Acetylcholine-secreting cells improve age-induced memory deficits

Molecular Therapy

Volumn 8, Issue 1, 2003, Pages 51-61

  Dickinson Anson, Heather ^a,b   Winkler, Jürgen ^c,d   Fisher, Lisa J ^a   Song, Hong Jun ^a   Poo, Mu Ming ^e   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Aging; Basal forebrain; Choline acetyltransferase; Engineered cells; Hippocampus; Learning; Medial septum; Memory; Neocortex; Nucleus basalis; Water maze

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE;

AGED; AGING; AMNESIA; ANIMAL CELL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL TRANSPLANTATION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; FOREBRAIN; GENE EXPRESSION; GENETIC ENGINEERING; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MALE; MAZE TEST; NONHUMAN; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPATIAL MEMORY; TRANSGENE;

ANIMALIA;

EID: 0043201413     PISSN: 15250016     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1525-0016(03)00145-X     Document Type: Article

References (41)

1. Bartus, R. T., Dean, R. L., Beer, B., and Lippa, A. S. (1982). The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-417.
2. Collerton, D. (1986). Cholinergic function and intellectual decline in Alzheimer's Disease. Neuroscience 19: 1-28.
3. Emre, M., Heckers, S., Mash, D. C., Geula, C., and Mesulam, M. M. (1993). Cholinergic innervation by the amygdaloid complex in the human brain and its alterations in old age and Alzheimer's disease. J. Comp. Neurol. 336: 117-134.
4. Cummings, J. L., and Kaufer, D. (1996). Neuropsychiatric aspects of Alzheimer's disease: the cholinergic hypothesis revisited. Neurology 47: 876-883.
5. Lehericy, S., et al. (1993). Heterogeneity and selectivity of the degeneration of cholinergic neurons in the basal forebrain of patients with Alzheimer's disease. J. Comp. Neurol. 330: 15-31.
6. Davis, K. L., et al. (1999). Cholinergic markers in elderly patients with early signs of Alzheimer's disease. JAMA 281: 1401-1434.
7. Geula, C., and Mesulam, M.-M. (1999). Cholinergic systems in Alzheimer disease. In Alzheimer Disease, pp. 269-292. Lippincott Williams & Wilkins, Philadelphia.
8. Mandel, R. J., Gage, F. H., and Thal, L. J. (1989). Spatial learning in rats: correlation with cortical choline acetyltransferase and improvement with NGF following NBM damage. Exp. Neurol. 104: 208-217.
9. Luine, V., and Hearns, M (1990). Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res. 523: 321-324.
10. Dunbar, G. L., Rylett, R. J., Schmidt, B. M., Sinclair, R. C., and Williams, L. R. (1993). Hippocampal choline acetyltransferase activity correlates with spatial learning in aged rats. Brain Res. 604: 266-272.
11. Smith, D. E., Roberts, J., Gage, F. H., and Tuszynski, M. H. (1999). Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy. Proc. Natl. Acad. Sci. USA 96: 10893-10898.
12. Koh, S., and Loy, R. (1988). Age-related loss of nerve growth factor sensitivity in rat basal forebrain neurons. Brain Res. 440: 396-401.
13. Fischer, W., Björklund, A., Chen, K., and Gage, F. H. (1991). NGF improves spatial memory in aged rats as a function of age. J. Neurosci. 11: 1889-1906.
14. Thal, L. (1999). Clinical trials in Alzheimer's disease. In Alzheimer's Disease, 2nd ed., pp. 423-439. Lippincott Williams & Wilkins, Philadelphia.
15. Fischer, W., Wictorin, K., Björklund, A., Williams, L. R., Varon, S., and Gage, F. H. (1987). Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329: 65-68.
16. Markowska, A. L., Koliatsos, V. E., Breckler, S. J., Price, D. L., and Olton, D. S. (1994). Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 14: 4815-4824.
17. Markowska, A. L., Price, D., and Koliatsos, V. E. (1995). Selective effects of nerve growth factor on spatial recent memory as assessed by a delayed nonmatching-to-position task in the water maze. J. Neurosci. 16: 3541-3548.
18. Chen, K. S., and Gage, F. H. (1995). Somatic gene transfer of NGF to the aged brain: behavioral and morphological amelioration. J. Neurosci. 15: 2819-2825.
19. Frick, K. M., Price, D. L., Koliatsos, V. E., and Markowska, A. L. (1997). The effects of nerve growth factor on spatial recent memory in aged rats persist after discontinuation of treatment. J. Neurosci. 17: 2543-2550.
20. Gustilo, M. C., Markowska, A. L., Breckler, S. J., Fleischman, C. A., Price, D. L., and Koliatsos, V. E. (1999). Evidence that nerve growth factor influences recent memory through structural changes in septohippocampal cholinergic neurons. J. Comp. Neurol. 405: 491-507.
21. Gage, F. H., Björklund, A., Stenevi, U., Dunnett, S. B., and Kelly, P. A. (1984). Intrahippocampal septal grafts ameliorate learning impairments in aged rats. Science 225: 533-536.
22. Dunnett, S. B., Toniolo, A., Fine, C. N., Ryan, A., Björklund, A., and Iversen, A. (1985). Transplantation of embryonic ventral forebrain neurons to the neocortex of rats with lesions of nucleus basalis magnocellularis - II. Sensorimotor and learning impairments. Neuroscience 16: 787-797.
23. Clarke, D. I., Gage, F. H., and Björklund, A. (1986). Formation of cholinergic synapses by intrahippocampal septal grafts as revealed by choline acetyltransferase immunohistochemistry. Brain Res 369: 151-162.
24. Gage, F. H., and Björklund, A. (1986). Cholinergic septal grafts into the hippocampal formation improve spatial learning and memory in aged rats by an atropine-sensitive mechanism. J Neurosci. 6: 2837-2847.
25. Nilsson, O. G., Shapiro, M. L., Gage, F. H., Olton, D. S., and Björklund, A. (1987). Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus. Exp. Brain Res. 67: 195-215.
26. Gage, F. H., Kawaja, M. D., and Fisher, L. J. (1991). Genetically modified cells: applications for intracerebral grafting. Trends Neurosci. 14: 328-333.
27. Fisher, L. J. (1995). Engineered cells: a promising therapeutic approach for neural disease. Restor. Neurol. Neurosci. 8: 49-57.
28. Sinden, J. D., Hodges, H., and Gray, J. A. (1995). Neural transplantation and recovery of cognitive function. Behav. Brain Sci. 18: 10-35.
29. Martinez-Serrano, A., Fischer, W., and Björklund, A. (1995). Reversal of age-dependent cognitive impairments and cholinergic neuron atrophy by NGF-secreting neural progenitors grafted to the basal forebrain. Neuron 15: 473-484.
30. Winkler, J., Suhr, S. T., Gage, F. H., Thal, L. J., and Fisher, L. J. (1995). Essential role of neocortical acetylcholine in spatial memory. Nature 375: 484-487.
31. Dickinson-Anson, H., Aubert, I., Gage, F. H., and Fisher, L. J. (1998). Hippocampal grafts of acetylcholine-producing cells are sufficient to improve behavioral performance following a unilateral fimbria-fornix lesion. Neuroscience 84: 771-781.
32. Fisher, L. J., Schinstine, M., Salvaterra, P., Dekker, A. J., Thal, L. J., and Gage, F. H. (1993). In vivo production and release of acetylcholine from primary fibroblasts genetically modified to express choline acetyltransferase. J. Neurochem. 61: 1323-1332.
33. Fonnum, F. (1969). Radiochemical microassays for the determination of choline acetyltransferase and cholinesterase activities. Biochem. J. 115: 465-472.
34. Tucek, S. (1978). Acetylcholine Synthesis in Neurons. Chapman & Hall, London.
35. Tabti, N., Alder, S., and Poo, M.-M. (1998). Culturing spinal neurons and muscle cells from Xenopus embryos. In Culturing Nerve Cells. MIT Press, Cambridge, MA.
36. Song, H.-J., Ming, G.-I., Fon, E., Bellucchio, E., Edwards, R. H., and Poo, M.-M. (1997). Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18: 815-826.
37. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. 4th ed. Academic Press, San Diego.
38. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Poo, M.-M., Dan, Y., Song, H.-J., Morimoto, T., and Popov, S. (1996). Calcium dependent vesicular exocytosis: from constitutive to regulated secretion. Cold Spring Harbor Symp. Quant. Biol. V60: 349-359.
40. Girod, R., Popov, S., Alder, J., Zheng, J. Q., Lohof, A., and Poo, M.-M. (1996). Spontaneous quantal transmitter secretion from myocytes and fibroblasts: comparison with neuronal secretion. J. Neurosci. 15: 2826-2838.
41. Gage, F. H., Björklund, A., Stenevi, U., Dunnett S. B., and Kelly, P. A. T. (1984). Intrahippocampal septal grafts ameliorate learning impairments in aged rats. Science 225: 533-536.