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Interactions between tachykinins and diverse, human nicotinic acetylcholine receptor subtypes

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Abstract

Nicotinic acetylcholine receptors (nAChR) are diverse members of the ligand-gated ion channel superfamily of neurotransmitter receptors and play critical roles in chemical signaling throughout the nervous system. Reports of effects of substance P (SP) on nAChR function prompted us to investigate interactions between several tachykinins and human nAChR subtypes using clonal cell lines as simple experimental models. Acute exposure to SP inhibits carbamylcholine- or nicotinestimulated function measured using86Rb+ efflux assays of human ganglionic (α3β4) nAChR expressed in SH-SY5Y neuroblastoma cells (IC50∼2.3 μM) or of human muscle-type (α1β1γδ) nAChR expressed in TE671/RD clonal cells (IC50∼21 μM). SP also acutely blocks function of rat ganglionic nAChR expressed in PC12 pheochromocytoma cells (IC50∼2.1 μM). Neurokinin A and eledoisin inhibit function (extrapolated IC50 values between 60 and 160 μM) of human muscle-type or ganglionic nAChR, but neurokinin B does not, and neither human nAChR is as sensitive as PC12 cell α3β4-nAChR to eledoisin or neurokinin A inhibition. At concentrations that produce blockade of nAChR function, SP fails to affect binding of [3H]acetylcholine to human muscle-type or ganglionic nAChR. SP-mediated blockade of rat or human ganglionic nAChR function is insurmountable by increasing agonist concentrations. Collectively, these results indicate that tachykinins act noncompetitively to inhibit human nAChR function with potencies that vary across tachykinins and nAChR subtypes. They also indicate that tachykinin actions at nAChR could further contribute to complex cross-talk between nicotinic cholinergic and tachykinin signals in regulation of nervous system activity.

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Abbreviations

ACh:

acetylcholine

[3H]ACh:

[3H]acetylcholine

Bgt:

α-bungarotoxin

CNS:

central nervous system

DMEM:

Dulbecco's modified Eagle's medium

I-Bgt:

125I-labeled mono-iodinated α-bungarotoxin

nAChR:

meotinic acetylcholine receptor

NK A:

neurokinin A

NK B:

neurokinin B

SP:

substance P

TK:

tachykinin(s)

References

  1. Changeux, J.-P., Galzi, J.-L., Devillers-Thiery, A., and Bertrand, D. 1992. The functional architecture of the acetylcholine receptor explored by affinity labeling and site directed mutagenesis. Quart. Rev. Biophys. 25:395–432.

    Article  CAS  Google Scholar 

  2. Lukas, R. J., and Bencherif, M. 1992. Heterogeneity and regulation of nicotinic acetylcholine receptors. Intl. Review Neurobiol. 34:25–131.

    CAS  Google Scholar 

  3. Sargent, P. B. 1993. The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16:403–443.

    Article  PubMed  CAS  Google Scholar 

  4. Lukas, R. J. 1995. Diversity and patterns of regulation of nicotinic receptor subtypes. Annals New York Acad. Sci. 757:153–168.

    CAS  Google Scholar 

  5. Lukas, R. J., Norman S. A. and Lucero L. 1993. Characterization of nicotinic acetylcholine receptors expressed by cells of the SH-SY5Y human neuroblastoma clonal line. Mol. Cell. Neurosci. 4: 1–12.

    Article  CAS  PubMed  Google Scholar 

  6. Vernallis, A. B., Conroy, W. G., and Berg, D. K. 1993. Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451–464.

    Article  PubMed  CAS  Google Scholar 

  7. Alkondon, M., and Albuquerque, E. X. 1993. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J. Pharmacol. Exp. Ther. 265:1455–1473.

    PubMed  CAS  Google Scholar 

  8. Puchacz, E. P., Buisson, B., Bertrand, D., and Lukas, R. J. 1994. Functional expression of nicotinic acetylcholine receptors containing rat α7 subunits in human SH-SY5Y neuroblastoma cells. F.E.B.S. Lett. 354:155–159.

    Article  CAS  Google Scholar 

  9. Whiting, P., and Lindstrom, J. 1987. Rurification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc. Natl. Acad. Sci. USA 84:595–599.

    Article  PubMed  CAS  Google Scholar 

  10. Flores, C. M., Rogers, S. W., Pabreza, L. A., Wolfe, B. B., and Kellar, K. J. 1992. A subtype of nicotinic cholinergic receptor in rat brain is composed of α4 and β2 subunits and is up-regulated by chronic nicotine treatment. Mol. Pharmacol. 41:31–37.

    PubMed  CAS  Google Scholar 

  11. Erspamer, V. 1981. The tachykinin peptide family. Trends Neurol. Sci. 4:267–269.

    Article  CAS  Google Scholar 

  12. Maggio, J. E. 1988. Tachykinins. Annu. Rev. Neurosci. 11:13–28.

    Article  PubMed  CAS  Google Scholar 

  13. Mussap, C. J., Geraghty, D. P., and Burcher E. 1993. Tachykinin receptors: A radioligand binding perspective. J. Neurochen. 60: 1987–2009.

    Article  CAS  Google Scholar 

  14. Steinacker, A., and Highstein, S. M. 1976. Pre- and post-synaptic action of substance P at the Mauther fiber-giant fiber synapse in the hatchet fish. Brain Res. 114:128–133.

    Article  PubMed  CAS  Google Scholar 

  15. Belcher, G., and Ryall, R. W. 1977. Substance P and Renshaw cells: A new concept of inhibitory synaptic interactions. J. Physiol. (Lond.) 272:105–119.

    CAS  Google Scholar 

  16. Davies, J., and Dray, A. 1977. Substance P and opiate receptors. Nature 268:351–352.

    Article  PubMed  CAS  Google Scholar 

  17. Krnjevic, K., and Lekic, D. 1977. Substance P selectively blocks excitation of Renshaw cell by acetylcholine. Can. J. Physiol. Pharmacol. 55:958–961.

    PubMed  CAS  Google Scholar 

  18. Ryall, R. W., and Belcher, G. 1977. Substance P selectively blocks nicotinic receptors on Renshaw cells: A possible synaptic inhibitory mechanism. Brain Res. 137:376–380.

    Article  PubMed  CAS  Google Scholar 

  19. Livett, B.G., Kozousek, V., Mizobe, F., and Dean, D. M. 1979. Substance P inhibits nicotinic activation of chromaffin cells. Nature 278:256–257.

    Article  PubMed  CAS  Google Scholar 

  20. Mizobe, F., Kozousek, V., Dean, D. M., and Livett, B. G. 1979. Pharmacological characterization of adrenal paraneurons: substance P and somatostatin as inhibitory modulators of the nicotinic response. Brain Res. 178:555–566.

    Article  PubMed  CAS  Google Scholar 

  21. Stallcup, W. B., and Patrick, J. 1980. Substance P enhances cholinergic receptor desensitization in a clonal nerve cell line. Proc. Natl. Acad. Sci., USA 77:634–638.

    Article  PubMed  CAS  Google Scholar 

  22. Ryall, R. W. 1982. Modulation of cholinergic transmission by substance P. Ciba Found. Symp. 91:267–280.

    PubMed  CAS  Google Scholar 

  23. Akasu, T., Kojima, M., and Koketsu, K. 1983. Substance P modulates the sensitivity of the nicotinic receptor in amphibian cholinergic transmission. Br. J. Pharmacol. 80:123–131.

    PubMed  CAS  Google Scholar 

  24. Akasu, T., Ohta, Y., and Koketsu, K. 1984. Neuropeptides facilitate the desensitization of nicotinic acetylcholine-receptor in frog skeletal muscle endplate. Brain Res. 290:342–347.

    Article  PubMed  CAS  Google Scholar 

  25. Clapham, D. E., and Neher, E. 1984. Substance P reduces acetylcholine-induced currents in isolated bovine chromaffin cells. J. Physiol. (Lond.) 347:255–277.

    CAS  Google Scholar 

  26. Ip, N. Y., and Zigmond, R. E. 1984. Substance P inhibits the acute stimulation of ganglionic tyrosine hydroxylase activity by a nicotinic agonist. Neurosci. 13:217–220.

    Article  CAS  Google Scholar 

  27. Role, L. W. 1984. Substance P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons. Proc. Natl. Acad. Sci., USA 81:2924–2928.

    Article  PubMed  CAS  Google Scholar 

  28. Boksa, P., and Livett, B. G. 1985. The substance P receptor subtype modulating catecholamine release from adrenal chromaffin cells. Brain Res. 332:29–38.

    Article  PubMed  CAS  Google Scholar 

  29. Eardley D., and McGee, Jr. R. 1985. Both substance P agonists and antagonists inhibit ion conductance through nicotinic acetylcholine receptors on PC12 cells. Eur. J. Pharmacol. 114:101–104.

    Article  PubMed  CAS  Google Scholar 

  30. Simasko, S. M., Soares, J. R., and Weiland, G. A. 1985. Structure-activity relationship for substance P inhibition of carbamylcholine-stimulated22Na+ flux in neuronal (PC12) and non-neuronal (BC3H-1) cell lines. J Pharmacol. Exp. Ther. 235:601–605.

    PubMed  CAS  Google Scholar 

  31. Simasko, S. M., Durkin, J. A., and Weiland, G. A. 1987. Effects of substance P on nicotinic acetylcholine receptor function in PC12 cells. J. Neurochem. 49:253–260.

    Article  PubMed  CAS  Google Scholar 

  32. Jiang, Z. G., and Dun, N. J. 1986. Facilitation of nicotinic response in the guinea pig prevertebral neurons by substance P. Brain Res. 363:196–198.

    Article  PubMed  CAS  Google Scholar 

  33. Livett, B. G., and Zhou, X. F. 1991. Substance P interactions with the nicotinic response. Annals New York Acad. Sci. 632:249–262

    CAS  Google Scholar 

  34. Min, C. K., and Weiland, G. A. 1992. Substance P inhibits carbamylcholine-stimulated22Na+ efflux from acetylcholine receptorenrichedTorpedo electroplaque membrane vesicles. Brain Res. 586:348–351.

    Article  PubMed  CAS  Google Scholar 

  35. Valenta, D. C., Downing, J. E., and Role, L. W. 1983. Peptide modulation of ACh receptor desensitization controls neurotransmitter release from chicken sympathetic neurons. J. Neurophysiol. 69:928–942.

    Google Scholar 

  36. Cheung, N. S., Karlsson, P., Wang, J. X., Bienert, M., Oehme, P., and Livett, B. G. 1994. Functional studies with substance P analogues: Effects of N-terminal, C-terminal, and C-terminus-extended analogues of substance P on nicotine-induced secretion and desensitization in cultured bovine adrenal chromaffin cells. J. Neurochem. 62:2246–2253.

    Article  PubMed  CAS  Google Scholar 

  37. Zhou, X. F., Marley, P. D., and Livett, B. G. 1991. Substance P modulates the time course of nicotinic but not muscarinic catecholamine secretion from perfused adrenal glands of rat. Br. J. Pharmacol. 104:159–165.

    PubMed  CAS  Google Scholar 

  38. Shinkai, M., Takayangi, I., and Kato, T. 1993. Tachykinin receptors of the NK2 type involved in the acetylcholine release by nicotine in guinea-pig bladder. Br. J. Pharmacol. 108:759–762.

    PubMed  CAS  Google Scholar 

  39. Hanley, M. R., Sandberg, B. E. B., Lee, C. M., Iversen, L. L., Brundish, D. E., and Wade, R. Specific binding of3H-substance P to rat brain membranes. Nature 286:810–812.

  40. Beaujouan, J. C., Torrens, Y., Herbet, A., Daguet, M.-C., Glowinski, J., and Prochiantz, A. 1982. Specific binding of an immunoreactive and biologically active125I-labeled substance P derivative to mouse mesencephalic cells in primary culture. Mol. Pharmacol. 22:48–55.

    PubMed  CAS  Google Scholar 

  41. Buck, S. H., Burcher, E., Shults, C. W., Lovenberg, W., and O-Donohue, T. L. 1984. Novel pharmacology of substance K-binding sites: A third type of tachykinin receptor. Science 226:987–989.

    Article  PubMed  CAS  Google Scholar 

  42. Bergstrom, L., Torrens, Y., Saffroy, M., Beaujouan, J. C., Lavielle, S., Chassaing, G., Morgat, J. L., Glowinski, J., and Marquet, A. 1987. [3H]Neurokinin B and125I-Bolton Hunter eledoisin label identical tachykinin binding sites in the rat brain. J. Neurochem. 48:125–133.

    PubMed  CAS  Google Scholar 

  43. Torrens, Y., Daguet De Montety, M. C., El Etr, M., Beaujouan, J. C., and Glowinski, J. 1989. Tachykinin receptors of the NK1 type (substance P) coupled positively to phospholipase C on cortical astrocytes from newborn mouse in primary culture. J. Neurochem. 52:1913–1918.

    Article  PubMed  CAS  Google Scholar 

  44. Cascieri, M. A., Huang, R.-R. C., Fong, T. M., Cheung, A. H., Sadowski, S., Ber, E., and Strader, C. D. 1992. Determination of the amino acid residues in substance P conferring selectivity and specificity for the rat neurokinin receptors Mol. Pharmacol. 41: 1096–1099.

    PubMed  CAS  Google Scholar 

  45. Heuillet, E., Menager, J., Fardin, V., Flamand, O., Bock, M., Garret, C., Crespo A., Fallourd, A. M., and Doble, A. 1993. Characterization of a human NK, tachykinin receptor in the astrocytoma cell line U 373 MG. J. Neurochem. 60:868–876.

    Article  PubMed  CAS  Google Scholar 

  46. Cheung, N. S., Small, D. H., and Livett, B. G. 1993. An amyloid peptide, beta A4 25–35, mimics the function of substance P on modulation of nicotine-evoked secretion and desensitization in cultured bovine adrenal chromaffin cells. J. Neurochem. 60:1163–1166.

    Article  PubMed  CAS  Google Scholar 

  47. Simmons, L. K., Schuetze, S. M., and Role, L. W. 1990. Substance P modulates single-channel properties of neuronal nicotinic acetylcholine receptors. Neuron 4:393–403.

    Article  PubMed  CAS  Google Scholar 

  48. Eisenhour, C. M., and Lukas, R. J. 1995. Interactions of tachykinins with diverse nicotinic acetylcholine receptor subtypes. Soc. Neurosci. Abst. 21:1336.

    Google Scholar 

  49. Lukas, R. J. 1984. Properties of curaremimetic neurotoxin binding sites in the rat central nervous system. Biochem. 23:1152–1160.

    Article  CAS  Google Scholar 

  50. Lukas, R. J. 1986. Characterization of curaremimetic neurotoxin binding sites on membrane fractions derived from the human medulloblastoma clonal cell line TE671. J. Neurochem. 46:1936–1941.

    Article  PubMed  CAS  Google Scholar 

  51. Lukas, R. J. 1989. Pharmacological distinctions between functional nicotinic acetylcholine receptors on the PC12 rat pheochromocytoma and TE671 human medulloblastoma. J. Pharmacol. Exp. Ther. 251:175–182.

    PubMed  CAS  Google Scholar 

  52. Lukas, R. J. 1990. Heterogeneity of high-affinity nicotinic [3H]acetylcholine binding sites. J. Pharmacol. Exp. Ther. 253:51–57.

    PubMed  CAS  Google Scholar 

  53. Lukas, R. J. 1986. Immunochemical and pharmacological distinctions between curaremimetic neurotoxin binding sites of central, autonomic, and peripheral origin. Proc. Natl. Acad. Sci. USA 83: 5741–5745.

    Article  PubMed  CAS  Google Scholar 

  54. Bencherif, M., and Lukas, R. J. 1993. Cytochalasin modulation of nicotinic cholinergic receptor expression and muscarinic receptor function in human TE671/RD cells: A possible functional role of the cytoskeleton. J. Neurochem. 61:852–864.

    Article  PubMed  CAS  Google Scholar 

  55. Lukas, R. J., and Cullen, M. J. 1988 An isotopic rubidium ion efflux assay for the functional characterization of nicotinic acetylcholine receptors on clonal cell lines. Anal. Biochem. 175:212–218.

    Article  PubMed  CAS  Google Scholar 

  56. Bencherif, M., Eisenhour, C. M., Prince, R. J., Lippiello, P. M., and Lukas, R. J. 1995. The “calcium antagonist” TMB-8 [3,4,5-trimethoxy benzoic acid 8-(diethylamino)octyl ester] is a potent, non-competitive, functional antagonist at diverse nicotinic acetylcholine receptor subtypes. J. Pharmacol. Exp. Ther. 275:1418–1426.

    PubMed  CAS  Google Scholar 

  57. Takenouchi, T., and Munekata, E. 1994. Inhibitory effects of beta-amyloid peptides on nicotine-induced Ca2+ influx in PC12h cells in culture. Neurosci. Lett. 173:147–150.

    Article  PubMed  CAS  Google Scholar 

  58. Lukas, R. J. 1993. Expression of ganglia-type nicotinic acetylcholine receptors and nicotinic ligand binding sites by cells of the IMR-32 human neuroblastoma clonal line. J. Pharm. Exper. Thera. 265:294–302.

    CAS  Google Scholar 

  59. Lukas, R. J. 1991. Effects of chronic nicotinic ligand exposure on functional activity of nicotinic acetylcholine receptors expressed by cells of the PC12 rat pheochromocytoma or the TE671/RD human clonal lines. J. Neurochem. 56:1134–1145.

    Article  PubMed  CAS  Google Scholar 

  60. Min, C. K., and Weiland, G. A. 1993. Effects of substance P on the binding of agonists to the nicotinic acetylcholine receptor ofTorpedo electroplaque. J. Neurochem. 60:2238–2246.

    Article  PubMed  CAS  Google Scholar 

  61. Boksa, P., and Livett, B. G. 1984. Substance P protects against desensitization of the nicotinic response in isolated adrenal chromaffin cells. J. Neurochem. 42:618–627.

    Article  PubMed  CAS  Google Scholar 

  62. Boksa, P., St.-Pierre, S., and Livett, B. G. 1982. Characterization of substance P and somatostatin receptors on adrenal chromaffin cells using structural analogues. Brain Res. 245:275–283.

    Article  PubMed  CAS  Google Scholar 

  63. Khalil, Z., Marley, P. D., and Livett, B. G. 1988. Mammalian tachykinins modulate the nicotinic sensory response of cultured bovine adrenal chromaffin cells. Brain Res. 459:289–297.

    Article  PubMed  CAS  Google Scholar 

  64. Min, C. K., Owens, J., and Weiland, G. A. 1994. Characterization of the binding of [3H]substance P to the nicotinic acetylcholine receptor ofTorpedo electroplaque. Mol. Pharmacol. 45:221–227.

    PubMed  CAS  Google Scholar 

  65. Blanton, M. P., Li, Y.-M., Stimson, E. R., Maggio, J. E., and Cohen, J. B. 1994. Agonist-induced photoincorporation of ap-benzoylphenylalanine derivative of substance P into membranespanning region 2 of theTorpedo nicotinic acetylcholine receptor δ subunit. Mol. Pharmacol. 46:1048–1055.

    PubMed  CAS  Google Scholar 

  66. Weiland, G. A., Durkin, J. A., Henley, J. M., and Simasko, S. M. 1987. Effects of substance P on the binding of ligands to nicotinic acetylcholine receptors. 1987. Mol. Pharmacol. 32:625–632.

    PubMed  CAS  Google Scholar 

  67. Stafford, G. A., Oswald, R. E., and Weiland, G. A. 1994. The beta subunit of neuronal nicotinic acetylcholine receptors is a determinant of the affinity for substance P inhibition. Mol. Pharmacol. 45:758–762.

    PubMed  CAS  Google Scholar 

  68. Stafford, G. A., Oswald, R. E., Figl, A., Cohen, B. N., Lester, H. A., and Weiland, G. A. 1994. The apparent affinity of substance P for the neuronal nAChR is not determined by a single domain of the β subunit. Biophys. J. 66:A432.

    Google Scholar 

  69. Reiser, G., and Hamprecht, B. 1988. Characterization of a substance P receptor activating a cation permeability in neuronal cell lines. Eur. J. Pharmacol. 145:273–280.

    Article  PubMed  CAS  Google Scholar 

  70. Ohkubo, H., and Nakanishi, S. 1991. Molecular characterization of the three tachykinin receptors. Annals New York Acad. Sci. 632:53–62.

    CAS  Google Scholar 

  71. Geraghty, D. P., Livett, B. G., Rogerson, F. M., and Burcher, E. 1990. A novel substance P binding site in bovine adrenal medulla. Neurosci. Lett. 112:276–281.

    Article  PubMed  CAS  Google Scholar 

  72. Boyd, N. D., and Leeman, S. E. 1987. Multiple actions of substance P that regulate the functional properties of acetylcholine receptors of clonal rat PC12 cells. J. Physiol. (Lond.) 389:69–97.

    CAS  Google Scholar 

  73. Matsubara, N., and Hess, G. P. 1992. On the mechanism of a mammalian neuronal type nicotinic acetylcholine receptor investigated by a rapid chemical kinetic technique: Detection and characterization of a short-lived, previously unobserved, main receptor form in PC12 cells. Biochem. 31:5477–5487.

    Article  CAS  Google Scholar 

  74. Utkin, Y. N., Lazakovich, E. M., Kasheverov, I. E., and Tsetlin, V. I. 1989. α-Bungarotoxin interacts with the rat brain tachykinin receptors. F.E.B.S. Lett. 255:111–115.

    Article  CAS  Google Scholar 

  75. Utkin, Y. N., Kasheverov, I. E., and Tsetlin, V. I. 1992. Effects of purified snake venom components on substance P binding to rat brain membranes. J. Natural Toxins 1:77–83.

    CAS  Google Scholar 

  76. Rotter A., and Jacobowitz, D. M. 1984. Localization of substance P, acetylcholinesterase, muscarinic receptors and alpha-bungarotoxin binding sites in the rat interpeduncular nucleus. Brain Res. Bull. 12:83–94.

    Article  PubMed  CAS  Google Scholar 

  77. Jansen, K. L., Faull, R. L., Dragunow, M., and Leslie R. A. 1991. Distribution of excitatory and inhibitory amino acid, sigma, monoamine, catecholamine, acetylcholine, opioid, neurotensin, substance P, adenosine and neuropeptide Y receptors in human motor and somatosensory cortex. Brain Res. 566:225–238.

    Article  PubMed  CAS  Google Scholar 

  78. Matteoli, M., Haimann, C., and De Camilli, P. 1990. Substance P-like immunoreactivity at the frog neuromuscular junction. Neurosci. 37:271–275.

    Article  CAS  Google Scholar 

  79. Basile, S., Cheung, N. S., and Livett, B. G. 1992. Chromatographic evidence for the presence of multiple tachykinins in the bovine adrenal medulla. J. Neurochem. 58:1584–1586.

    Article  PubMed  CAS  Google Scholar 

  80. Fuxe, K., Siegel, R. A., Andersson, K., Eneroth, P., Mascagni, F., and Agnati, L. F. 1985. Acute continuous exposure to cigarette smoke produces discrete changes in cholycystokinin and substance P levels in the hypothalamus and preoptic area of the male rat. Acta Physiol. Scand. 125:437–443.

    Article  PubMed  CAS  Google Scholar 

  81. Naftchi, N. E., Maker, H., Lapin, E., Sleis, J., Lajtha, A., and Leeman, S. 1988. Acute reduction of brain substance P induced by nicotine. Neurochem. Res. 13:305–309.

    Article  PubMed  CAS  Google Scholar 

  82. Takayanagi, I., Moriya, M., Kurata, R., and Koike, K. 1991. Effects of ageing on nicotine-induced contraction and substance P-like materials release in guinea-pig bronchus. Gen. Pharmacol. 22: 783–785.

    PubMed  CAS  Google Scholar 

  83. Akasu, T. 1986. The effects of substance P on neuromuscular transmission in the frog. Neurosci. Res. 3:275–284.

    Article  PubMed  CAS  Google Scholar 

  84. Molinero, M. T., and Del Rio, J. 1987. Substance P, nicotinic acetylcholine receptors and antinociception in the rat. Neuropharm. 26:1715–1720.

    Article  CAS  Google Scholar 

  85. Brunsson, I., Fahrenkrug, J., Jodal, M., Sjoqvist, A., and Lundgren, O. 1995. Substance P effects on blood flow, fluid transport and vasoactive intestinal polypeptide release in the feline small intestine. J. Physiol. (Lond.) 483:727–734.

    CAS  Google Scholar 

  86. Sastry, B. V. 1995. Neuropharmacology of nicotine: Effects on the autoregulation of acetylcholine release by substance P and methionine enkephalin in rodent cerebral slices and toxicological implications. Clin. Exp. Pharmacol. Physiol. 22:288–290.

    PubMed  CAS  Google Scholar 

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Lukas, R.J., Eisenhour, C.M. Interactions between tachykinins and diverse, human nicotinic acetylcholine receptor subtypes. Neurochem Res 21, 1245–1257 (1996). https://doi.org/10.1007/BF02532402

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