Systemic treatment with GPI 1046 improves spatial memory and reverses cholinergic neuron atrophy in the medial septal nucleus of aged mice

Brain Research

Volumn 842, Issue 1, 1999, Pages 109-118

  Sauer, Hansjörg ^a   Francis, Jonathan M ^a   Jiang, Hong ^a   Hamilton, Gregory S ^a   Steiner, Joseph P ^a  

^a GUILFORD PHARMACEUTICALS INC   (United States)

Author keywords

Aging; GPI 1046; Immunophilin; Morris water maze

Indexed keywords

1 (3,3 DIMETHYL 1,2 DIOXOPENTYL) 2 PYRROLIDINECARBOXYLIC ACID 3 (3 PYRIDYL)PROPYL ESTER; IMMUNOPHILIN; NOOTROPIC AGENT; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ARTICLE; ATROPHY; CHOLINERGIC NERVE; DRUG EFFECT; HIPPOCAMPUS; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECALL; SPATIAL MEMORY; TASK PERFORMANCE;

AGING; ANIMALS; ATROPHY; IMMUNOPHILINS; IMMUNOSUPPRESSIVE AGENTS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; PARASYMPATHETIC NERVOUS SYSTEM; PYRROLIDINES; SEPTAL NUCLEI; TACROLIMUS BINDING PROTEINS; TIME FACTORS;

EID: 0033581334     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01851-X     Document Type: Article

References (64)

1. Ingram D.K. Complex maze learning in rodents as a model of age-related memory impairment. Neurobiol. Aging. 9:1988;475-485.
2. Lowy A.M., Ingram D.K., Olton D.S., Waller S.B., Reynolds M.A., London E.D. Discrimination learning requiring different memory components in rats: age and neurochemical comparisons. Behav. Neurosci. 99:1985;638-651.
3. Barnes C.A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93:1979;74-104.
4. Bartus R.T., Dean R.L., Goas J.A., Lippa A.S. Age-related changes in passive avoidance retention: modulation with dietary choline. Science. 209:1980;301-303.
5. Ingram D.K., London E.D., Goodrick C.L. Age and neurochemical correlates of radial maze performance in rats. Neurobiol. Aging. 2:1981;41-48.
6. Gage F.H., Dunnett S.B., Björklund A. Spatial learning and motor deficits in aged rats. Neurobiol. Aging. 5:1984;43-48.
7. Fischer W., Chen K.S., Gage F.H., Björklund A. Progressive decline in spatial learning and integrity of forebrain cholinergic neurons in rats during aging. Neurobiol. Aging. 13:1991;9-23.
8. Fischer W., Gage F.H., Björklund A. Degenerative changes in forebrain cholinergic nuclei correlate with cognitive impairments in aged rats. Eur. J. Neurosci. 1:1989;34-45.
9. Gage F.H., Chen K.S., Buszaki G., Armstrong D. Experimental approaches to age-related cognitive impairments. Neurobiol. Aging. 9:1988;645-655.
10. Luine V., Bowling D., Hearnes M. Spatial memory deficits in aged rats: contribution of monoaminergic systems. Brain Res. 537:1990;271-278.
11. Richter-Levin G., Segal M. Serotonin, aging and cognitive functions of the hippocampus. Rev. Neurosci. 7:1996;103-113.
12. Zhang W.Q., Mundy W., Thai L., Hudson P.M., Gallagher M., Tilson H.A., Hong J.S. Decreased glutamate release correlates with elevated dynorphin content in the hippocampus of aged rats with spatial memory learning deficits. Hippocampus. 1:1991;391-398.
13. Deupree D.L., Turner D.A., Watters C.L. Spatial performance correlates with in vitro potentiation in young and aged F344 rats. Neurobiol. Aging. 555:1991;1-9.
14. Shen J., Barnes C.A., McNaughton B.L., Skaggs W.E., Weaver K.L. The effect of aging on experience-dependent plasticity of hippocampal place cells. J. Neurosci. 17:1997;6769-6782.
15. Fordyce D.E., Wehner J.M. Effects of aging on spatial learning and hippocampal protein kinase C in mice. Neurobiol. Aging. 14:1993;309-317.
16. Costantini L.C., Chaturvedi P., Armistead D.M., McCaffrey P.G., Deacon T.W., Isacson O. A novel immunophilin ligand: distinct branching effects on dopaminergic neurons in culture and neurotrophic actions after oral administration in an animal model of Parkinson's disease. Neurobiol. Dis. 2:1998;97-106.
17. Kitamura Y., Itano Y., Kubo T., Nomura Y. Suppressive effect of FK-506, a novel immuno-suppressant, against MPTP-induced dopamine depletion in the striatum of young C57BL/6 mice. J. Neuroimmunol. 50:1994;221-224.
18. Ross D.T., Valentine H.L., Guo H., Hamilton G.S., Huang W., Suzdak P.D., Steiner J.P. Novel neuroimmunophilin ligands for FKBP 12 possess potent neurotrophic activity in the mouse MPTP model of Parkinson's disease. Soc. Neurosci. Abstr. 22:1996;297.14.
19. Steiner J.P., Connolly M.A., Valentine H.L., Hamilton G.S., Dawson T.M., Hester L., Snyder S.H. Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin. Ann. Nat. Med. 3:1997;421-428.
20. Gold B.G., Katoh K., Storm-Dickerson T. The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. Neurosci. 15:1995;7509-7516.
21. Gold B.G., Zeleny-Pooley M., Chaturvedi P., Wang M.S. Oral administration of a nonimmunosuppressant FKBP-12 ligand speeds nerve regeneration. NeuroReport. 9:1998;553-558.
22. Harper S., Bilsland J., Young L., Bristow L., Boyce S., Mason G., Rigby M., Hewson L., Smith D., O'Donnell R., O'Connor D., Hill R.G., Evans D., Swain C., Williams B., Hefti F. Analysis of the neurotrophic effects of GPI-1046 on neuron survival and regeneration in culture and in vivo. Neuroscience. 88:1998;257-267.
23. Steiner J.P., Hamilton G.S., Ross D.T., Valentine H.L., Guo H., Connolly M.A., Liang S., Ramsey C., Li J., Huang W., Howorth P., Soni R., Fuller M., Sauer H., Nowotnik A.C., Suzdak P.D. Neurotrophic immunophilin ligands stimulate structural and functional recovery in neurodegenerative animal models. Proc. Natl. Acad. Sci. U.S.A. 94:1998;2019-2024.
24. Lindner M.D., Balch A.H., van der Maelen C.P. Short forms of the "reference" and "working memory" Morris water maze for assessing age-related deficits. Behav. Neural Biol. 58:1992;94-102.
25. E.B.V. Jensen, H.J.G. Gundersen, The Rotator, Research report no. 247, Dept. of Theoretical Statistics, Inst. of Mathematics and Stereological Res. Lab., University of Aarhus, Denmark, 1992.
26. Gage F.H., Wictorin K., Fischer W., Williams L.R., Varon S., Björklund A. Retrograde cell changes in medial septum and diagonal band following fimbria-fornix transection: quantitative temporal analysis. Neuroscience. 19:1986;241-255.
27. Bellush L.L., Wright A.M., Walker J.P., Kopchick J., Colvin R.A. Caloric restriction and spatial learning in old mice. Physiol. Behav. 60:1996;541-547.
28. Lamberty Y., Gower A.J. Age-related changes in spontaneous behavior and learning in NMRI mice from maturity to middle age. Physiol. Behav. 47:1990;1137-1144.
29. Lamberty Y., Gower A.J. Simplifying environmental cues in a Morris-type water maze improves place learning in old NMRI mice. Behav. Neural Biol. 56:1991;89-100.
30. Lindner M.D. Reliability, distribution and validity of age-related cognitive deficits in the Morris water maze. Neurobiol. Learn. Mem. 68:1997;203-220.
31. Hornberger J.C., Buell S.J., Flood D.G., McNeill T.H., Coleman P.D. Stability of numbers but not size of mouse forebrain cholinergic neurons to 53 months. Neurobiol. Aging. 6:1995;269-275.
32. Fischer W., Björklund A., Chen K.S., Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 11:1991;1889-1906.
33. Chen K.S., Masliah E., Mallory M., Gage F.H. Synaptic loss in cognitively impaired aged rats is ameliorated by chronic human nerve growth factor infusion. Neuroscience. 68:1995;19-27.
34. Fischer W., Wictorin K., Björklund A., Williams L.R., Varon S., Gage F.H. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature. 329:1987;65-68.
35. Gallagher M., Pelleymounter M.A. An age-related spatial learning deficit: choline uptake distinguishes "impaired" and "unimpaired" rats. Neurobiol. Aging. 9:1988;363-369.
36. Markowska A.L., Koliatsos V.E., Breckler S.J., Price D.L., Olton D.S. Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 14:1994;4815-4824.
37. Pelleymounter M.A., Cullen M.J., Baker M.B., Gollub M., Wellman C. The effects of intrahippocampal BDNF and NGF on spatial learning in aged Long Evans rats. Mol. Chem. Neuropathol. 29:1996;211-226.
38. Schreiber S.L. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science. 251:1991;283-287.
39. Martin C., Chapman K.E., Seckl J.R., Ashley R.H. Partial cloning and differential expression of ryanodine receptor/calcium-release channel genes in human tissues including the hippocampus and cerebellum. Neuroscience. 85:1998;205-216.
40. Nakanishi S., Maeda N., Mikoshiba K. Immunohistochemical localization of an inositol 1,4,5-trisphosphate receptor, P400, in neural tissue: studies in developing and adult mouse brain. J. Neurosci. 11:1991;2075-2086.
41. Nakashima Y., Nishimura S., Maeda A., Barsoumian E.L., Hakamata Y., Nakai J., Allen P.D., Imoto K., Kita T. Molecular cloning and characterization of a human brain ryanodine receptor. FEBS Lett. 417:1997;157-162.
42. Brillantes A.B., Ondrias K., Scott A., Kobrinsky E., Ondriasova E., Moschella M.C., Jayaraman T., Landers M., Ehrlich B.E., Marks A.R. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell. 77:1994;513-523.
43. Cameron A.M., Steiner J.P., Sabatini D.M., Kaplin A.I., Walensky L.D., Snyder S.H. Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. U.S.A. 92:1995;1784-1788.
44. Marks A.R. Cellular functions of immunophilins. Physiol. Rev. 76:1996;631-649.
45. Snyder S.H., Sabatini D.M. Immunophilins and the nervous system. Nat. Med. 1:1995;32-37.
46. Reyes M., Stanton P.K. Induction of hippocampal long-term depression requires release of Ca2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci. 16:1996;5951-5960.
47. Schiegg A., Gerstner W., Ritz R., van Hemmen J.L. Intracellular Ca2+ stores can account for the time course of LTP induction: a model of Ca2+ dynamics in dendritic spines. J. Neurophysiol. 74:1995;1046-1055.
48. Wang Y., Rowan M.J., Anwyl R. Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent, but dependent on Ca2+ influx via low-voltage-activated Ca2+ channels and release of Ca2+ from intracellular stores. J. Neurophysiol. 77:1997;812-825.
49. Wang Y., Wu J., Rowan M.J., Anwyl R. Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J. Physiol. (London). 495:1996;755-767.
50. Cavallaro S., Meiri N., Yi C.L., Musco S., Ma W., Goldberg J., Alkon D.L. Late memory-related genes in the hippocampus revealed by RNA fingerprinting. Proc. Natl. Acad. Sci. U.S.A. 94:1997;9669-9673.
51. Haug L.S., Ostvold A.C., Cowburn R.F., Garlind A., Winblad B., Bogdanovich N., Walaas S.I. Decreased inositol (1,4,5)-trisphosphate receptor levels in Alzheimer's disease cerebral cortex: selectivity of changes and possible correlation to pathological severity. Neurodegeneration. 5:1996;169-176.
52. Young L.T., Kish S.J., Li P.P., Warsh J.J. Decreased brain 3[H]inositol 1,4,5-trisphosphate binding in Alzheimer's disease. Neurosci. Lett. 94:1988;198-202.
53. Kurumatani T., Fastbom J., Bonkale W.L., Bogdanovic N., Winblad B., Ohm T.G., Cowburn R.F. Loss of inositol 1,4,5-trisphosphate receptor sites and decreased PKC levels correlate with staging of Alzheimer's disease neurofibrillary pathology. Brain Res. 796:1998;209-221.
54. Lu Y.F., Tomizawa K., Moriwaki A., Hayashi Y., Tokuda M., Itano T., Hatase O., Matsui H. Calcineurin inhibitors, FK506 and cyclosporin A, suppress the NMDA receptor-mediated potentials and LTP, but not depotentiation in the rat hippocampus. Brain Res. 729:1996;142-146.
55. Wang J.H., Kelly P.T. Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. J. Neurophysiol. 78:1997;2702-2716.
56. Lopez-Ilasaca M., Schiene C., Kullertz G., Tradler T., Fischer G., Wetzker R. Effects of FK506-binding protein 12 and FK506 on autophosphorylation of epidermal growth factor receptor. J. Biol. Chem. 273:1998;9430-9434.
57. Wang T., Li B.Y., Danielson P.D., Shah P.C., Rockwell S., Lechleider R.J., Martin J., Manganaro T., Donahoe P.K. The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell. 86:1996;435-444.
58. Okadome T., Oeda E., Saitoh M., Ichijo H., Moses H.L., Miyazono K., Kawabata M. Characterization of the interaction of FKBP12 with the transforming growth factor-beta type I receptor in vivo. J. Biol. Chem. 271:1996;21687-21690.
59. Chen Y.G., Liu F., Massague J. Mechanism of TGFbeta receptor inhibition by FKBP12. EMBO J. 16(1997):1997;3866-3876.
60. Wang T., Donahoe P.K., Zervos A.S. Specific interaction of type I receptors of the TGF-beta family with the immunophilin FKBP-12. Science. 265:1994;674-676.
61. Bassing C.H., Shou W., Muir S., Heitman J., Matzuk M.M., Wang X.F. FKBP12 is not required for the modulation of transforming growth factor beta receptor I signaling activity in embryonic fibroblasts and thymocytes. Cell Growth Differ. 9:1998;223-228.
62. Shou W., Aghdasi B., Armstrong D.L., Guo Q., Bao S., Charng M.J., Mathews L.M., Schneider M.D., Hamilton S.L., Matzuk M.M. Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature. 391:1998;489-492.
63. Lindholm D., Hengerer B., Zafra F., Thoenen H. Transforming growth factor-beta 1 stimulates expression of nerve growth factor in the rat CNS. NeuroReport. 1:1990;9-12.
64. Hahn M., Lorez H., Fischer G. The immortalized astroglial cell line RC7 is a new model system for the study of nerve growth factor (NGF) regulation: stimulation by interleukin-1 beta and transforming growth factor-beta 1 is additive and affected differently by dibutyryl cyclic AMP. Glia. 10:1994;286-295.