The mosaic of brain glial hyperactivity during normal ageing and its attenuation by food restriction

Neuroscience

Volumn 89, Issue 3, 1999, Pages 687-699

  Morgan, T E ^a   Xie, Z ^a   Goldsmith, S ^b   Yoshida, T ^c   Lanzrein, A S ^a   Stone, D ^a   Rozovsky, I ^a   Perry, G ^d   Smith, M A ^d   Finch, C E ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b RMB Bldg #124 St Elizabeth H   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ageing; Apolipoprotein E; Brain; Clusterin; Food restriction; Glial fibrillary acidic protein

Indexed keywords

APOLIPOPROTEIN E; CLUSTERIN; COMPLEMENT COMPONENT C3 RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; HEME OXYGENASE; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BASAL GANGLION; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS CALLOSUM; DIET RESTRICTION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGING; ANIMALS; ASTROCYTES; FOOD DEPRIVATION; FROZEN SECTIONS; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MICROGLIA; OXIDATIVE STRESS; RATS; RATS, INBRED BN; RATS, INBRED F344; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0032910605     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00334-0     Document Type: Article

References (81)

1. Aboitiz F., Rodriguez E., Olivares R., Zaidel E. Age-related differences in the fibre composition of the human corpus callosum: sex differences. NeuroReport. 7:1996;1761-1764.
2. Barnes C.A. Normal ageing: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 17:1994;13-18.
3. Beatty W.W., Clouse A.B., Bierley R.A. Effects of long-term restricted feeding on radial maze performance by aged rats. Neurobiol. Aging. 8:1987;325-327.
4. Bond N.W., Everitt A.V., Walton J. Effects of dietary restriction on radial maze performance and flavor memory in aged rats. Neurobiol. Aging. 10:1989;27-30.
5. Bronson R. T. (1990) Rate of occurrence of lesions in 20 inbred and hybrid genotypes of rats and mice sacrificed at 6 month intervals during the first years of life. In Genetic Effects on Ageing II (ed. Harrison D. E.), pp. 279-358. Telford, Caldwell, NJ.
6. Carney J.M., Starke-Reed P.E., Oliver C.N., Landum R.W., Cheng M.S., Wu J.F., Floyd R.A. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spintrapping compound N-tert-butyl-α-phenylnitrone. Proc. natn. Acad. Sci. U.S.A. 88:1991;3633-3636.
7. Cini M., Moretti A. Lipid peroxidation and protein oxidation in aging brain. Neurobiol. Aging. 16:1995;53-57.
8. Coleman P.D., Kaplan B.B., Osterburg H.H., Finch C.E. Brain poly(A) RNA during aging: stability of yield and sequence complexity in two rat strains. J. Neurochem. 34:1980;335-345.
9. de la Cruz C.P., Revilla E., Steffen V., Rodriguez-Gomez J.A., Cano J., Machado A. Protection of the aged substantia nigra of the rat against oxidative damage by (-)-deprenyl. Br. J. Pharmac. 117:1996;1756-1760.
10. Dubey A., Forster M.J., Lal H., Sohal R.S. Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Archs Biochem. Biophys. 333:1996;189-197.
11. Dwyer B.E., Nishimura R.N., Lu S.Y. Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of a new heme oxygenase antibody. Response to oxidative stress. Molec. Brain Res. 30:1995;37-47.
12. Fagan A.M., Gage F.H. Cholinergic sprouting in the hippocampus: a proposed role for IL-1. Expl Neurol. 110:1990;105-120.
13. Finch C. E. and Morgan T. E. (1997) Food restriction and brain ageing. In The Ageing Brain (ed. Mattson M.), Advances in Cell Ageing Gerontology, Vol. 2, pp. 279-297. JAI Press, Greenwich, CT.
14. Frederickson R.C. A. Astroglia in Alzheimer's disease. Neurobiol. Aging. 13:1992;239-253.
15. Geinisman Y., Detoledo-Morrell L., Morrell F., Heler R.E. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological, and morphological perspectives. Prog. Neurobiol. 45:1995;223-252.
16. Gómez-Isla T., Price J.L., McKeel N.W. Jr., Morris J.C., Growdon J.H., Hyman B.T. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer disease. J. Neurosci. 16:1996;4491-4500.
17. Goss J.R., Finch C.E., Morgan D.G. GFAP RNA prevalence is increased in aging and in wasting mice. Expl Neurol. 108:1990;266-268.
18. Goss J.R., Finch C.E., Morgan D.G. Age-related changes in glial fibrillary acid protein mRNA in the mouse brain. Neurobiol. Aging. 12:1991;165-170.
19. Hayakawa K., Konishi Y., Takeshi M. Development and aging of brain midline structures: assessment with MR imaging. Radiology. 172:1989;171-177.
20. Hof P.R., Morrison J.H. Hippocampal and neocortical involvement in normal brain aging and dementia: morphological and neurochemical profile of the vulnerable circuits. J. Am. geront. Soc. 44:1996;857-864.
21. Hori N., Hirotsu I., Davis P.J., Carpenter D.O. Long-term potentiation is lost in aged rats but preserved by calorie restriction. NeuroReport. 3:1992;1085-1088.
22. Ingram D.K., Weindruch R., Spangler E.L., Freeman J.R., Walford R.L. Dietary restriction benefits learning and motor performance of aged mice. J. Geront. 42:1987;78-81.
23. Joseph J.A., Whitaker J., Roth G., Ingram D.K. Life-long dietary restriction affects striatally-mediated behavioral responses in aged rats. Neurobiol. Aging. 4:1983;191-196.
24. Kemper T. L. (1994) Neuroanatomical and neuropathological changes during aging and dementia. In Clinical Neurology of Aging (eds Albert M. L. and Knoefel J. E.), pp. 3-67. Oxford University Press, New York.
25. Kohama S.G., Goss J.R., Finch C.E., McNeill T.H. Increases of glial fibrillary acidic protein in the aging female mouse brain. Neurobiol. Aging. 16:1995;59-67.
26. Koistinaho J., Miettinen S., Keinanen R., Vartiainen N., Roivainen R., Laitinen J.T. Long-term induction of haem oxygenase-1 (HSP-32) in astrocytes and microglia following transient focal brain ischaemia in the rat. Eur. J. Neurosci. 8:1996;2265-2272.
27. Krekosi C.A., Parhad I.M., Fung T.S., Clark A.W. Ageing is associated with divergent effects on Nf-L and GFAP transcription in rat brain. Neurobiol. Aging. 17:1996;833-842.
28. LaDu M.J., Gilligan S.M., Reardon C.A., Getz G.S., Van Eldik L.J., Holtzman D.M. Characterization of apolipoprotein E-containing particles from CSF and cultured astrocytes. Soc. Neurosci. Abstr. 23:1997;828.
29. Lampert-Etchells M., McNeill T.H., Laping N.J., Zarow C., Finch C.E., May P.C. Sulfated glycoprotein-2 is increased in rat hippocampus following entorhinal cortex lesioning. Brain Res. 653:1991;101-106.
30. Lanahan A., Lydfor G., Stevenson G.S., Worley P.F., Barnes C.A. Selective alteration of long-term potentiation-induced transcriptional response in hippocampus of aged-memory impaired rats. J. Neurosci. 17:1997;2878-2885.
31. Landfield P.W., Braun L.D., Pitler T.A., Lindsey J.D., Lynch G.D. Hippocampal aging in rats: a morphometric study of multiple variables in thin sections. Neurobiol. Aging. 2:1981;265-275.
32. Laping N.J., Morgan T.E., Nichols N.R., Rozovsky I., Young-Chan C., Zarow C., Finch C.E. Transforming growth factor-β1 induces neuronal and astrocyte genes: tubulin α1, glial fibrillary acidic protein, and clusterin. Neuroscience. 58:1994;563-572.
33. Laping N.J., Teter B., Anderson C., O'Callaghan J.P., Johnson S.A., Finch C.E. Age-related increases in glial fibrillary acidic protein are not associated with proportionate changes in transcription rates or DNA methylation in the cerebral cortex and hippocampus of male rats. J. Neurosci. Res. 39:1994;710-717.
34. Lewis D.A., Campbell M.J., Terry R.D., Morrison J.H. Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. J. Neurosci. 7:1987;1799-1808.
35. Major D.E., Kesslak J.P., Cotman C.W., Finch C.E., Day J.R. Life-long dietary restriction attentuates age-related increases in glial fibrillary acidic protein (GFAP) mRNA in the rat hippocampus. Neurobiol. Aging. 18:1997;523-526.
36. Masoro E.H. Dietary restriction and aging. J. Am. geriatr. Soc. 41:1993;994-1000.
37. May P.C., Telford N., Salo D., Anderson C.P., Kohama S.G., Finch C.E., Walford R.L., Weindruch R. Failure of dietary restriction to retard age-related neurochemical changes in mice. Neurobiol. Aging. 13:1992;787-791.
38. McCall M.A., Gregg R.G., Behringer R.R., Brenner M., Delaney C.L., Galbreath E.J., Zhang C.L., Pearce R.A., Chiu S.Y., Messing A. Targeted deletion in GFAP alters neuronal physiology. Proc. natn. Acad. Sci. U.S.A. 93:1996;6361-6366.
39. McGeer P.L., Kawamata T., Walker D.G., Akiyama H., Tooyama I., McGeer E.G. Microglia in degenerative neurological disease. Glia. 7:1993;84-92.
40. Meda L., Cassatella M.A., Szendrei G.I., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by β-amyloid protein and interferon-γ Nature. 374:1995;647-650.
41. Morgan T.E., Nichols N.R., Pasinetti G.M., Finch C.E. TGF-β1 mRNA increases in macrophage/microglia cells of the hippocampus in response to deafferentation and kainic acid-induced neurodegeneration. Expl Neurol. 120:1993;291-301.
42. Morgan T.E., Laping N.J., Rozovsky I., Oda T., Hogan H., Finch C.E., Pasinetti G.M. Clusterin expression in astrocytes is influenced by TGF-β1 and heterotypic cell interactions. J. Neuroimmun. 58:1995;101-110.
43. Morgan T.E., Rozovsky I., Goldsmith S.K., Stone D.J., Yoshida T., Finch C.E. Increased transcription of the astrocyte gene GFAP during middle-age is attenuated by food restriction: implications for the role of oxidative stress. Free Rad. Biol. Metab. 23:1997;524-528.
44. Nichols N.R., Day J.R., Laping N.J., Johnson S.A., Finch C.E. GFAP mRNA increases with age in rat and human brain. Neurobiol. Aging. 14:1993;421-429.
45. Nichols N.R., Finch C.E., Nelson J.F. Food restriction delays the age-related increases of GFAP mRNA in rat hypothalamus. Neurobiol. Aging. 16:1995;105-110.
46. O'Steen W.K., Landfield P.W. Dietary restriction does not alter retinal aging in the Fischer 344 rat. Neurobiol. Aging. 12:1991;455-462.
47. O'Steen W.K., Cadwallader L.B., Vinsant S., Landfield P.W. Biomarkers of hippocampal and retinal aging are not altered by dietary restriction. Soc. Neurosci. Abstr. 16:1991;190.
48. Pasinetti G.M., Kohama S., Rheinhard J.F. Jr., Cheng H.W., McNeill T.H., Finch C.E. Striatal responses to decortication. I. Dopaminergic and astrocytic activities. Brain Res. 567:1991;253-259.
49. Pasinetti G.P., Finch C.E. Sulfated glycoprotein-2 (SGP-2) mRNA is expressed in rat striatal astrocytes following ibotenic acid lesions. Neurosci. Lett. 13:1991;1-4.
50. Pasinetti G.M., Nichols N.R., Tocco G., Morgan T., Laping N., Finch C.E. Transforming growth factor-β1 (TGF-β1) and fibronectin mRNA in rat brain: responses to injury and cell-type localization. Neuroscience. 54:1993;893-907.
51. Pasinetti G. M., Hassler M., Stone D. and Finch C. E. (1998) Glial gene expression during ageing in rat striatum and in long-term responses to 6-OHDA lesion. Synapse (in press).
52. Perry V., Matyszak M., Fearn S. Altered antigen expression of microglia in aged rodent CNS. Glia. 7:1993;60-67.
53. Peters A. Age related changes in oligodendrocytes in monkey cerebral cortex. J. comp. Neurol. 37:1996;153-163.
54. Peters A., Leahu D., Moss M.B., McNally K.J. The effects of ageing on area 46 of the frontal cortex of the rhesus monkey. Cerebral Cortex. 6:1994;621-635.
55. Pitsikas N., Algeri S. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. J. Geront. 13:1992;369-373.
56. Poirier J., Hess M., May P.C., Finch C.E. Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Molec. Brain Res. 11:1991;97-106.
57. Poirier J. Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease. Trends Neurosci. 17:1994;525-530.
58. Premkumar D.R., Smith M.A., Richey P.L., Petersen R.B., Castellani R., Kutty R.K., Wiggert B., Perry G., Kalaria R.N. Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem. 65:1995;1399-1402.
59. Rapp P.R., Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. natn. Acad. Sci. U.S.A. 93:1996;9926-9930.
60. Rasmussen T., Schliemann T., Sørensen J.C., Zimmer J., West M.J. Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol. Aging. 17:1996;143-147.
61. 2u-globulin. J. biol. Chem. 262:1987;12821-12825.
62. Roth G.S., Ingram D.K., Joseph J.A. Delayed loss of striatal dopamine receptors during aging of dietarily restricted rats. Brain Res. 300:1984;27-32.
63. Rozovsky I., Finch C.E., Morgan T.E. Age-related activation of microglia and astrocytes: in vitro studies show persistence phenotypes of ageing, increased proliferation, and resistance to down-regulation. Neurobiol. Aging. 19:1998;97-103.
64. Rozovsky I., Laping N.J., O'Callaghan J.P., Finch C.E. Transcriptional regulation of GFAP expression by corticosterone in vitro is influenced by the duration of time in culture and by neuron-astrocyte interactions. Endocrinology. 136:1995;2066-2073.
65. Salat D., Ward A., Kaye J.A., Janowsky J.S. Sex differences in the corpus callosum with aging. Neurobiol. Aging. 18:1997;191-197.
66. Schipper H.E., Stopa E.G. Expression of heme oxygenase-1 in the senescent and Alzheimer-diseased brain. Ann. Neurol. 37:1995;758-768.
67. Senut M.C., Jazat F., Choi N.H., Lamour Y. Protein SP40,40-like immunoreactivity in the rat brain: progressive increase with age. Eur. J. Neurosci. 4:1992;917-928.
68. Shanmugaratnam J., Berg E., Kimerer L., Johnson R.J., Amaratunga A., Schreiber B.M., Fine R.E. Retinal Muller glia secrete apolipoproteins E and J which are efficiently assembled into lipoprotein particles. Molec. Brain Res. 50:1997;113-120.
69. Smith M.A., Kutty R.K., Richey P.L., Yan S.D., Stern D., Chader G.J., Wiggert B., Petersen R.B., Perry G. Hemeoxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease. Am. J. Path. 145:1994;42-47.
70. Smith M.A., Taneda S., Richey P.L., Miyata S., Yan S.D., Stern D., Sayre L.M., Monnier V.M., Perry G. Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc. natn. Acad. Sci. U.S.A. 91:1994;5710-5714.
71. Soong N.W., Hinton D.R., Cortopassi G., Arnheim N. Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nature Genet. 2:1992;318-321.
72. Soong N.W., Dang M.H., Hinton D.R., Arnheim N. Mitochondrial DNA deletions are rare in the free radical-rich retinal environment. Neurobiol. Aging. 17:1996;827-831.
73. Sprott R. L. and Austad S. N. (1996) Animal models for ageing research. In Handbook of the Biology of Ageing, 4th edn, pp. 3-23. Academic, San Diego.
74. Vijayan V.K., Cotman C.W. Lysosomal enzyme changes in young and aged control and entorhinal-lesioned rats. Neurobiol. Aging. 4:1983;12-23.
75. Vitek M.P., Bjattacharya K., Glendening M.J., Stopa E., Vlassara H., Bucala R., Manogue K., Cerami A. Advanced glycation end products contribute to amyloidosis in Alzheimer's disease. Proc. natn. Acad. Sci. U.S.A. 91:1994;4766-4770.
76. Weindruch R. and Walford R. L. (1988) The Retardation of Aging and Disease by Dietary Restriction. C. C. Thomas, Springfield, IL.
77. Weindruch R., Sohal R.S. Caloric intake and ageing. New Engl. J. Med. 337:1997;986-994.
78. Wyss-Coray T., Masliah E., Mallory M., McConologue L., Johnson-Wood K., Lin C., Mucke L. Amyloidogenic role of cytokine TGF-β1 in transgenic mice and in Alzheimer's disease. Nature. 389:1997;603-606.
79. Yoshida T., Goldsmith S., Morgan T.E., Stone D., Finch C.E. Transcription supports age-related increases of GFAP gene expression in the male rat brain. Neurosci. Lett. 215:1996;107-110.
80. Yu B. P. (ed.) (1994) Modulation of Aging Processes by Dietary Restriction. CRC, Boca Raton, FL.
81. Zhang Y., Appelkvist E.-L., Kristensson K., Dallner G. The lipid compositions of different regions of the rat brain during development and ageing. Neurobiol. Aging. 17:1996;869-875.