroscience 49 (1992) 681-691
57. Zhang C., Roepke T.A., Kelly M.J., and Rønnekleiv O.K. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J. Neurosci. 28 (2008) 4423-4434
58. Zhu M.H., Chae M., Kim H.J., Lee Y.M., Kim M.J., Jin N.G., Yang D.K., So I., and Kim K.W. Desensitization of canonical transient receptor potential channel 5 by protein kinase C. Am. J. Physiol. Cell Physiol. 289 (2005) C591-C600