Muscarinic receptor-mediated GTP-Eu binding in the hippocampus and prefrontal cortex is correlated with spatial memory impairment in aged rats

Neurobiology of Aging

Volumn 28, Issue 4, 2007, Pages 619-626

  Zhang, Hai Yan ^a   Watson, Mona L ^a   Gallagher, Michela ^b   Nicolle, Michelle M ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

G protein subunit; GTP binding; Hippocampus; Muscarinic M1 acetylcholine receptor; Prefrontal cortex

Indexed keywords

EUROPIUM; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANOSINE TRIPHOSPHATE; MUSCARINIC M1 RECEPTOR;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; HIPPOCAMPUS; LEARNING DISORDER; LONG EVANS RAT; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SIGNAL TRANSDUCTION; SPATIAL MEMORY; WESTERN BLOTTING;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CELL MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; GUANOSINE TRIPHOSPHATE; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY DISORDERS; MUSCARINIC AGONISTS; OXOTREMORINE; PREFRONTAL CORTEX; PROTEIN BINDING; RATS; RATS, LONG-EVANS; RECEPTORS, MUSCARINIC; SPACE PERCEPTION;

EID: 33847093516     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2006.02.016     Document Type: Article

References (42)

1. Araujo D.M., Lapchak P.A., Meaney M.J., Collier B., and Quirion R. Effects of aging on nicotinic and muscarinic autoreceptor function in the rat brain: relationship to presynaptic cholinergic markers and binding sites. J Neurosci 10 9 (1990) 3069-3078
2. Aubert I., Rowe W., Meaney M.J., Gauthier S., and Quirion R. Cholinergic markers in aged cognitively impaired Long-Evans rats. Neuroscience 67 2 (1995) 277-292
3. Ayyagari P.V., Gerber M., Joseph J.A., and Crews F.T. Uncoupling of muscarinic cholinergic phosphoinositide signals in senescent cerebral cortical and hippocampal membranes. Neurochem Int 32 1 (1998) 107-115
4. Bartus R.T. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163 2 (2000) 495-529
5. Bartus R.T., Dean III R.L., Beer B., and Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 217 4558 (1982) 408-414
6. Baxter M.G., Bucci D.J., Sobel T.J., Williams M.J., Gorman L.K., and Gallagher M. Intact spatial learning following lesions of basal forebrain cholinergic neurons. Neuroreport 7 8 (1996) 1417-1420
7. Baxter M.G., and Gallagher M. Intact spatial learning in both young and aged rats following selective removal of hippocampal cholinergic input. Behav Neurosci 110 3 (1996) 460-467
8. Bizon J.L., Helm K.A., Han J.S., Chun H.J., Pucilowska J., Lund P.K., et al. Hypothalamic-pituitary-adrenal axis function and corticosterone receptor expression in behaviourally characterized young and aged Long-Evans rats. Eur J Neurosci 14 10 (2001) 1739-1751
9. Blanc E.M., Kelly J.F., Mark R.J., Waeg G., and Mattson M.P. 4-Hydroxynonenal, an aldehydic product of lipid peroxidation, impairs signal transduction associated with muscarinic acetylcholine and metabotropic glutamate receptors: possible action on Galpha(q/11). J Neurochem 69 (1997) 570-580
10. Chen C.A., and Manning D.R. Regulation of G proteins by covalent modification. Oncogene 20 13 (2001) 1643-1652
11. Chouinard M.L., Gallagher M., Yasuda R.P., Wolfe B.B., and McKinney M. Hippocampal muscarinic receptor function in spatial learning-impaired aged rats. Neurobiol Aging 16 6 (1995) 955-963
12. Crews F.T., Kurian P., and Freund G. Cholinergic and serotonergic stimulation of phosphoinositide hydrolysis is decreased in Alzheimer's disease. Life Sci 25/26 (1994) 1993-2002
13. De Sarno P., and Jope R.S. Phosphoinositide hydrolysis activated by muscarinic or glutamatergic, but not adrenergic, receptors is impaired in ApoE-deficient mice and by hydrogen peroxide and peroxynitrite. Exp Neurol 152 1 (1998) 123-128
14. Fischer W.H., Gage F.H., and Bjorklund A. Degenerative changes in forebrain cholinergic nuclei correlate with cognitive impairments in aged rats. Eur J Neurosci 1 1 (1989) 34-45
15. Gallagher M., Burwell R., and Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107 (1993) 618-626
16. Greenwood A.F., Powers R.E., and Jope R.S. Phosphoinositide hydrolysis, Gaq, phospholipase C, and protein kinase C in post-mortem human brain: effects of post-mortem interval, subject age, and Alzheimer's disease. Neuroscience 69 1 (1995) 125-138
17. Han J.S., Bizon J.L., Chun H.J., Maus C.E., and Gallagher M. Decreased glucocorticoid receptor mRNA and dysfunction of HPA axis in rats after removal of the cholinergic innervation to hippocampus. Eur J Neurosci 16 7 (2002) 1399-1404
18. Jope R.S., Song L., and Powers R.E. Cholinergic activation of phosphoinositide signaling is impaired in Alzheimer's disease brain. Neurobiol Aging 18 1 (1997) 111-120
19. Joseph J.A., Culter R., and Roth G.S. Changes in G protein-mediated signal transduction in aging and Alzheimer's disease. Ann NY Acad Sci 695 (1993) 42-45
20. Joseph J.A., Erat S., Denisova N., and Villalobos-Molina R. Receptor- and age-selective effects of dopamine oxidation on receptor-G protein interactions in the striatum. Free Radic Biol Med 24 5 (1998) 827
21. Joseph J.A., Fisher D.R., and Strain J. Muscarinic receptor subtype determines vulnerability to oxidative stress in COS-7 cells. Free Radic Biol Med 32 2 (2002) 153-161
22. Joseph J.A., Villalobos-Molina R., Denisova N., Erat S., Cutler R., and Strain J. Age differences in sensitivity to H2O2- or NO-induced reductions in K(+)-evoked dopamine release from superfused striatal slices: reversals by PBN or Trolox. Free Radic Biol Med 20 6 (1996) 821-830
23. Ladner C.J., and Lee J.M. Pharmacological drug treatment of Alzheimer disease: the cholinergic hypothesis revisited. J Neuropathol Exp Neurol 57 8 (1998) 719-731
24. Levey A.I., Kitt C.A., Simonds W.F., Price D.L., and Brann M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 11 10 (1991) 3218-3226
25. Li X., Song L., and Jope R.S. Cholinergic stimulation of AP-1 and NF kappa B transcription factors is differentially sensitive to oxidative stress in SH-SY5Y neuroblastoma: relationship to phosphoinositide hydrolysis. J Neurosci 16 19 (1996) 5914-5922
26. Li X., Song L., and Jope R.S. Glutathione depletion exacerbates impairment by oxidative stress of phosphoinositide hydrolysis, AP-1, and NF-kappaB activation by cholinergic stimulation. Brain Res Mol Brain Res 53 1/2 (1998) 196-205
27. Mesulam M., Shaw P., Mash D., and Weintraub S. Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann Neurol 55 6 (2004) 815-828
28. Muir J.L. Acetylcholine, aging, and Alzheimer's disease. Pharmacol Biochem Behav 56 4 (1997) 687-696
29. Nicolle M.M., Colombo P.J., Gallagher M., and McKinney M. Metabotropic glutamate receptor-mediated hippocampal phosphoinositide turnover is blunted in spatial learning impaired aged rats. J Neurosci 19 21 (1999) 9604-9610
30. Nicolle M.M., Gallagher M., and McKinney M. Visualization of muscarinic receptor-mediated phosphoinositide turnover in the hippocampus of young and aged, learning impaired Long Evans rats. Hippocampus 11 (2001) 741-746
31. Nicolle M.M., Gonzales J., Sugaya K., Baskerville K., Bryan D., Lund K., et al. Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 107 3 (2001) 415-431
32. Perry E.K., Johnson M., Kerwin J.M., Piggott M.A., Court J.A., Shaw P.J., et al. Convergent cholinergic activities in aging and Alzheimer's disease. Neurobiol Aging 13 3 (1992) 393-400
33. Petersen R.C., Thomas R.G., Grundman M., Bennett D., Doody R., Ferris S., et al. Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med 352 23 (2005) 2379-2388
34. Potter P.E., Gaughan C., and Assouline Y. Lesion of septal-hippocampal neurons with 192 IgG-saporin alters function of M1 muscarinic receptors. Neuropharmacology 38 4 (1999) 579-586
35. Rossi M.A., Mash D.C., and deToledo-Morrell L. Spatial memory in aged rats is related to PKCgamma-dependent G-protein coupling of the M1 receptor. Neurobiol Aging 26 1 (2005) 53-68
36. Roth G.S., Joseph J.A., and Mason R.P. Membrane alterations as causes of impaired signal transduction in Alzheimer's disease and aging. Trends Neurosci 18 5 (1995) 203-206
37. Smith T.D., Gallagher M., and Leslie F.M. Cholinergic binding sites in rat brain: analysis by age and cognitive status. Neurobiol Aging 16 2 (1995) 161-173
38. Stevens P.A., Pediani J., Carrillo J.J., and Milligan G. Coordinated agonist regulation of receptor and G protein palmitoylation and functional rescue of palmitoylation-deficient mutants of the G protein G11alpha following fusion to the alpha 1b-adrenoreceptor. Palmitoylation of G11alpha is not required for interaction with beta*gamma complex. J Biol Chem 276 38 (2001) 35883-35890
39. Tayebati S.K., Amenta F., El-Assouad D., and Zaccheo D. Muscarinic cholinergic receptor subtypes in the hippocampus of aged rats. Mech Ageing Develop 123 5 (2002) 521-528
40. Tsang S.W.Y., Lai M.K.P., Kirvell S., Francis P.T., Esiri M.M., Hope T., et al. Impaired coupling of muscarinic M1 receptors to G-proteins in the neocortex is associated with severity of dementia in Alzheimer's disease. Neurobiol Aging 27 (2006) 1216-1223
41. van der Zee E.A., and Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog Neurobiol 58 5 (1999) 409-471
42. Yamagami K., Joseph J.A., and Roth G.S. Decrement of muscarinic receptor-stimulated low-KMGTPase in striatum and hippocampus from the aged rat. Brain Res 576 (1992) 327-331