Neuronal and Astrocyte Expression of Nicotinic Receptor Subunit β4 in the Adult Mouse Brain

Journal of Comparative Neurology

Volumn 468, Issue 3, 2004, Pages 322-333

  Gahring, Lorise C ^a,b   Persiyanov, Karina ^b   Rogers, Scott W ^a,b  

^a Education and Clinical Center   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Hippocampus; Immunohistochemistry; Interneurons; Mouse strains; Nicotinic receptors

Indexed keywords

GLUTAMATE DEHYDROGENASE; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; ASTROCYTE; AUDITORY NERVOUS SYSTEM; BRAIN; FOREBRAIN; HABENULA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURON; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; RHOMBENCEPHALON; THALAMUS;

ANIMALS; ASTROCYTES; AUDITORY CORTEX; BRAIN CHEMISTRY; FEMALE; HABENULA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED CBA; NERVE TISSUE PROTEINS; NEURONS; RECEPTORS, NICOTINIC; RHOMBENCEPHALON; SPECIES SPECIFICITY; THALAMUS;

EID: 0346389568     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10942     Document Type: Article

References (65)

1. Albuquerque EX, Pereira EF, Bonfante-Cabarcas R, Marchioro M, Matsubayashi H, Alkondon M, Maelicke A. 1996. Nicotinic acetylcholine receptors on hippocampal neurons: cell compartment-specific expression and modulatory control of channel activity. Prog Brain Res 109:111-124.
2. Albuquerque EX, Alkondon M, Pereira EF, Castro NG, Schrattenholz A, Barbosa CT, Bonfante-Cabarcas R, Aracava Y, Eisenberg HM, Maelicke A. 1997. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280:1117-1136.
3. Alkondon M, Albuquerque EX. 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.
4. Atluri P, Fleck MW, Shen Q, Mah SJ, Stadfelt D, Barnes W, Goderie SK, Temple S, Schneider AS. 2001. Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 240:143-156.
5. Azam L, Winzer-Serhan UH, Chen Y, Leslie FM. 2002. Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 444:260-274.
6. Berger F, Gage FH, Vijayaraghavan S. 1998. Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871-6881.
7. Boulter J, O'Shea-Greenfield A, Duvoisin RM, Connolly JG, Wada E, Jensen A, Gardner PD, Ballivet M, Deneris ES, McKinnon D, et al. 1990. Alpha 3, alpha 5, and beta 4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a gene cluster. J Biol Chem 265:4472-4482.
8. Britto LR, Rogers SW, Hamassaki-Britto DE, Duvoisin RM. 1994. Nicotinic acetylcholine receptors in the ground squirrel retina: localization of the beta 4 subunit by immunohistochemistry and in situ hybridization. Vis Neurosci 11:569-577.
9. Carlson NG, Gahring LC, Twyman RE, Rogers SW. 1997. Identification of amino acids in the glutamate receptor, GluR3, important for antibody-binding and receptor-specific activation. J Biol Chem 272:11295-11301.
10. Cauley K, Marks M, Gahring LC, Rogers SW. 1996. Nicotinic receptor subunits alpha 3, alpha 4, and beta 2 and high affinity nicotine binding sites are expressed by P19 embryonal cells. J Neurobiol 30:303-314.
11. Chiaia NL, Rhoades RW, Bennett-Clarke CA, Fish SE, Killackey HP. 1991. Thalamic processing of vibrissal information in the rat. I. Afferent input to the medial ventral posterior and posterior nuclei. J Comp Neurol 314:201-216.
12. Chmielowska J, Carvell GE, Simons DJ. 1989. Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285:325-338.
13. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R. 1997. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132:107-124.
14. Curran EJ, Watson SJ, Jr. 1995. Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361:57-76.
15. Dani JA, Ji D, Zhou FM. 2001. Synaptic plasticity and nicotine addiction. Neuron 31:349-352.
16. Dineley-Miller K, Patrick J. 1992. Gene transcripts for the nicotinic acetylcholine receptor subunit, beta4, are distributed in multiple areas of the rat central nervous system. Brain Res Mol Brain Res 16:339-344.
17. Duvoisin RM, Deneris ES, Patrick J, Heinemann S. 1989. The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: beta 4. Neuron 3:487-496.
18. Fix AS, Ross JF, Stitzel SR, Switzer RC. 1996. Integrated evaluation of central nervous system lesions: stains for neurons, astrocytes, and microglia reveal the spatial and temporal features of MK-801-induced neuronal necrosis in the rat cerebral cortex. Toxicol Pathol 24:291-304.
19. Flood P, Krasowski MD. 2000. Intravenous anesthetics differentially modulate ligand-gated ion channels. Anesthesiology 92:1418-1425.
20. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ. 1992. A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41:31-37.
21. Flores CM, DeCamp RM, Kilo S, Rogers SW, Hargreaves KM. 1996. Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of alpha3beta4, a novel subtype in the mammalian nervous system. J Neurosci 16:7892-7901.
22. Francis MM, Vazquez RW, Papke RL, Oswald RE. 2000. Subtype-selective inhibition of neuronal nicotinic acetylcholine receptors by cocaine is determined by the alpha4 and beta4 subunits. Mol Pharmacol 58:109-119.
23. Franklin P, Paxinos G. 1997. The mouse brain. New York: Academic Press.
24. Gahring LC, Carlson NG, Kulmar RA, Rogers SW. 1996. Neuronal expression of tumor necrosis factor alpha in the murine brain. Neuroimmunomodulation 3:289-303.
25. Gahring LC, Carlson NG, Meyer EL, Rogers SW. 2001. Granzyme B proteolysis of a neuronal glutamate receptor generates an autoantigen and is modulated by glycosylation. J Immunol 166:1433-1438.
26. Gahring LC, Persiyanov, Dunn D, Weiss R, Meyer EL, Rogers SW. 2004. Mouse strain-specific nicotinic acetylcholine receptor expression by inhibitory interneurons and astrocytes in the dorsal hippocampus. J Comp Neurol 468:334-346.
27. Harris RM, Hendrickson AE. 1987. Local circuit neurons in the rat ventrobasal thalamus - a GABA immunocytochemical study. Neuroscience 21:229-236.
28. Harvey SC, Maddox FN, Luetje CW. 1996. Multiple determinants of dihydro-beta-erythroidine sensitivity on rat neuronal nicotinic receptor alpha subunits. J Neurochem 67:1953-1959.
29. Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, Zahm DS. 1997. The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 9:354-381.
30. Jacquin MF, Hu JW, Sessle BJ, Renehan WE, Waite PM. 1992. Intraaxonal Neurobiotin injection rapidly stains the long-range projections of identified trigeminal primary afferents in vivo: comparisons with HRP and PHA-L. J Neurosci Methods 45:71-86.
31. Jensen KF, Killackey HP. 1987. Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci 7:3529-3543.
32. Lawand NB, Lu Y, Westlund KN. 1999. Nicotinic cholinergic receptors: potential targets for inflammatory pain relief. Pain 80:291-299.
33. Ledoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. 1987. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123-146.
34. Lindstrom J. 1996. Neuronal nicotinic acetylcholine receptors. Ion Channels 4:377-450.
35. Lukas RJ, Changeux JP, Le Novere N, Albuquerque EX, Balfour DJ, Berg DK, Bertrand D, Chiappinelli VA, Clarke PB, Collins AC, Dani JA, Grady SR, Kellar KJ, Lindstrom JM, Marks MJ, Quik M, Taylor PW, Wonnacott S. 1999. International Union of Pharmacology. XX. Current status of the nomenclature for nicotinic acetylcholine receptors and their subunits. Pharmacol Rev 51:397-401.
36. Marks MJ, Campbell SM, Romm E, Collins AC. 1991. Genotype influences the development of tolerance to nicotine in the mouse. J Pharmacol Exp Ther 259:392-402.
37. Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, Collins AC. 1992. Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J Neurosci 12:2765-2784.
38. Marks MJ, Smith KW, Collins AC. 1998. Differential agonist inhibition identifies multiple epibatidine binding sites in mouse brain. J Pharmacol Exp Ther 285:377-386.
39. McGehee DS. 2002. Nicotinic receptors and hippocampal synaptic plasticity... it's all in the timing. Trends Neurosci 25:171-172.
40. Mihailoff GA. 1993. Cerebellar nuclear projections from the basilar pontine nuclei and nucleus reticularis tegmenti pontis as demonstrated with PHA-L tracing in the rat. J Comp Neurol 330:130-146.
41. Mirzoian A, Luetje CW. 2002. Modulation of neuronal nicotinic acetylcholine receptors by mercury. J Pharmacol Exp Ther 302:560-567.
42. Papa M, Diewald L, Carey MP, Esposito FJ, Gironi Carnevale UA, Sadile AG. 2002. A rostro-caudal dissociation in the dorsal and ventral striatum of the juvenile SHR suggests an anterior hypo- and a posterior hyperfunctioning mesocorticolimbic system. Behav Brain Res 130:171-179.
43. Papke RL, Heinemann SF. 1991. The role of the beta 4-subunit in determining the kinetic properties of rat neuronal nicotinic acetylcholine alpha 3-receptors. J Physiol 440:95-112.
44. Parker MJ, Beck A, Luetje CW. 1998. Neuronal nicotinic receptor beta2 and beta4 subunits confer large differences in agonist binding affinity. Mol Pharmacol 54:1132-1139.
45. Parker MJ, Harvey SC, Luetje CW. 2001. Determinants of agonist binding affinity on neuronal nicotinic receptor beta subunits. J Pharmacol Exp Ther 299:385-391.
46. Perry DC, Xiao Y, Nguyen HN, Musachio JL, Davila-Garcia MI, Kellar KJ. 2002. Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J Neurochem 82:468-481.
47. Picciotto MR, Corrigall WA. 2002. Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics. J Neurosci 22:3338-3341.
48. Picciotto MR, Caldarone BJ, Brunzell DH, Zachariou V, Stevens TR, King SL. 2001. Neuronal nicotinic acetylcholine receptor subunit knockout mice: physiological and behavioral phenotypes and possible clinical implications. Pharmacol Ther 92:89-108.
49. Picciotto MR, Brunzell DH, Caldarone BJ. 2002. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport 13:1097-1106.
50. Piggott MA, Marshall EF, Thomas N, Lloyd S, Court JA, Jaros E, Costa D, Perry RH, Perry EK. 1999. Dopaminergic activities in the human striatum: rostrocaudal gradients of uptake sites and of D1 and D2 but not of D3 receptor binding or dopamine. Neuroscience 90:433-445.
51. Quik M, Polonskaya Y, McIntosh JM, Kulak JM. 2002. Differential nicotinic receptor expression in monkey basal ganglia: effects of nigrostriatal damage. Neuroscience 112:619-630.
52. Rhoades RW, Fish SE, Chiaia NL, Bennett-Clarke C, Mooney RD. 1989. Organization of the projections from the trigeminal brainstem complex to the superior colliculus in the rat and hamster: anterograde tracing with Phaseolus vulgaris leucoagglutinin and intra-axonal injection. J Comp Neurol 289:641-656.
53. Rogers SW, Mandelzys A, Deneris ES, Cooper E, Heinemann S. 1992. The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J Neurosci 12:4611-4623.
54. Rogers SW, Gahring LC, Collins AC, Marks M. 1998. Age-related changes in neuronal nicotinic acetylcholine receptor subunit alpha4 expression are modified by long-term nicotine administration. J Neurosci 18:4825-4832.
55. Rogers SW, Gregori NZ, Carlson N, Gahring LC, Noble M. 2001. Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33:306-313.
56. Rubinstein M, Phillips TJ, Bunzow JR, Falzone TL, Dziewczapolski G, Zhang G, Fang Y, Larson JL, McDougall JA, Chester JA, Saez C, Pugsley TA, Gershanik O, Low MJ, Grandy DK. 1997. Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and methamphetamine. Cell 90:991-1001.
57. Sudweeks SN, Yakel JL. 2000. Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 527 Pt 3:515-528.
58. Voorn P, Gerfen CR, Groenewegen HJ. 1989. Compartmental organization of the ventral striatum of the rat: immunohistochemical distribution of enkephalin, substance P, dopamine, and calcium-binding protein. J Comp Neurol 289:189-201.
59. Winzer-Serhan UH, Leslie FM. 1997. Codistribution of nicotinic acetylcholine receptor subunit alpha3 and beta4 mRNAs during rat brain development. J Comp Neurol 386:540-554.
60. Yamakura T, Chavez-Noriega LE, Harris RA. 2000. Subunit-dependent inhibition of human neuronal nicotinic acetylcholine receptors and other ligand-gated ion channels by dissociative anesthetics ketamine and dizocilpine. Anesthesiology 92:1144-1153.
61. Zachariou V, Caldarone BJ, Weathers-Lowin A, George TP, Elsworth JD, Roth RH, Changeux JP, Picciotto MR. 2001. Nicotine receptor inactivation decreases sensitivity to cocaine. Neuropsychopharmacology 24:576-589.
62. Zahm DS, Heimer L. 1993. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220-232.
63. Zoli M, Lena C, Picciotto MR, Changeux JP. 1998. Identification of four classes of brain nicotinic receptors using beta2 mutant mice. J Neurosci 18:4461-4472.
64. Zwart R, Vijverberg HP. 1997. Potentiation and inhibition of neuronal nicotinic receptors by atropine: competitive and noncompetitive effects. Mol Pharmacol 52:886-895.
65. Zwart R, Van Kleef RG, Vijverberg HP. 1999. Physostigmine and atropine potentiate and inhibit neuronal alpha 4 beta 4 nicotinic receptors. Ann NY Acad Sci 868:636-639.