Neurobiology of Aging
Volume 26, Issue 7 , Pages 1061-1072 , July 2005

Aging and subcellular localization of m2 muscarinic autoreceptor in basalocortical neurons in vivo

  • Marion Décossas

      Affiliations

    • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5541, Laboratoire d’Histologie-Embryologie, Université Victor Ségalen-Bordeaux 2, 146 rue Léo-Saignat, 33076 Bordeaux Cedex, France
    • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5162, Laboratoire de Génomique Fonctionnelle des Trypanosomatides, ATIPE Interaction Mitochondrie-Cytosquelette chez les Trypanosomes, Université Victor Ségalen-Bordeaux 2, 146 rue Léo-Saignat, 33076 Bordeaux Cedex, France
  • ,
  • Évelyne Doudnikoff

      Affiliations

    • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5541, Laboratoire d’Histologie-Embryologie, Université Victor Ségalen-Bordeaux 2, 146 rue Léo-Saignat, 33076 Bordeaux Cedex, France
  • ,
  • Bertrand Bloch

      Affiliations

    • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5541, Laboratoire d’Histologie-Embryologie, Université Victor Ségalen-Bordeaux 2, 146 rue Léo-Saignat, 33076 Bordeaux Cedex, France
  • ,
  • Véronique Bernard

      Affiliations

    • Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5541, Laboratoire d’Histologie-Embryologie, Université Victor Ségalen-Bordeaux 2, 146 rue Léo-Saignat, 33076 Bordeaux Cedex, France
    • Biologie de la Synapse Cholinergique, Université René Descartes—Paris 5, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France
    • Corresponding Author InformationCorresponding author. Tel.: +33 1 42 86 20 68; fax: +33 1 42 86 33 99.

Received 12 March 2004 ,Revised 7 September 2004 ,Accepted 24 September 2004.

References 

  1. Araujo DM, et al. Effects of aging on nicotinic and muscarinic autoreceptor function in the rat brain: relationship to presynaptic cholinergic markers and binding sites. J Neurosci. 1990;10(9):3069–3078
  2. Bartus RT. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol. 2000;163(2):495–529
  3. Bernard V, et al. Subcellular redistribution of m2 muscarinic acetylcholine receptors in striatal interneurons in vivo after acute cholinergic stimulation. J Neurosci. 1998;18(23):10207–10218
  4. Bernard V, Levey AI, Bloch B. Regulation of the subcellular distribution of m4 muscarinic acetylcholine receptors in striatal neurons in vivo by the cholinergic environment: evidence for regulation of cell surface receptors by endogenous and exogenous stimulation. J Neurosci. 1999;19(23):10237–10249
  5. Biegon A, et al. Aging and brain cholinergic muscarinic receptor subtypes: an autoradiographic study in the rat. Neurobiol Aging. 1989;10(4):305–310
  6. Birthelmer A, et al. Presynaptic regulation of neurotransmitter release in the cortex of aged rats with differential memory impairments. Pharmacol Biochem Behav. 2003;75(1):147–162
  7. Chen LW, et al. Cholinergic neurons expressing substance P receptor (NK(1)) in the basal forebrain of the rat: a double immunocytochemical study. Brain Res. 2001;904(1):161–166
  8. Conner JM, et al. Nontropic actions of neurotrophins: subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation. Proc Natl Acad Sci USA. 2001;98(4):1941–1946
  9. Dai J, et al. Impaired axonal transport of cortical neurons in Alzheimer's disease is associated with neuropathological changes. Brain Res. 2002;948(1–2):138–144
  10. De Lacalle S, et al. Reduced retrograde labelling with fluorescent tracer accompanies neuronal atrophy of basal forebrain cholinergic neurons in aged rats. Neuroscience. 1996;75(1):19–27
  11. de Lacalle S, Iraizoz I, Ma Gonzalo L. Differential changes in cell size and number in topographic subdivisions of human basal nucleus in normal aging. Neuroscience. 1991;43(2/3):445–456
  12. Decossas M, Bloch B, Bernard V. Trafficking of the muscarinic m2 autoreceptor in cholinergic basalocortical neurons in vivo: differential regulation of plasma membrane receptor availability and intraneuronal localization in acetylcholinesterase-deficient and -inhibited mice. J Comp Neurol. 2003;462(3):302–314
  13. Dunbar GL, et al. Hippocampal choline acetyltransferase activity correlates with spatial learning in aged rats. Brain Res. 1993;604(1–2):266–272
  14. Dunnett S. Cholinergic grafts, memory and ageing. Trends Neurosci. 1991;14(8):371–376
  15. Elrod K, Buccafusco JJ. Correlation of the amnestic effects of nicotinic antagonists with inhibition of regional brain acetylcholine synthesis in rats. J Pharmacol Exp Ther. 1991;258(2):403–409
  16. Eva C, et al. Nerve growth factor modulates the expression of muscarinic cholinergic receptor messenger RNA in telencephalic neuronal cultures from newborn rat brain. Brain Res Mol Brain Res. 1992;14(4):344–351
  17. Finch CE. Neuron atrophy during aging: programmed or sporadic?. Trends Neurosci. 1993;16(3):104–110
  18. Francis PT, et al. The cholinergic hypothesis of Alzheimer's disease: a review of progress. J Neurol Neurosurg Psychiatr. 1999;66(2):137–147
  19. Gallagher M, Colombo PJ. Ageing: the cholinergic hypothesis of cognitive decline. Curr Opin Neurobiol. 1995;5(2):161–168
  20. Jagoda EM, Shimoji K, Ravasi L, Yamada M, Gomeza J, Wess J, et al. Regional brain uptake of the muscarinic ligand, [18F]FP-TZTP, is greatly decreased in M2 receptor knockout mice but not in M1, M3 and M4 receptor knockout mice. Neuropharmacology. 2003;44(5):653–661
  21. Lebrun C, et al. A comparison of the working memory performances of young and aged mice combined with parallel measures of testing and drug-induced activations of septo-hippocampal and nbm-cortical cholinergic neurones. Neurobiol Aging. 1990;11(5):515–521
  22. Levey AI, et al. Light and electron microscopic study of m2 muscarinic acetylcholine receptor in the basal forebrain of the rat. J Comp Neurol. 1995;351(3):339–356
  23. Levey AI, et al. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci. 1991;11(10):3218–3226
  24. Ludlam WH, et al. mRNAs encoding muscarinic and substance P receptors in cultured sympathetic neurons are differentially regulated by LIF or CNTF. Dev Biol. 1994;164(2):528–539
  25. Luine V, Hearns M. Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res. 1990;523(2):321–324
  26. Mesulam MM. Some cholinergic themes related to Alzheimer's disease: synaptology of the nucleus basalis, location of m2 receptors, interactions with amyloid metabolism, and perturbations of cortical plasticity. J Physiol (Paris). 1998;92(3–4):293–298
  27. Moore H, et al. Potassium, but not atropine-stimulated cortical acetylcholine efflux, is reduced in aged rats. Neurobiol Aging. 1996;17(4):565–571
  28. Mufson EJ, et al. Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol. 1999;57(4):451–484
  29. Narang N. In situ determination of M1 and M2 muscarinic receptor binding sites and mRNAs in young and old rat brains. Mech Ageing Dev. 1995;78(3):221–239
  30. Newhouse PA, et al. Age-related effects of the nicotinic antagonist mecamylamine on cognition and behavior. Neuropsychopharmacology. 1994;10(2):93–107
  31. Nilsson OG, Gage FH. Anticholinergic sensitivity in the aging rat septohippocampal system as assessed in a spatial memory task. Neurobiol Aging. 1993;14(5):487–497
  32. Nordberg A, Alafuzoff I, Winblad B. Nicotinic and muscarinic subtypes in the human brain: changes with aging and dementia. J Neurosci Res. 1992;31(1):103–111
  33. Perry EK, et al. Alteration in nicotine binding sites in Parkinson's disease. Lewy body dementia and Alzheimer's disease: possible index of early neuropathology. Neuroscience. 1995;64(2):385–395
  34. Podruchny TA, et al. In vivo muscarinic 2 receptor imaging in cognitively normal young and older volunteers. Synapse. 2003;48(1):39–44
  35. Quirion R, et al. Facilitation of acetylcholine release and cognitive performance by an M(2)-muscarinic receptor antagonist in aged memory-impaired. J Neurosci. 1995;15(2):1455–1462
  36. Reenstra WR, Yaar M, Gilchrest BA. Aging affects epidermal growth factor receptor phosphorylation and traffic kinetics. Exp Cell Res. 1996;227(2):252–255
  37. Rouse ST, Thomas TM, Levey AI. Muscarinic acetylcholine receptor subtype, m2: diverse functional implications of differential synaptic localization. Life Sci. 1997;60(13/14):1031–1038
  38. Rye DB, et al. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience. 1984;13(3):627–643
  39. Semba K, Fibiger HC. Organization of central cholinergic systems. Prog Brain Res. 1989;79:37–63
  40. Shigemoto R, et al. Immunocytochemical localization of rat substance P receptor in the striatum. Neurosci Lett. 1993;153(2):157–160
  41. Smith ML, Booze RM, Cholinergic and GABAergic neurons in the nucleus basalis region of young and aged rats . Neuroscience. 1995;67(3):679–688
  42. Smith TD, Gallagher M, Leslie FM. Cholinergic binding sites in rat brain: analysis by age and cognitive status. Neurobiol Aging. 1995;16(2):161–173
  43. Stemmelin J, et al. Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience. 2000;96(2):275–289
  44. Terry AV, Buccafusco JJ. The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther. 2003;306(3):821–827
  45. Terry AV, Buccafusco JJ, Jackson WJ. Scopolamine reversal of nicotine enhanced delayed matching-to-sample performance in monkeys. Pharmacol Biochem Behav. 1993;45(4):925–929
  46. Turrini P, et al. Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy. Neuroscience. 2001;105(2):277–285
  47. Vilaro MT, Palacios JM, Mengod G. Multiplicity of muscarinic autoreceptor subtypes? Comparison of the distribution of cholinergic cells and cells containing mRNA for five subtypes of muscarinic receptors in the rat brain. Brain Res Mol Brain Res. 1994;21(1–2):30–46
  48. Vilaro MT, et al. Muscarinic M2 receptor mRNA expression and receptor binding in cholinergic and non-cholinergic cells in the rat brain: a correlative study using in situ hybridization histochemistry and receptor autoradiography. Neuroscience. 1992;47(2):367–393
  49. Vitiello B, et al. Cognitive and behavioral effects of cholinergic, dopaminergic, and serotonergic blockade in humans. Neuropsychopharmacology. 1997;16(1):15–24
  50. Zhang W, et al. Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J Neurosci. 2002;22(5):1709–1717

PII: S0197-4580(04)00308-2

doi: 10.1016/j.neurobiolaging.2004.09.007

Neurobiology of Aging
Volume 26, Issue 7 , Pages 1061-1072 , July 2005