Aging in the hippocampus: Interrelated actions of neurotrophins and glucocorticoids

Neuroscience and Biobehavioral Reviews

Volumn 21, Issue 5, 1997, Pages 615-629

  McLay, Robert N ^a,c   Freeman, Scott M ^a   Harlan, Richard E ^a   Ide, Charles F ^b   Kastin, Abba J ^a   Zadina, James E ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Tulane University   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Adrenalectomy; Aging; Alzheimer's disease; Brain derived neurotrophic factor; Calcium; Corticosteroids; Feedback; Glucocorticoids; Growth factors; Hippocampus; Hypothalamic pituitary adrenal axis; Learning; Memory; Nerve growth factors; Neurotrophins; Pyramidal neurons; Senility; Steroids; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; GLUCOCORTICOID; NERVE GROWTH FACTOR; NEUROTROPHIN;

ADRENALECTOMY; AGING; ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; COGNITION; FEEDBACK SYSTEM; HIPPOCAMPUS; HORMONE ACTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SENESCENCE; SENILITY; STRESS;

AGING; ANIMALS; GLUCOCORTICOIDS; HIPPOCAMPUS; HUMANS; NERVE GROWTH FACTORS;

EID: 0030723964     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(96)00046-2     Document Type: Article

References (165)

1. Ahima R., Krozowski Z., Harlan R. Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by corticosteroids. J. Comp. Neurol. 313:1991;522-538.
2. Alberch J., Perez-Navarro E., Arenas E., Marsal J. Involvement of nerve growth factor and its receptor in the regulation of the cholinergic function in aged rats. J. Neurochem. 57:1991;1483-1487.
3. Aloe L. Adrenalectomy decreases nerve growth factor in young adult rat hippocampus. Proc. Natl Acad. Sci. U.S.A. 86:1989;5636-5640.
4. Aloe L., Alleva E., Bohm A., Levi-Montalcini R. Aggressive behavior induces release of nerve growth factor from mouse salivary gland into the bloodstream. Proc. Natl Acad. Sci. U.S.A. 83:1986;6184-6187.
5. Aloe L., Bracci-Laudiero L., Alleva E., Lambiase A., Micera A., Tirassa P. Emotional stress induced by parachute jumping enhances blood nerve growth factor levels and the distribution of nerve growth factor receptors in lymphocytes. Proc. Natl Acad. Sci. U.S.A. 91:1994;10440-10444.
6. Anderson D.J. Cell fate determination in the peripheral nervous system: the sympathoadrenal progenitor. J. Neurobiol. 24:1993;185-198.
7. Arbel I., Kadar T., Silbermann M., Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res. 657:1994;227-235.
8. Armanini M.P., Hutchins C., Stein B.A., Sapolsky R.M. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res. 532:1990;7-12.
9. Barbany G., Persson H. Regulation of neurotrophin mRNA expression in the rat brain by glucocorticoids. Eur. J. Neurosci. 4:1992;396-403.
10. Barbany G., Persson H. Adrenalectomy attenuates kainic acid-elicited increases of messenger RNAs for neurotrophins and their receptors in the rat brain. Neuroscience. 54:1993;909-922.
11. Barnes C.A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psych. 93:1979;74-104.
12. Barnes C.A. Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 17:1994;13-18.
13. Bishop J.F., Mueller G.P., Mouradian M.M. A calcium responsive promoter in the rat BDNF gene. Soc. Neurosci. Abstr. 20:1994;1308.
14. Bouffard J.P., Jarrard L.E. Acquisition of a complex place task in rats with selective ibotenate lesions of hippocampal formation: combined lesions of subiculum and entorhinal cortex versus hippocampus. Behav. Neurosci. 102:1988;828-834.
15. Byers M.R., Wheeler E.F., Bothwell M. Altered expression of NGF and P75 NGF-receptor by fibroblasts of injured teeth precedes sensory nerve sprouting. Growth Factors. 6:1992;41-52.
16. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res. 611:1993;342-346.
17. Chao H.M., McEwen B.S. Glucocorticoids and the expression of mRNAs for neurotrophins, their receptors and GAP-43 in the rat hippocampus. Brain Res. Molec. Brain Res. 650:1994;271-276.
18. Cheng B., Goodman Y., Begley J.G., Mattson M.P. Neurotrophin-4/5 protects hippocampal and cortical neurons against energy deprivation- and excitatory amino acid-induced injury. Brain Res. 650:1994;331-335.
19. Cheng B., Mattson M.P. NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 640:1994;56-67.
20. Cohen S. Purification and metabolic effects of a nerve growth promoting protein from the mouse salivary gland and its neurocytoxic antiserum. Proc. Natl Acad. Sci. U.S.A. 46:1960;302-311.
21. Colangelo A., Mocchetti I., Hayes V.Y., Isackson P.J. Induction of NGF and bFGF mRNA by glucocorticoids in rat brain. Soc. Neurosci. Abstr. 20:1994;1302.
22. Coleman P.D., Flood D.G. Dendritic proliferation in the aging brain as a compensatory repair mechanism. Progr. Brain Res. 70:1986;227-237.
23. Coleman P.D., Flood D.G. Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol. Aging. 8:1987;521-545.
24. Cosi C., Spoerri P.E., Comelli M.C., Guidolin D., Skaper S.D. Glucocorticoids depress activity-dependent expression of BDNF mRNA in hippocampal neurones. Neuroreport. 4:1993;527-530.
25. Crutcher K.A., Weingartner J. Hippocampal NGF levels are not reduced in the aged Fischer 344 rat. Neurobiol. Aging. 12:1991;449-454.
26. D'Mello S.R., Heinrich G. Multiple signalling pathways interact in the regulation of nerve growth factor production in L929 fibroblasts. J. Neurochem. 57:1991;1570-1576.
27. D'Mello S.R., Jiang C., Lamberti C., Martin S.C., Heinrich G. Differential regulation of the nerve growth factor and brain-derived neurotrophic factor genes in L929 mouse fibroblasts. J. Neurosci. Res. 33:1992;519-526.
28. DiStefano P.S., Friedman B., Radziejewski C., Alexander C., Boland P., Schick C.M., Lindsay R.M., Wiegand S.J. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 8:1992;983-993.
29. Drachman D.A., Hughes J.R. Memory and the hippocampal complexes. 3. Aging and temporal EEG abnormalities Neurology. 21:1971;1-14.
30. Dragunow M., Faull R.L., Lawlor P., Beilharz E.J., Singleton K., Walker E.B., Mee E. In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimer's disease temporal lobes. Neuroreport. 6:1995;1053-1057.
31. Dunn J.D., Orr S.E. Differential plasma corticosterone responses to hippocampal stimulation. Exp. Brain Res. 54:1984;1-6.
32. Eckenhoff M.F., Rakic P. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J. Neurosci. 8:1988;2729-2747.
33. Fabrazzo M., Costa E., Mocchetti I. Stimulation of nerve growth factor biosynthesis in developing rat brain by reserpine: steroids as potential mediators. Molec. Pharmac. 39:1991;144-149.
34. Feldman S., Conforti N. Participation of the dorsal hippocampus in the glucocorticoid feedback effect on adrenocortical activity. Neuroendocrinology. 30:1980;52-55.
35. Feldman S., Weidenfeld J. The dorsal hippocampus modifies the negative feedback effect of glucocorticoids on the adrenocortical and median eminence CRF-41 responses to photic stimulation. Brain Res. 614:1993;227-232.
36. Fernandez-Sanchez M.T., Novelli A. Basic fibroblast growth factor protects cerebellar neurons in primary culture from NMDA and non-NMDA receptor mediated neurotoxicity. Fedn. Eur. Biochem. Socs Lett. 335:1993;124-131.
37. Finch, C.E. Longevity, senescence and the genome. Chicago: University of Chicago Press; 1990.
38. Fischer W., Bjorklund A., Chen K., Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 11:1991;1889-1906.
39. Foreman P.J., Taglialatela G., Angelucci L., Turner C.P., Perez-Polo J.R. Nerve growth factor and p75NGFR factor receptor mRNA change in rodent CNS following stress activation of the hypothalamo-pituitary-adrenocortical axis. J. Neurosci. Res. 36:1993;10-18.
40. Foreman P.J., Taglialatela G., Jackson G.R., Perez-Polo J.R. Dexamethasone blocks nerve growth factor induction of nerve growth factor receptor mRNA in PC12 cells. J. Neurosci. Res. 31:1992;52-57.
41. Friedman W.J., Larkfors L., Ayer-LeLievre C., Ebendal T., Olson L., Persson H. Regulation of beta-nerve growth factor expression by inflammatory mediators in hippocampal cultures. J. Neurosci. Res. 27:1990;374-382.
42. Frim D.M., Yee W.M., Isacson O. NGF reduces striatal excitotoxic neuronal loss without affecting concurrent neuronal stress. Neuroreport. 4:1993;655-658.
43. Frolkis, V.V. Aging and life-prolonging processes. New York: Wieg Press; 1982.
44. Gallagher M., Nicolle M.M. Animal models of normal aging: relationship between cognitive decline and markers in hippocampal circuitry. Behav. Brain Res. 57:1993;155-162.
45. Geinisman Y., de Toledo-Morrell L., Morrell F., Persina I.S., Rossi M. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus. 2:1992;437-444.
46. Gibbs R.B., Wu D., Hersh L.B., Pfaff D.W. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp. Neurol. 129:1994;70-80.
47. Gnahn H., Hefti F., Heumann R., Schwab M.E., Thoenen H. NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain? Brain Res. 285:1983;45-52.
48. Gotz R., Koster R., Winkler C., Raulf F., Lottspeich F., Schartl M., Thoenen H. Neurotrophin-6 is a new member of the nerve growth factor family. Nature. 372:1994;266-269.
49. Gould E., Cameron H.A., Daniels D.C., Woolley C.S., McEwen B.S. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 12:1992;3642-3650.
50. Gould E., Woolley C.S., Cameron H.A., Daniels D.C., McEwen B.S. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth J. Comp. Neurol. 313:1991;486-493.
51. Gruman, G.J. The fixed period controversy. New York: Arno Press; 1979.
52. Hellweg R., Fischer W., Hock C., Gage F.H., Bjorklund A., Thoenen H. Nerve growth factor levels and choline acetyltransferase activity in the brain of aged rats with spatial memory impairments. Brain Res. 537:1990;123-130.
53. Henriksson B.G., Soderstrom S., Gower A.J., Ebendal T., Winblad B., Mohammed A.H. Hippocampal nerve growth factor levels are related to spatial learning ability in aged rats. Behav. Brain Res. 48:1992;15-20.
54. Horel J.A. The neuroanatomy of amnesia. A critique of the hippocampal memory hypothesis. Brain. 101:1978;403-445.
55. Horner H.C., Packan D.R., Sapolsky R.M. Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology. 52:1990;57-64.
56. Houlgatte R., Wion D., Brachet P. Levels of nerve growth factor secreted by rat primary fibroblasts and iris transplants are influenced by serum and glucocorticoids. Brain Res. Devl. Brain. 47:1989;171-179.
57. Hyman B.T., VanHorsen G.W., Damasio A.R., Barnes C.L. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science. 225:1984;1168-1170.
58. Isaeff M., Goya L., Timiras P.S. Alterations in the growth and protein content of human neuroblastoma cells in vitro induced by thyroid hormones, stress and ageing. J. Reprod. Fert. Suppl. 46:1993;21-33.
59. Issa A.M., Rowe W., Gauthier S., Meaney M.J. Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J. Neurosci. 10:1990;3247-3254.
60. Jack C.R. Jr., Petersen R.C., O'Brien P.C., Tangalos E.G. MR-based hippocampal volumetry in the diagnosis of Alzheimer's disease. Neurology. 42:1992;183-188.
61. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12:1991;118-134.
62. Jap Tjoen San E.R., Schmidt-Michels M., Oestreicher A.B., Schotman P., Gispen W.H. Dexamethasone-induced effects on B-50/GAP-43 expression and neurite outgrowth in PC12 cells. J. Molec. Neurosci. 3:1992;189-195.
63. Jehan F., Neveu I., Naveilhan P., Brachet P., Wion D. Complex interactions among second messenger pathways, steroid hormones, and protooncogenes of the Fos and Jun families converge in the regulation of the nerve growth factor gene. J. Neurochem. 60:1993;1843-1853.
64. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
65. Katoh-Semba R., Semba R., Kato H., Ueno M., Arakawa Y., Kato K. Regulation by androgen of levels of the beta subunit of nerve growth factor and its mRNA in selected regions of the mouse brain. J. Neurochem. 62:1994;2141-2147.
66. Kawakami M., Seto K., Terasawa E., Yoshida K., Miyamoto T., Sekiguchi M., Hattori Y. Influence of electrical stimulation and lesion in limbic structure upon biosynthesis of adrenocorticoid in the rabbit. Neuroendocrinology. 3:1968;337-348.
67. Koh J.Y., Gwag B.J., Lobner D., Choi D.W. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science. 268:1995;573-575.
68. Koide T., Wieloch T.W., Siesjo B.K. Chronic dexamethasone pretreatment aggravates ischemic neuronal necrosis. J. Cereb. Blood Flow Metab. 6:1986;395-404.
69. Koivisto K., Reinikainen K.J., Hanninen T., Vanhanen M., Helkala E.L., Mykkanen L., Laakso M., Pyorala K., Riekkinen P.J. Sr. Prevalence of age-associated memory impairment in a randomly selected population from eastern Finland. Neurology. 45:1995;741-747.
70. Kokaia Z., Zhao Q., Kokaia M., Elmer E., Metsis M., Smith M.L., Siesjo B.K., Lindvall O. Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage. Exp. Neurol. 136:1995;73-88.
71. Kononen J., Soinila S., Persson H., Honkaniemi J., Hokfelt T., Pelto-Huikko M. Neurotrophins and their receptors in the rat pituitary gland: regulation of BDNF and trk B mRNA levels by adrenal hormones. Molec. Brain. Res. 27:1995;347-354.
72. Korsching S., Thoenen H. Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation. Proc. Natl Acad. Sci. U.S.A. 80:1983;3513-3516.
73. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl Acad. Sci. U.S.A. 92:1995;8856-8860.
74. Lakshmanan J. Nerve growth factor levels in mouse serum: variations due to stress. Neurochem. Res. 12:1987;393-397.
75. Landfield P.W., Baskin R.K., Pitler T.A. Brain aging correlates: retardation by hormonal-pharmacological treatments. Science. 214:1981;581-584.
76. Lapchak P.A., Araujo D.M., Beck K.D., Finch C.E., Johnson S.A., Hefti F. BDNF and trkB mRNA expression in the hippocampal formation of aging rats. Neurobiol. Aging. 14:1993;121-126.
77. Larkfors L., Ebendal T., Whittemore S.R., Persson H., Hoffer B., Olson L. Decreased level of nerve growth factor (NGF) and its messenger RNA in the aged rat brain. Brain Res. 427:1987;55-60.
78. Larkfors L., Stromberg I., Ebendal T., Olson L. Nerve growth factor protein level increases in the adult rat hippocampus after a specific cholinergic lesion. J. Neurosci. Res. 18:1987;525-531.
79. Leibrock J., Lottspeich F., Hohn A., Hofer M., Hengerer B., Masiakowski P., Thoenen H., Barde Y.A. Molecular cloning and expression of brain-derived neurotrophic factor. Nature. 341:1989;149-152.
80. Levi-Montalcini R., Hamburger V. A diffusible agent of mouse sarcoma producing hyperplasia of sympathetic ganglia and hyper-neurotization of viscera of the chick embryo. J. Exp. Zool. 123:1953;287.
81. Levy B., Langer E. Aging free from negative stereotypes: successful memory in China and among the American deaf. J. Personal. Soc. Psych. 66:1994;989-997.
82. Lindholm D., Castren E., Hengerer B., Zafra F., Berninger B., Thoenen H. Differential regulation of nerve growth factor (NGF) synthesis in neurons and astrocytes by glucocorticoid hormones. Eur. J. Neurosci. 4:1992;404-410.
83. Lindholm D., da Penha Berzaghi M., Cooper J., Thoenen H., Castren E. Brain-derived neurotrophic factor and neurotrophin-4 increase neurotrophin-3 expression in the rat hippocampus. Int. J. Devl Neurosci. 12:1994;745-751.
84. Lindholm D., Hengerer B., Heumann R., Carroll P., Thoenen H. Glucocorticoid hormones negatively regulate nerve growth factor expression in vivo and in cultured rat fibroblasts. Eur. J. Neurosci. 2:1990;795-801.
85. Loy R., Taglialatela G., Angelucci L., Heyer D., Perez-Polo R. Regional CNS uptake of blood-borne nerve growth factor. J. Neurosci. Res. 39:1994;339-346.
86. Lucidi-Phillipi C.A., Gage F.H. The neurotrophic hypothesis and the cholinergic basal forebrain projection. Progr. Brain Res. 98:1993;241-249.
87. Maehlen J., Torvik A. Necrosis of granule cells of hippocampus in adrenocortical failure. Acta Neuropathol. 80:1990;85-87.
88. Malamud, N. Neuropathology of organic brain syndrome associated with aging. In: Gaitz, C.M., ed. Aging and the brain. New York: Plenum Publishing; 1972.
89. Malmgren, R. Epidemiology of aging. In: Cummings, J.L.; Coffey, C.E. eds. Textbook of geriatric neuropsychiatry. Washington DC: American Psychiatric Press; 1996:17-33.
90. Maness L.M., Kastin A.J., Weber J.T., Banks W.A., Beckman B.S., Zadina J.E. The neurotrophins and their receptors: structure, function, and neuropathology. Neurosci. Biobehav. Rev. 18:1994;143-159.
91. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65:1995;1740-1751.
92. Mattson M.P., Scheff S.W. Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy. J. Neurotrauma. 11:1994;3-33.
93. Mattson M.P., Zhang Y., Bose S. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp. Neurol. 121:1993;1-13.
94. McEwen B.S. Re-examination of the glucocorticoid hypothesis of stress and aging. Progr. Brain Res. 93:1992;365-383.
95. McEwen B.S. The plasticity of the hippocampus is the reason for its vulnerability. Semin. Neurosci. 6:1994;239-246.
96. McNeill T.H., Masters J.N., Finch C.E. Effect of chronic adrenalectomy on neuron loss and distribution of sulfated glycoprotein-2 in the dentate gyrus of prepubertal rats. Exp. Neurol. 111:1991;140-144.
97. Mervis R.F., Pope D., Lewis R., Dvorak R.M., Williams L.R. Exogenous nerve growth factor reverses age-related structural changes in neocortical neurons in the aging rat. A quantitative Golgi study. Ann. N.Y. Acad. Sci. 640:1991;95-101.
98. Milner, B. Amnesia following operation on the temporal lobes. In: Whitty, C.W.M.; Zangwills, O.L., eds. Amnesia. London: Butterworths; 1996;109-133.
99. Mizoguchi K., Kunishita T., Chui D.H., Tabira T. Stress induces neuronal death in the hippocampus of castrated rats. Neurosci. Lett. 138:1992;157-160.
100. Nabeshima T., Nitta A., Hasegawa T. Impairment of learning and memory and the accessory symptom in aged rat as senile dementia model (3): Oral administration of propentofylline produces recovery of reduced NGF content in the brain of aged rats. Yakubutsu Seishin Kodo. 13:1993;89-95.
101. Nawa H., Carnahan J., Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur. J. Neurosci. 7:1995;1527-1535.
102. Neveu, I.; Barbot, N.; Jehan, F.; Wion, D.; Brachet, P., Antagonistic effects of dexamethasone and 1,25-dihydroxyvitamine D3 on the synthesis of nerve growth factor. Molec. Cell. Endocr., 78, R1-6 1991.
103. Neveu I., Jehan F., Houlgatte R., Wion D., Brachet P. Activation of nerve growth factor synthesis in primary glial cells by phorbol 12-myristate 13-acetate: role of protein kinase C. Brain Res. 570:1992;316-322.
104. Neveu I., Jehan F., Wion D. Alteration in the levels of 1,25-(OH)2D3 and corticosterone found in experimental diabetes reduces nerve growth factor (NGF) gene expression in vitro. Life Sci. 50:1992;1769-1772.
105. Newcomer J.W., Craft S., Hershey T., Askins K., Bardgett M.E. Glucocorticoid-induced impairment in declarative memory performance in adult humans. J. Neurosci. 14:1994;2047-2053.
106. Nieuwenhuys R. The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat. Embryol. 190:1994;307-337.
107. Nishizuka M., Katoh-Semba R., Eto K., Arai Y., Iizuka R., Kato K. Age- and sex-related differences in the nerve growth factor distribution in the rat brain. Brain Res. Bull. 27:1991;685-688.
108. Nistico G., Ciriolo M.R., Fiskin K., Iannone M., De Martino A., Rotilio G. NGF restores decrease in catalase activity and increases superoxide dismutase and glutathione peroxidase activity in the brain of aged rats. Free Radic. Bio. Med. 12:1992;177-181.
109. Olton D.S., Walker J.A., Wolf W.A. A disconnection analysis of hippocampal function. Brain Res. 233:1982;241-253.
110. Oppenheim R.W., Yin Q.W., Prevette D., Yan Q. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature. 360:1992;755-757.
111. Otten U., Baumann J.B., Girard J. Stimulation of the pituitary-adrenocortical axis by nerve growth factor. Nature. 282:1979;413-414.
112. Pan Z., Perez-Polo R. Role of nerve growth factor in oxidant homeostasis: glutathione metabolism. J. Neurochem. 61:1993;1713-1721.
113. Phillips H.S., Hains J.M., Armanini M., Laramee G.R., Johnson S.A., Winslow J.W. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron. 7:1991;695-702.
114. Plotsky P.M. Hypophyseotropic regulation of adenohypophyseal adrenocorticotropin secretion. Fedn Proc. 44:1985;207-213.
115. Pollard H., Cantagrel S., Charriaut-Marlangue C., Moreau J., Ben Ari Y. Apoptosis associated DNA fragmentation in epileptic brain damage. Neuroreport. 5:1994;1053-1055.
116. Powers, R.E. Neurobiology of aging. In: Coffey, C.E.; Cummings, J.L., eds. Textbook of geriatric neuropsychiatry. Washington DC: American Psychiatric Press; 1994;35-69.
117. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 117:1985;2505-2511.
118. Sabol S.L., Higuchi H. Transcriptional regulation of the neuropeptide Y gene by nerve growth factor: antagonism by glucocorticoids and potentiation by adenosine 3′,5′-monophosphate and phorbol ester. Molec. Endocr. 4:1990;384-392.
119. Sandi C., Rose S.P. Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 647:1994;106-112.
120. Sapolsky R.M. A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults. J. Neurosci. 5:1985;1228-1232.
121. Sapolsky R.M., Krey L.C., McEwen B.S. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl Acad. Sci. U.S.A. 81:1984;6174-6177.
122. Sapolsky R.M., Krey L.C., McEwen B.S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5:1985;1222-1227.
123. Sapolsky R.M., Stein-Behrens B.A., Armanini M.P. Long-term adrenalectomy causes loss of dentate gyrus and pyramidal neurons in the adult hippocampus. Exp. Neurol. 114:1991;246-249.
124. Sapolsky R.M., Zola-Morgan S., Squire L.R. Inhibition of glucocorticoid secretion by the hippocampal formation in the primate. J. Neurosci. 11:1991;3695-3704.
125. Saporito M.S., Brown E.R., Hartpence K.C., Wilcox H.M., Robbins E., Vaught J.L., Carswell S. Systemic dexamethasone administration increases septal Trk autophosphorylation in adult rats via an induction of nerve growth factor. Molec. Pharmac. 45:1994;395-401.
126. Scaccianoce S., Cigliana G., Nicolai R., Muscolo L.A., Porcu A., Navarra D., Perez-Polo J.R., Angelucci L. Hypothalamic involvement in the activation of the pituitary-adrenocortical axis by nerve growth factor. Neuroendocrinology. 58:1993;202-209.
127. Schipper H.M., Liang J.J., Wang E. Quiescent and cycling cell compartments in the senescent and Alzheimer-diseased human brain. Neurology. 43:1993;87-94.
128. Schonfield D., Robertson B.A. Memory storage and aging. Can. J. Psychol. 20:1966;228-236.
129. Scott S.A., Liang S., Weingartner J.A., Crutcher K.A. Increased NGF-like activity in young but not aged rat hippocampus after septal lesions. Neurobiol. Aging. 15:1994;337-346.
130. Scully J.L., Otten U. Glucocorticoid modulation of neurotrophin expression in immortalized mouse hippocampal neurons. Neurosci. Lett. 155:1993;11-14.
131. Seckl J.R., Olsson T. Glucocorticoid hypersecretion and the age-impaired hippocampus: cause or effect? J. Endocr. 145:1995;201-211.
132. Siminoski K., Murphy R.A., Rennert P., Heinrich G. Cortisone, testosterone, and aldosterone reduce levels of nerve growth factor messenger ribonucleic acid in L-929 fibroblasts. Endocrinology. 121:1987;1432-1437.
133. Singh M., Meyer E.M., Simpkins J.W. The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology. 136:1995;2320-2324.
134. Sloviter R.S., Dean E., Neubort S. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system. J. Comp. Neurol. 330:1993;337-351.
135. Sloviter R.S., Sollas A.L., Dean E., Neubort S. Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: characterization of an in vivo model of controlled neuronal death. J. Comp. Neurol. 330:1993;324-336.
136. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.L., Paul L.A., Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science. 243:1989;535-538.
137. Smith M.A., Makino S., Altemus M., Michelson D., Hong S.K., Kvetnansky R., Post R.M. Stress and antidepressants differentially regulate neurotrophin 3 mRNA expression in the locus coeruleus. Proc. Natl Acad. Sci. U.S.A. 92:1995;8788-8792.
138. Smith M.A., Makino S., Kim S.Y., Kvetnansky R. Stress increases brain-derived neurotrophic factor messenger ribonucleic acid in the hypothalamus and pituitary. Endocrinology. 136:1995;3743-3750.
139. Smith M.A., Makino S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 15:1995;1768-1777.
140. Springer J.E., Loy R. Intrahippocampal injections of antiserum to nerve growth factor inhibit sympathohippocampal sprouting. Brain Res. Bull. 15:1985;629-634.
141. Su J.H., Anderson A.J., Cummings B.J., Cotman C.W. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport. 5:1994;2529-2533.
142. Sun F.Y., Costa E., Mocchetti I. Adrenal steroids mediate the increase of hippocampal nerve growth factor biosynthesis following bicuculline convulsions. Neuropsychopharmacology. 8:1993;219-225.
143. Taglialatela G., Angelucci L., Scaccianoce S., Foreman P.J., Perez-Polo J.R. Nerve growth factor modulates the activation of the hypothalamo-pituitary-adrenocortical axis during the stress response. Endocrinology. 129:1991;2212-2218.
144. Tocco M.D., Contreras M.L., Koizumi S., Dickens G., Guroff G. Decreased levels of nerve growth factor receptor on dexamethasone-treated PC12 cells. J. Neurosci. Res. 20:1988;411-419.
145. Tomlinson, B. Morphological brain changes in non-demented old people. In: VanPraag H.M.; Kalverboer, A.K., eds. Aging of the central nervous system. New York: De Ervon F. Bohn; 1996.
146. Tourigny-Rivard M.F., Raskind M., Rivard D. The dexamethasone suppression test in an elderly population. Biol. Psychiatr. 16:1981;1177-1184.
147. Tria M.A., Fusco M., Vantini G., Mariot R. Pharmacokinetics of nerve growth factor (NGF) following different routes of administration to adult rats. Exp. Neurol. 127:1994;178-183.
148. Valenti G. Psychoneuroendocrinology of aging: the brain as target organ of hormones. Psychoneuroendocrinology. 17:1992;279-282.
149. Van der Zee C.E., Lourenssen S., Stanisz J., Diamond J. NGF deprivation of adult rat brain results in cholinergic hypofunction and selective impairments in spatial learning. Eur. J. Neurosci. 7:1995;160-168.
150. Van Hoesen G.W., Hyman B.T., Damasio A.R. Cell-specific pathology in neural systems of the temporal lobe in Alzheimer's disease. Progr. Brain Res. 70:1986;321-335.
151. Vantini G., Schiavo N., Di Martino A., Polato P., Triban C., Callegaro L., Toffano G., Leon A. Evidence for a physiological role of nerve growth factor in the central nervous system of neonatal rats. Neuron. 3:1989;267-273.
152. Virgin C.E. Jr., Ha T.P., Packan D.R., Tombaugh G.C., Yang S.H., Horner H.C., Sapolsky R.M. Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J. Neurochem. 57:1991;1422-1428.
153. Volpe B.T., Wessel T.C., Mukherjee B., Federoff H.J. Temporal pattern of internucleosomal DNA fragmentation in the striatum and hippocampus after transient forebrain ischemia. Neurosci. Lett. 186:1995;157-160.
154. Wallace J.E., Krauter E.E., Campbell B.A. Animal models of declining memory in the aged: short-term and spatial memory in the aged rat. J. Gerontol. 35:1980;355-363.
155. Warner, H.R.; Butler, R.N.; Sprott, R.L.; Schneider, E.L. Modern biological theories of aging. New York: Raven Press; 1987.
156. Werrbach-Perez K., Jackson G., Marchetti D., Morgan B., Thorpe L., Perez-Polo J.R. Growth factor-mediated protection in aging CNS. Progr. Brain Res. 86:1990;183-194.
157. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet. 344:1994;769-772.
158. Whishaw I.Q., Cassel J.C., Jarrad L.E. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J. Neurosci. 15:1995;5779-5788.
159. Wion D., Houlgatte R., Brachet P. Dexamethasone rapidly reduces the expression of the beta-NGF gene in mouse L-929 cells. Exp. Cell Res. 162:1986;562-565.
160. Wion D., MacGrogan D., Neveu I., Jehan F., Houlgatte R., Brachet P. 1,25-Dihydroxyvitamin D3 is a potent inducer of nerve growth factor synthesis. J. Neurosci. Res. 28:1991;110-114.
161. Woodruff-Pak, D.S. Psychology and aging. Englewood Cliffs: Prentice-Hall; 1988.
162. Yakovlev A.G., De Bernardi M.A., Fabrazzo M., Brooker G., Costa E., Mocchetti I. Regulation of nerve growth factor receptor mRNA content by dexamethasone: in vitro and in vivo studies. Neurosci. Lett. 116:1990;216-220.
163. Yamamoto S., Yoshimine T., Fujita T., Kuroda R., Irie T., Fujioka K., Hayakawa T. Protective effect of NGF atelocollagen mini-pellet on the hippocampal delayed neuronal death in gerbils. Neurosci. Lett. 141:1992;161-165.
164. Yankner B.A., Caceres A., Duffy L.K. Nerve growth factor potentiates the neurotoxicity of beta amyloid. Proc. Natl Acad. Sci. U.S.A. 87:1990;9020-9023.
165. Zornetzer S.F., Boast C., Hamrick M. Neuroanatomic localization and memory processing in mice: the role of the dentate gyrus of the hippocampus. Physiol. Behav. 13:1974;569-575.