The α4β2α5 nicotinic cholinergic receptor in rat brain is resistant to up-regulation by nicotine in vivo

Journal of Neurochemistry

Volumn 104, Issue 2, 2008, Pages 446-456

  Mao, Danyan ^a   Perry, David C ^b   Yasuda, Robert P ^a   Wolfe, Barry B ^a   Kellar, Kenneth J ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

5 nicotinic subunit; Nicotine; Nicotinic receptor; Regulation; Subunit composition

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR; RECEPTOR ANTIBODY; RECEPTOR SUBUNIT; EPIBATIDINE; FUSED HETEROCYCLIC RINGS; NICOTINIC AGENT; PROTEIN SUBUNIT; PYRIDINE DERIVATIVE;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; IMMUNOPRECIPITATION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SUPERIOR COLLICULUS; THALAMUS; TISSUE DISTRIBUTION; TOBACCO DEPENDENCE; UPREGULATION; ANIMAL; BINDING SITE; DRUG EFFECT; GENETICS; METABOLISM; METHODOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BINDING SITES; BRAIN; IMMUNOPRECIPITATION; NICOTINE; NICOTINIC AGONISTS; PROTEIN SUBUNITS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; UP-REGULATION;

EID: 37349116624     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05011.x     Document Type: Article

References (55)

1. Alkondon M. Albuquerque E. X. (2001) Nicotinic acetylcholine receptor α7 and α4β2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J. Neurophysiol. 86, 3043 3055.
2. Alkondon M. Albuquerque E. X. (2002) A non-α7 nicotinic acetylcholine receptor modulates excitatory input to hippocampal CA1 interneurons. J. Neurophysiol. 87, 1651 1654.
3. Alkondon M., Pereira E. F. R. Albuquerque E. X. (1998) α-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res. 810, 257 263.
4. 3H]nicotine binding sites in human brain. J. Neurochem. 50, 1243 1247.
5. Bevington P. R. (1969) Data reduction and error analysis for the physical sciences, pp. 58 64. McGraw-Hill Companies, New York.
6. Boulter J., O'Shea-Greenfield A., Duvoisin R., Connolly J., Wada E., Jensen A., Gardner P., Ballivet M., Deneris E. McKinnon D (1990) α3, α5, and β4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a gene cluster. J. Biol. Chem. 265, 4472 4482.
7. 3H]nicotine binding in human postmortem brain. J. Pharmacol. Exp. Ther. 282, 7 13.
8. Buisson B. Bertrand D. (2001) Chronic exposure to nicotine upregulates the human α4β2 nicotinic acetylcholine receptor function. J. Neurosci. 21, 1819 1829.
9. Champtiaux N., Gotti C., Cordero-Erausquin M. et al. (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J. Neurosci. 23, 7820 7829.
10. Conroy W. G. Berg D. K. (1995) Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270, 4424 4431.
11. Conroy W. G. Berg D. K. (1998) Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the α4, β2, and α5 gene products. Mol. Pharmacol. 53, 392 401.
12. Davila-Garcia M. I., Houghtling R. A., Qasba S. S. Kellar K. J. (1999) Nicotinic receptor binding sites in rat primary neuronal cells in culture: characterization and their regulation by chronic nicotine. Brain Res. Mol. Brain Res. 66, 14 23.
13. Del Signore A., Gotti C., Rizzo A., Moretti M. Paggi P (2004) Nicotinic acetylcholine receptor subtypes in the rat sympathetic ganglion: pharmacological characterization, subcellular distribution and effect of pre- and postganglionic nerve crush. J. Neuropathol. Exp. Neurol. 63, 138 150.
14. Flores C., Rogers S., Pabreza L., Wolfe B. Kellar K (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.
15. Fucile S., Barabino B., Palma E., Grassi F., Limatola C., Mileo A. M., Alema S., Ballivet M. Eusebi F. (1997) α5 subunit forms functional α3β4α5 nAChRs in transfected human cells. Neuroreport 8, 2433 2436.
16. Gerzanich V., Wang F., Kuryatov A. Lindstrom J (1998) α5 subunit alters desensitization, pharmacology, Ca++ permeability and Ca++ modulation of human neuronal α3 nicotinic receptors. J. Pharmacol. Exp. Ther. 286, 311 320.
17. Girod R., Crabtree G., Ernstrom G., Ramirez-Latorre J., McGehee D. Role L. (1999) Heteromeric complexes of alpha5 and/or alpha 7 subunits. Effects of calcium and potential role of nicotine-induced presynaptic facilitation. Ann. NY Acad. Sci. 30, 578 590.
18. Gopalakrishnan M., Molinari E. J. Sullivan J. P. (1997) Regulation of human α4β2 neuronal nicotinic acetylcholine receptor by cholinergic channel ligands and second messenger pathways. Mol. Pharmacol. 52, 524 534.
19. Gotti C., Moretti M., Zanardi A., Gaimarri A., Champtiaux N., Changeux J-P., Whiteaker P., Marks M. J., Clementi F. Zoli M. (2005) Heterogeneity and selective targeting of neuronal nicotinic acetylcholine receptor (nAChR) subtypes expressed on retinal afferents of the superior colliculus and lateral geniculate nucleus: identification of a new native nAChR subtype α3β2(α5 or β3) enriched in retinocollicular afferents. Mol. Pharmacol. 68, 1162 1171.
20. Hernandez S. C., Vicini S., Xiao Y., Davila-Garcia M. I., Yasuda R. P., Wolfe B. B. Kellar K. J. (2004) The nicotinic receptor in the rat pineal gland is an α3β4 subtype. Mol. Pharmacol. 66, 978 987.
21. Karlin A Akabas M. H. (1995) Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15, 1231 1244.
22. Kuryatov A., Luo J., Cooper J. Lindstrom J. (2005) Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol. Pharmacol. 68, 1839 1851.
23. Mao D., Yasuda R. P., Fan H., Wolfe B. B. Kellar K. J. (2006) Heterogeneity of nicotinic cholinergic receptors in rat superior cervical and nodose ganglia. Mol. Pharmacol. 70, 1693 1699.
24. Marks M., Burch J. Collins A. (1983) Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J. Pharmacol. Exp. Ther. 226, 817 825.
25. Marks M., Pauly J., Gross S., Deneris E., Hermans-Borgmeyer I., Heinemann S. Collins A (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12, 2765 2784.
26. Marritt A. M., Cox B. C., Yasuda R. P., McIntosh J. M., Xiao Y., Wolfe B. B. Kellar K. J. (2005) Nicotinic cholinergic receptors in the rat retina: simple and mixed heteromeric subtypes. Mol. Pharmacol. 68, 1656 1668.
27. 0-α-connotoxin MII binding in rat mesostriatal dopamine pathway following continuous infusion of nicotine. Neuroscience 137, 565 572.
28. Musachio J., Horti A., London E. D. Dannals R. F. (1997) Synthesis of a radioiodinated analog of epibatidine: (±)-exo-2-(2-iodo-5-pyridyl)-7- azabicyclo[2.2.1]heptane for in vitro and in vivo studies of nicotinic acetylcholine receptors. J. Labelled Compds. Radiopharm. 39, 39 48.
29. Nashmi R., Dickinson M. E., McKinney S., Jareb M., Labarca C., Fraser S. E. Lester H. A. (2003) Assembly of α4β2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J. Neurosci. 23, 11554 11567.
30. Nguyen H. N., Rasmussen B. A. Perry D. C. (2003) Subtype-selective up-regulation by chronic nicotine of high-affinity nicotinic receptors in rat brain demonstrated by receptor autoradiography. J. Pharmacol. Exp. Ther. 307, 1090 1097.
31. Nguyen H. N., Rasmussen B. A. Perry D. C. (2004) Binding and functional activity of nicotinic cholinergic receptors in selected rat brain regions are increased following long-term but not short-term nicotine treatment. J. Neurochem. 90, 40 49.
32. Peng X., Gerzanich V., Anand R., Whiting P. Lindstrom J (1994) Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol. Pharmacol. 46, 523 530.
33. Peng X., Gerzanich V., Anand R., Wang F. Lindstrom J (1997) Chronic nicotine treatment up-regulates α3 and α7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol. Pharmacol. 51, 776 784.
34. Perry D. C., Davila-Garcia M. I., Stockmeier C. A. Kellar J. K. (1999) Increased nicotinic receptors in brains from smokers: membrane binding and autoradiography studies. J. Pharmacol. Exp. Ther. 289, 1545 1552.
35. Perry D., Xiao Y., Nguyen H., Musachio J., Davila-Garcia M. Kellar K. (2002) Measuring nicotinic receptors with characteristics of α4β2, α3β2 and α3β4 subtypes in rat tissues by autoradiography. J. Neurochem. 82, 468 481.
36. Perry D. C., Mao D., Gold A. B., McIntosh J. M., Pezzullo J. C. Kellar K. J. (2007) Chronic nicotine differentially regulates α6- and β3-containing nicotinic cholinergic receptors in rat brain. J. Pharmacol. Exp. Ther. 322, 306 315.
37. Ramirez-Latorre J., Yu C. R., Qu X., Perin F., Karlin A. Role L. (1996) Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature 380, 347 351.
38. Rogers S., Mandelzys A., Deneris E., Cooper E. Heinemann S. (1992) The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J. Neurosci. 12, 4611 4623.
39. Salas R., Orr-Urtreger A., Broide R. S., 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.
40. Sallette J., Pons S., Devillers-Thiery A., Soudant M., Prado de Carvalho L., Changeux J-P. Corringer P. J. (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46, 595 607.
41. Salminen O., Murphy K. L., McIntosh J. M., Drago J., Marks M. J., Collins A. C. Grady S. R. (2004) Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol. Pharmacol. 65, 1526 1535.
42. Schwartz R. Kellar K. J. (1983) Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science 220, 214 216.
43. Stitzel J. A., Blanchette J. M. Collins A. C. (1998) Sensitivity to the seizure-inducing effects of nicotine is associated with strain-specific variants of the α5 and α7 nicotinic receptor subunit genes. J. Pharmacol. Exp. Ther. 284, 1104 1111.
44. Sudweeks S. N. Yakel J. L. (2000) Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J. Physiol. (Lond.) 527, 515 528.
45. 3 human acetylcholine receptors. Mol. Pharmacol. 71, 769 776.
46. Turner J. R. Kellar K. J. (2005) Nicotinic cholinergic receptors in the rat cerebellum: multiple heteromeric subtypes. J. Neurosci. 25, 9258 9265.
47. Vallejo Y. F., Buisson B., Bertrand D. Green W. N. (2005) Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J. Neurosci. 25, 5563 5572.
48. Wada E., McKinnon D., Heinemann S., Patrick J. Swanson L. W. (1990) The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (α5) in the rat central nervous system. Brain Res. 526, 45 53.
49. Wang F., Nelson M. E., Kuryatov A., Olale F., Cooper J., Keyser K. Lindstrom J. (1998) Chronic nicotine treatment up-regulates human α3β2 but not α3β4 acetylcholine receptors stably transfected in human embryonic kidney cells. J. Biol. Chem. 273, 28721 28732.
50. Whiting P. Lindstrom J. (1987) Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc. Natl Acad. Sci. USA 84, 595 599.
51. Wonnacott S. (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci. 20, 92 98.
52. Xiao Y. Kellar K. J. (2004) The comparative pharmacology and up-regulation of rat neuronal nicotinic receptor subtype binding sites stably expressed in transfected mammalian cells. J. Pharmacol. Exp. Ther. 310, 98 107.
53. Yeh J. J., Ferreira M., Ebert S., Yasuda R. P., Kellar K. J. Wolfe B. B. (2001) Axotomy and nerve growth factor regulate levels of neuronal nicotinic acetylcholine receptor α3 subunit protein in the rat superior cervical ganglion. J. Neurochem. 79, 258 265.
54. Yu C. R. Role L. W. (1998) Functional contribution of the α5 subunit to neuronal nicotinic channels expressed by chick sympathetic ganglion neurons. J. Physiol. (Lond.) 509, 667 681.
55. Zoli M., Moretti M., Zanardi A., McIntosh J. M., Clementi F. Gotti C. (2002) Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J. Neurosci. 22, 8785 8789.