Expression of nicotinic acetylcholine receptor subunits in the cerebral cortex in Alzheimer's disease: Histotopographical correlation with amyloid plaques and hyperphosphorylated-tau protein

European Journal of Neuroscience

Volumn 11, Issue 7, 1999, Pages 2551-2565

  Wevers, A ^a   Monteggia, L ^a   Nowacki, S ^a   Bloch, W ^a   Schutz, U ^a   Lindstrom, J ^a   Pereira, E F R ^a   Eisenberg, H ^a   Giacobini, E ^a   De Vos, R A I ^a   Steur, E N H J ^a   Maelicke, A ^a   Albuquerque, E X ^a   Schroder, H ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cholinergic transmission; Human brain; 4 subunit; 7 subunit; amyloid

Indexed keywords

AMYLOID BETA PROTEIN; MESSENGER RNA; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; CHOLINERGIC TRANSMISSION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEUROPATHOLOGY; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0032971370     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00676.x     Document Type: Article

References (65)

1. Albuquerque, E.X., Alkondon, M., Pereira, E.F.R., Castro, N.G., Schrattenholz, A., Barbosa, C.T.F., Bonfante‐Cabarcas, R., Aracava, Y., Eisenberg, H.M., Maelicke, A. 1997 Properties of neuronal nicotinic acetylcholine receptors: Pharmacological characterization and modulation of synaptic function. J. Pharmacol. Exp. Ther., 280, 1 20.
2. Alkondon, M. & 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, 455 1473.
3. Del Alonso, A.C., Grundke‐Iqbal, I., Iqbal, K. 1996 Alzheimer’s disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nature Med., 2, 783 787.
4. Araujo, D.M., Lapchak, P.A., Robitaille, Y., Gauthier, S., Quirion, R. 1988 Differential alteration of various cholinergic markers in cortical and subcortical regions of human brain in Alzheimer’s disease. J. Neurochem., 50, 1914–23.
5. Arriagada, P.V., Growdon, J.H., Hedley‐Whyte, E.T., Hyman, B.T. 1992 Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer’s disease. Neurology, 42, 631 639.
6. Barbosa, C.T.F., Alkondon, M., Aracava, Y., Maelicke, A., Albuquerque, E.X. 1996 Ligand‐gated ion channels in acutely dissociated rat hippocampal neurons with long dendrites. Neurosci. Lett., 210, 177 180.
7. Bartus, R.T., Dean, R.L. III, Beer, B., Lippa, A.S. 1982 The cholinergic hypothesis of geriatric memory dysfunction. Science, 217, 408 417.
8. Beyreuther, K., Pollwein, P., Multhaup, G., Mönning, U., König, G., Dyrks, T., Schubert, W., Masters, C.L. 1993 Regulation and expression of the Alzheimer’s β/A4 amyloid protein precursor in health, disease, and Down’s syndrome. Ann. NY Acad. Sci., 695, 91 102.
9. Biernat, J., Mandelkow, E.‐M., Schröter, C., Lichtenberg‐Kraag, B., Steiner, B., Berling, B., Meyer, H., Mercken, M., Vandermeeren, A., Goedert, M., Mandelkow, E. 1992 The switch of tau protein to an Alzheimer‐like state includes the phosphorylation of two serine‐proline motifs upstream of the microtubule binding region. EMBO J., 11, 1593 1597.
10. Birtsch, C., Wevers, A., Traber, J., Maelicke, A., Bloch, W., Schröder, H. 1997 Expression of α4–1 and α5 nicotinic cholinoceptor mRNA in the aging rat cerebral cortex. Neurobiol. Aging, 18, 335 342.
11. Bowen, D.M., Francis, P.T., Chessell, I.P., Webster, S. 1994 Neurotransmission – the missing link integrating Alzheimer research? Trends Neurosci., 17, 149 150.
12. Cartaud, J. & Changeux, J.P. 1993 Post‐transcriptional compartmentalization of acetylcholine receptor biosynthesis in the subneural domain of muscle and electrocyte junctions. Eur. J. Neurosci., 5, 191 202.
13. Chavez‐Noriega, L.E., Crona, J.H., Washburn, M.S., Urrutia, A., Elliott, K.J., Johnson, E.C. 1997 Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4, and hα7 expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther., 280, 346 356.
14. Davies, P. & Feisullin, S. 1981 Postmortem stability of α‐bungarotoxin binding sites in mouse and human brain. Brain Res., 216, 449 454.
15. Deneris, E.S., Boulter, J., Connolly, J., Wada, E., Wada, K., Goldman, D., Swanson, L.W., Patrick, J., Heinemann, S. 1989 Genes encoding neuronal nicotinic acetylcholine receptors. Clin. Chem., 35, 731 737.
16. Doucette‐Stamm, L., Monteggia, L.M., Donnelly‐Roberts, D., Wang, M.T., Lee, J., Tian, J., Giordano, T. 1994 Cloning and sequence of the human α7 nicotinic acetylcholine receptor. Drug Dev. Res., 30, 252 256.
17. Einstein, G., Buranosky, R., Crain, B.J. 1994 Dendritic pathology of granule cells in Alzheimer’s disease is unrelated to neuritic plaques. J. Neurosci., 14, 5077 5088.
18. Elliott, K.J., Ellis, S.B., Berckhan, K.J., Urrutia, A., Chavez‐Noriega, L.E., Johnson, E.C., Velicelebi, G., Harpold, M.M. 1996 Comparative structure of human neuronal α2‐α7 and β2‐β4 nicotinic acetylcholine receptor subunits and functional expression of the α2 α3 α4 α7 β2, and β4 subunits. J. Mol. Neurosci., 7, 217 228.
19. Fibiger, H.C. 1991 Cholinergic mechanism in learning, memory and dementia: review of recent evidence. Trends Neurosci., 14, 220 223.
20. Flores, C.M., Rogers, S.W., Pabreza, L.A., Wolfe, B.B., 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.
21. Flynn, D. & Mash, D.C. 1986 Characterization of [3H]‐ l ‐nicotine binding in human cerebral cortex: comparison between Alzheimer’s disease and the normal. J. Neurochem., 47, 1948–54.
22. Geula, C. & Mesulam, M.‐M. 1989 Cortical cholinergic fibers in aging and Alzheimer’s disease: a morphometric study. Neuroscience, 33, 469 481.
23. Giacobini, E., DeSarno, P., Clark, B., McIlhany, M. 1989 The cholinergic receptor system of the human brain: neurochemical and pharmacological aspects in aging and Alzheimer. In: Nordberg, A., Fuxe, K., Holmstedt, B. & Sundwall, A, eds. Progress in Brain Research 79. Elsevier, Amsterdam, pp. 335 343.
24. Goate, A., Chartier‐Harlin, M.C., Mullan, M., Brown, J., Crawford, F., Fidani, L., Giuffra, L., Haynes, A., Irving, N., James, L. 1991 Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature, 349, 704 706.
25. Goedert, M. 1993 Tau protein and the neurofibrillary pathology of Alzheimer’s disease. Trends Neurosci., 16, 460 465.
26. Gopalakrishnan, M., Monteggia, L.M., Anderson, D.J., Molinari, E.J., Piattoni‐Kaplan, M., Donnelly‐Roberts, D., Arneric, S.P., Sullivan, J.P. 1996 Stable expression, pharmacologic properties and regulation of the human neuronal nicotinic acetylcholine α4β2 receptor. J. Pharmacol. Exp. Ther., 276, 289 297.
27. Gotti, C., Fornasari, D., Clementi, F. 1997 Human neuronal nicotinic receptors. Prog. Neurobiol., 53, 199 237.
28. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981 Improved patch‐clamp techniques for high resolution current recording from cells and cell‐free membrane patches. Pflügers Arch., 391, 85 100.
29. Hardy, J. 1997 Amyloid, the presenilins and Alzheimer’s disease. Trends Neurosci., 20, 154 159.
30. Jones, G.M.M., Sahakian, B.J., Levy, R., Warburton, D.M., Gray, J.A. 1992 Effects of acute subcutaneous nicotine on attention, information processing and short‐term memory in Alzheimer’s disease. Psychopharmacology, 108, 485 494.
31. Kuhar, J.M., De Souza, E.B., Unnerstall, J.R. 1986 Neurotransmitter receptor mapping by autoradiography and other methods. Annu. Rev. Neurosci., 9, 27 59.
32. Lang, W. & Henke, H. 1983 Cholinergic receptor binding and autoradiography in brains of non‐neurological and senile dementia of Alzheimer type patients. Brain Res., 267, 271 280.
33. Levy‐Lahad, E., Wijsman, E.M., Nemens, E., Anderson, L., Goddard, K.A.B., Weber, J.L., Bird, T.D., Schellenberg, G.D. 1995 A familial Alzheimer’s disease locus on chromosome I. Science, 269, 970 977.
34. Mandelkow, E.‐M. & Mandelkow, E. 1993 Tau as a marker for Alzheimer’s disease. Trends Biochem. Sci., 18, 480 483.
35. McLane, K., Wu, X., Lindstrom, J., Conti‐Tronconi, B. 1992 Epitope mapping of polyclonal and monoclonal antibodies against two alpha bungarotoxin‐binding subunits from neuronal nicotinic receptors. J. Neuroimmunol., 38, 115 128.
36. Monteggia, L.M., Gopalakrishnan, M., Touma, E., Idler, K.B., Nash, N., Arneric, S.P., Sullivan, J.P., Giordano, T. 1995 Cloning and transient expression of genes encoding the human α4 and β2 neuronal nicotinic acetylcholine receptor (nAChR) subunits. Gene, 155, 189 193.
37. Neve, R.L. & Robakis, N.K. 1998 Alzheimer’s disease: a re‐examination of the amyloid hypothesis. Trends Neurosci., 21, 15 19.
38. Newhouse, P.A., Potter, A., Corwin, J., Lenox, R. 1992 Acute nicotinic blockade produces cognitive impairment in normal humans. Psychopharmacology, 108, 480 484.
39. Newhouse, P.A., Sunderland, T., Narang, P.K., Mellow, A.M., Fertig, J.B., Lawlor, B.A., Murphy, D.L. 1991 Neuroendocrine, physiologic and behavioral responses following intravenous nicotine in non‐smoking healthy volunteers and in patients with Alzheimer’s disease. Psychoneuroendocrinology, 15, 471 484.
40. Newhouse, P.A., Sunderland, T., Tariot, P.N., Blumhardt, C.L., Weingartner, H., Mellow, A., Murphy, D.L. 1988 Intravenous nicotine in Alzheimer’s disease: a pilot study. Psychopharmacology, 95, 171 175.
41. Nordberg, A., Alafuzoff, I., Winblad, B. 1992 Nicotinic and muscarinic subtypes in the human brain: changes with aging and dementia. J. Neurosci. Res., 31, 103 111.
42. Nordberg, A. & Winblad, B. 1986 Reduced number of [3H]nicotine and [3H]acetylcholine binding sites in the frontal cortex of Alzheimer brains. Neurosci. Lett., 72, 115 119.
43. Peng, X., Anand, R., Whiting, P., Lindstrom, J. 1994a Nicotine‐induced upregulation of neuronal nicotinic receptors results from a disease in the rate of turnover. Mol. Pharmacol., 46, 523 530.
44. Peng, X., Katz, M., Gerzanich, V., Anand, R., Lindstrom, J. 1994b Human α7 acetylcholine receptor: cloning of the α7 subunit from the SH‐SY5Y cell line and determination of pharmacological properties of native receptors and functional α7 homomers expressed in Xenopus oocytes. Mol. Pharmacol., 45, 546 554.
45. Rinne, J.O., Myllykylä, T., Lönnberg, P., Marjamaki, P. 1991 A postmortem study of brain nicotinic receptors in Parkinson’s and Alzheimer’s disease. Brain Res., 547, 167 170.
46. Rinne, J.O., Säkö, E., Paljärvi, L., Mölsä, P.K., Rinne, U.K. 1988 A comparison of brain choline acetyltransferase activity in Alzheimer’s disease multi‐infarct dementia and combined dementia. J. Neural. Transm., 73, 121 128.
47. Role, L.W. 1992 Diversity in primary structure and function of neuronal nicotinic acetylcholine receptor channels. Curr. Opin. Neurobiol., 2, 254 262.
48. Rubboli, F., Court, J.A., Sala, C., Morris, C., Chini, B., Perry, E., Clementi, F. 1994 Distribution of nicotinic receptors in the human hippocampus and thalamus. Eur. J. Neurosci., 6, 1596 1604.
49. Schröder, H., Giacobini, E., Struble, R.G., Zilles, K., Maelicke, A. 1991 Nicotinic cholinoceptive neurons of the frontal cortex are reduced in Alzheimer’s disease. Neurobiol. Aging, 12, 259 262.
50. Schröder, H. & Wevers, A. 1998 Nicotinic acetylcholine receptors in Alzheimer’s disease. Alzheimer’s Dis. Rev., 3, 21 27.
51. Schröder, H., Zilles, K., Luiten, P.G.M., Strosberg, A.D., Aghchi, A. 1989a Human cortical neurons contain both nicotinic and muscarinic acetylcholine receptors: an immunocytochemical double‐labeling study. Synapse, 4, 319 326.
52. Schröder, H., Zilles, K., Maelicke, A., Hajós, F. 1989b Immunohisto‐ and cytochemical localization of cortical nicotinic cholinoceptors in rat and man. Brain Res., 502, 287 295.
53. Séguela, P., Wadiche, J., Dineley‐Miller, K., Dani, J.A., Patrick, J.W. 1993 Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci., 13, 596 604.
54. Sherrington, R., Rogaev, E.I., Liang, Y., Rogaeva, E.A., Levesque, G., Ikeda, M., Chi, H., Lin, C., Li, G., Holman, K., Tsuda, T., Mar, L., Foncin, J.‐F., Bruni, A.C., Montesi, M.P., Sorbi, S., Rainero, I., Pinessi, L., Nee, L., Chumakov, I., Pollen, D., Brookes, A., Sanseau, P., Polinsky, R.J., Wasco, W., Da Silva, H.A.R., Haines, J.L., Pericak‐Vance, M.A., Tanzi, R.E., Roses, A.D., Fraser, P.E., Rommens, J.M., StGeorge‐Hyslop, P.H. 1995 Cloning of a gene bearing missense mutations in early‐onset familial Alzheimer’s disease. Nature, 375, 754 760.
55. Strittmatter, W.J., Saunders, A.M., Schmechel, D., Pericak‐Vance, M., Enghild, J., Salvesen, G.S., Roses, A.D. 1993 Apolipoprotein E: high‐avidity binding to β‐amyloid and increased frequency of type 4 allele in late‐onset familial Alzheimer disease. Proc. Natl Acad. Sci. USA, 90, 1977–81.
56. Sugaya, K., Giacobini, E., Chiappinelli, V.A. 1990 Nicotinic acetylcholine receptor subtypes in human frontal cortex: changes in Alzheimer’s disease. J. Neurosci. Res., 27, 349 359.
57. Terry, R., Masliah, E., Salmon, D., Butters, N., DeTeresa, R., Hill, R., Hansen, L., Katzman, R. 1991 Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol., 30, 572 580.
58. Wevers, A., Jeske, A., Lobron, C., Birtsch, C.,. Heinemann, S., Maelicke, A., Schröder, R., Schröder, H. 1994 Cellular distribution of nicotinic acetylcholine receptor subunit mRNAs in the human cerebral cortex as revealed by non‐isotopic in situ hybridization. Mol. Brain Res., 25, 122 128.
59. Wevers, A., Sullivan, J.P., Giordano, T., Birtsch, C., Monteggia, L.M., Nowacki, S., Arneric, S., Schröder, H. 1995 Cellular distribution of the mRNA for the α7 subunit of the nicotinic acetylcholine receptor in the human cerebral cortex. Drug Dev. Res., 36, 103 110.
60. Whitehouse, P.J. & Kalaria, R.N. 1995 Nicotinic receptors and neurodegenerative dementing diseases: basic research and clinical implications. Alzheimer Dis. Assoc. Disord., 9 (Suppl. 2), 3 5.
61. Whitehouse, P.J., Martino, A.M., Antuono, P.G., Lowenstein, P.R., Coyle, J.T., Price, D.L., Kellar, K.J. 1986 Nicotinic acetylcholine binding sites in Alzheimer’s disease. Brain Res., 371, 146 151.
62. Whitehouse, P.J., Martino, A.M., Marcus, K.A., Zweig, R.M., Singer, H.S., Price, D.L., Kellar, K.J. 1988a Reductions in acetylcholine and nicotine binding in several degenerative diseases. Arch. Neurol., 45, 722 724.
63. Whitehouse, P.J., Martino, A.M., Wagster, M.V., Price, D.L., Mayeux, R., Atack, J.R., Kellar, K.J. 1988b Reductions in [ 3 H]nicotinic acetylcholine binding in Alzheimer’s disease and Parkinson’s disease: an autoradiographic study. Neurology, 38, 720 723.
64. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T. 1982 Alzheimer’s disease and senile dementia: a loss of neurons in the basal forebrain. Science, 215, 1237 1239.
65. Whiting, P.J. & Lindstrom, J.M. 1988 Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. J. Neurosci., 8, 3395 3404.