Nicotinic acetylcholine receptors control acetylcholine and noradrenaline release in the rodent habenulo-interpeduncular complex

British Journal of Pharmacology

Volumn 171, Issue 23, 2014, Pages 5209-5224

  Beiranvand, F ^a   Zlabinger, C ^a   Orr Urtreger, A ^b   Ristl, R ^c   Huck, S ^a   Scholze, P ^a  

^a Medical University of Vienna   (Austria)

^b TEL AVIV UNIVERSITY   (Israel)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; NICOTINIC RECEPTOR; NORADRENALIN; PROTEIN SUBUNIT;

ANIMAL; C57BL MOUSE; FEMALE; GENETICS; HABENULA; INTERPEDUNCULAR NUCLEUS; KNOCKOUT MOUSE; MALE; METABOLISM; PROTEIN SUBUNIT; SPRAGUE DAWLEY RAT;

ACETYLCHOLINE; ANIMALS; FEMALE; HABENULA; INTERPEDUNCULAR NUCLEUS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOREPINEPHRINE; PROTEIN SUBUNITS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC;

EID: 84939942074     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12841     Document Type: Article

References (50)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol. 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol. 170: 1582-1606.
3. 3H]norepinephrine release from mouse hippocampal synaptosomes. Mol Pharmacol 70: 967-976.
4. Baddick CG, Marks MJ, (2011). An autoradiographic survey of mouse brain nicotinic acetylcholine receptors defined by null mutants. Biochem Pharmacol 82: 828-841.
5. Berridge CW, Waterhouse BD, (2003). The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42: 33-84.
6. Bianco IH, Wilson SW, (2009). The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364: 1005-1020.
7. Bierut LJ, Stitzel JA, Wang JC, Hinrichs AL, Grucza RA, Xuei X, et al. (2008). Variants in nicotinic receptors and risk for nicotine dependence. Am J Psychiatry 165: 1163-1171.
8. Brown DA, Docherty RJ, Halliwell JV, (1983). Chemical transmission in the rat interpeduncular nucleus in vitro. J Physiol 341: 655-670.
9. Brown RWB, Collins AC, Lindstrom JM, Whiteaker P, (2007). Nicotinic α5 subunit deletion locally reduces high-affinity agonist activation without altering nicotinic receptor numbers. J Neurochem 103: 204-215.
10. Bruijnzeel AW, (2012). Tobacco addiction and the dysregulation of brain stress systems. Neurosci Biobehav Rev 36: 1418-1441.
11. David R, Ciuraszkiewicz A, Simeone X, Orr-Urtreger A, Papke RL, McIntosh JM, et al. (2010). Biochemical and functional properties of distinct nicotinic acetylcholine receptors in the superior cervical ganglion of mice with targeted deletions of nAChR subunit genes. Eur J Neurosci 31: 978-993.
12. Fischer H, Orr-Urtreger A, Role LW, Huck S, (2005). Selective deletion of the α5 subunit differentially affects somatic-dendritic versus axonally targeted nicotinic ACh receptors in mouse. J Physiol 563: 119-137.
13. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ, (2011). Habenular α5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471: 597-601.
14. Frahm S, Slimak MA, Ferrarese L, Santos-Torres J, Antolin-Fontes B, Auer S, et al. (2011). Aversion to nicotine is regulated by the balanced activity of β4 and α5 nicotinic receptor subunits in the medial habenula. Neuron 70: 522-535.
15. Fucile S, Barabino B, Palma E, Grassi F, Limatola C, Mileo AM, et al. (1997). α5 subunit forms functional α3β4α5 nAChRs in transfected human cells. Neuroreport 8: 2433-2436.
16. Gallego X, Molas S, Amador-Arjona A, Marks MJ, Robles N, Murtra P, et al. (2012). Overexpression of the CHRNA5/A3/B4 genomic cluster in mice increases the sensitivity to nicotine and modifies its reinforcing effects. Amino Acids 43: 897-909.
17. ++ modulation of human neuronal α3 nicotinic receptors. J Pharmacol Exp Ther 286: 311-320.
18. Glick SD, Sell EM, McCallum SE, Maisonneuve IM, (2011). Brain regions mediating α3β4 nicotinic antagonist effects of 18-MC on nicotine self-administration. Eur J Pharmacol 669: 71-75.
19. Grady SR, Meinerz NM, Cao J, Reynolds AM, Picciotto MR, Changeux JP, et al. (2001). Nicotinic agonists stimulate acetylcholine release from mouse interpeduncular nucleus: a function mediated by a different nAChR than dopamine release from striatum. J Neurochem 76: 258-268.
20. Grady SR, Moretti M, Zoli M, Marks MJ, Zanardi A, Pucci L, et al. (2009). Rodent habenulo-interpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the α3β4∗ and α3β3β4∗ subtypes mediate acetylcholine release. J Neurosci 29: 2272-2282.
21. Grady SR, Wageman CR, Patzlaff NE, Marks MJ, (2012). Low concentrations of nicotine differentially desensitize nicotinic acetylcholine receptors that include α5 or α6 subunits and that mediate synaptosomal neurotransmitter release. Neuropharmacology 62: 1935-1943.
22. Hsu YW, Tempest L, Quina LA, Wei AD, Zeng H, Turner EE, (2013). Medial habenula output circuit mediated by α5 nicotinic receptor-expressing GABAergic neurons in the interpeduncular nucleus. J Neurosci 33: 18022-18035.
23. Jackson KJ, Marks MJ, Vann RE, Chen X, Gamage TF, Warner JA, et al. (2010). Role of α5 nicotinic acetylcholine receptors in pharmacological and behavioral effects of nicotine in mice. J Pharmacol Exp Ther 334: 137-146.
24. Kawaja MD, Flumerfelt BA, Hrycyshyn AW, (1989). Glutamate decarboxylase immunoreactivity in the rat interpeduncular nucleus: a light and electron microscope investigation. Neuroscience 30: 741-753.
25. Kennett A, Heal DJ, Wonnacott S, (2012). Pharmacological differences between rat frontal cortex and hippocampus in the nicotinic modulation of noradrenaline release implicate distinct receptor subtypes. Nicotine Tob Res 14: 1339-1345.
26. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
27. Kim U, Chang SY, (2005). Dendritic morphology, local circuitry, and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J Comp Neurol 483: 236-250.
28. Klemm WR, (2004). Habenular and interpeduncularis nuclei: shared components in multiple-function networks. Med Sci Monit 10: RA261-RA273.
29. Kobayashi Y, Sano Y, Vannoni E, Goto H, Suzuki H, Oba A, et al. (2013). Genetic dissection of medial habenula-interpeduncular nucleus pathway function in mice. Front Behav Neurosci 7: 17.
30. Kulak JM, McIntosh JM, Yoshikami D, Olivera BM, (2001). Nicotine-evoked transmitter release from synaptosomes: functional association of specific presynaptic acetylcholine receptors and voltage-gated calcium channels. J Neurochem 77: 1581-1589.
31. Kuryatov A, Onksen J, Lindstrom J, (2008). Roles of accessory subunits in α4β2 nicotinic receptors. Mol Pharmacol 74: 132-143.
32. Lecourtier L, Kelly PH, (2007). A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Biobehav Rev 31: 658-672.
33. Lena C, Changeux J-P, Mulle C, (1993). Evidence for 'preterminal' nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J Neurosci 13: 2680-2688.
34. McCormick DA, Prince D, (1987). Acetylcholine causes rapid nicotinic excitation in the medial habenular nucleus of the guinea pig, in vitro. J Neurosci 7: 742-752.
35. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
36. Mulle C, Vidal C, Benoit P, Changeux J-P, (1991). Existence of different subtypes of nicotinic acetylcholine receptors in the rat habenulo-interpeduncular system. J Neurosci 11: 2588-2597.
37. Oleskevich S, Descarries L, Lacaille JC, (1989). Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9: 3803-3815.
38. Papke RL, Heinemann SF, (1994). Partial agonist properties of cytisine on neuronal nicotinic receptors containing the β2 subunit. Mol Pharmacol 45: 142-149.
39. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl. Acids Res. 42 (Database Issue): D1098-1106.
40. Qin C, Luo M, (2009). Neurochemical phenotypes of the afferent and efferent projections of the mouse medial habenula. Neuroscience 161: 827-837.
41. Ramirez-Latorre J, Yu CR, Qu X, Perin F, Karlin A, Role LW, (1996). Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature 380: 347-351.
42. Ren J, Qin C, Hu F, Tan J, Qiu L, Zhao S, et al. (2011). Habenula 'cholinergic' neurons co-release glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69: 445-452.
43. Robertson SD, Plummer NW, de Marchena J, Jensen P, (2013). Developmental origins of central norepinephrine neuron diversity. Nat Neurosci 16: 1016-1023.
44. Salas R, Orr-Urtreger A, Broide RS, Beaudet A, Paylor R, De Biasi M, (2003). The nicotinic acetylcholine receptor subunit α5 mediates short-term effects of nicotine in vivo. Mol Pharmacol 63: 1059-1066.
45. Salas R, Sturm R, Boulter J, De Biasi M, (2009). Nicotinic receptors in the habenulo-interpeduncular system are necessary for nicotine withdrawal in mice. J Neurosci 29: 3014-3018.
46. Salminen O, Murphy KL, McIntosh JM, Drago J, Marks MJ, Collins AC, et al. (2004). Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 65: 1526-1535.
47. Scholze P, Koth G, Orr-Urtreger A, Huck S, (2012). Subunit composition of α5-containing nicotinic receptors in the rodent habenula. J Neurochem 121: 551-560.
48. Wang F, Gerzanich V, Wells GB, Anand R, Peng X, Keyser K, et al. (1996). Assembly of human neuronal nicotinic receptor α5 subunits with α3, β2, and β4 subunits. J Biol Chem 271: 17656-17665.
49. Wonnacott S, (1997). Presynaptic nicotinic ACh receptors. Trends Neurosci 20: 92-98.
50. Yamaguchi T, Danjo T, Pastan I, Hikida T, Nakanishi S, (2013). Distinct roles of segregated transmission of the septo-habenular pathway in anxiety and fear. Neuron 78: 537-544.