Stress, Aging, and Neurodegenerative Disorders: Molecular Mechanismsa
Corresponding Author
JORGE BUSCIGLIO
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
J. Busciglio was supported in part by grants from the Alzheimer's Association and the University of Connecticut. G. Gilad was supported by grants from the Israel Science Foundation, the German-Israeli Foundation for Scientific Research and Development, and the Theodore and Vada Stanley Foundation. Olivier Toussaint is a Scientific Collaborator of the FNRS, Belgium and acknowledges the Biomed and Health Research Programme, Concerted Action Programme on Molecular Gerontology, BMH1 CT94 1710, European Union.
Address for correspondence: Dr. J. Busciglio, Department of Pharmacology, MC-6125, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06030. Telephone: (860) 679-3578; Fax: (860) 679-3693; e-mail: [email protected]Search for more papers by this authorJULIE K. ANDERSEN
Division of Biogerontology, Ethel Percy Andrus Gerontology Center, University of Southern California, Los Angeles, California 90089-0191 USA
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorHYMAN M. SCHIPPER
Lady Davis Institute for Medical Research, Jewish General Hospital and McGill University, Montreal QC H3T 1E2, Canada
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorGAD M. GILAD
Laboratory of Neuroscience, Assaf Rarofeli Medical Center, Zrifin 70300, Israel
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorRICHARD McCARTY
Department of Psychology, University of Virginia, Charlottesville, Virginia 22903 USA
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorFULVIO MARZATICO
Institute of Pharmacology, University of Pavia, Pavia, Italy
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorOLIVIER TOUSSAINT
Unit of Cellular Biochemistry and Biology, The University of Namur, FUNDP, Rue de Bruxelles, 61, B-5000 Namur, Belgium
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorCorresponding Author
JORGE BUSCIGLIO
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
J. Busciglio was supported in part by grants from the Alzheimer's Association and the University of Connecticut. G. Gilad was supported by grants from the Israel Science Foundation, the German-Israeli Foundation for Scientific Research and Development, and the Theodore and Vada Stanley Foundation. Olivier Toussaint is a Scientific Collaborator of the FNRS, Belgium and acknowledges the Biomed and Health Research Programme, Concerted Action Programme on Molecular Gerontology, BMH1 CT94 1710, European Union.
Address for correspondence: Dr. J. Busciglio, Department of Pharmacology, MC-6125, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06030. Telephone: (860) 679-3578; Fax: (860) 679-3693; e-mail: [email protected]Search for more papers by this authorJULIE K. ANDERSEN
Division of Biogerontology, Ethel Percy Andrus Gerontology Center, University of Southern California, Los Angeles, California 90089-0191 USA
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorHYMAN M. SCHIPPER
Lady Davis Institute for Medical Research, Jewish General Hospital and McGill University, Montreal QC H3T 1E2, Canada
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorGAD M. GILAD
Laboratory of Neuroscience, Assaf Rarofeli Medical Center, Zrifin 70300, Israel
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorRICHARD McCARTY
Department of Psychology, University of Virginia, Charlottesville, Virginia 22903 USA
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorFULVIO MARZATICO
Institute of Pharmacology, University of Pavia, Pavia, Italy
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this authorOLIVIER TOUSSAINT
Unit of Cellular Biochemistry and Biology, The University of Namur, FUNDP, Rue de Bruxelles, 61, B-5000 Namur, Belgium
Department of Pharmacology, University of Connecticut Health Center, Farmington, Connecticut 06030-6125, USA
Search for more papers by this author
REFERENCES
- 1
Mann, D. A.
1991. Is the pattern of nerve cell loss in aging and Alzheimer's disease a real, or an apparent selectivity? Neurobiol.
Aging
12: 340–343.
- 2
Hall, E.D., P. K. Andrus, J. S. Althaus, et al.
1993. Hydroxyl radical production and lipid peroxidation parallels selective post-ischemic vulnerability in gerbil brain.
J. Neurosci. Res.
34: 107–112.
- 3
Miller, J. D.
1992. Pharmacological intervention in sleep and circadian processes.
Ann. Rep. Med. Chem.
27: 11–19.
- 4
Meijer, J. H., H. Albus, F. F. Weidema, et al.
1993. The effects of glutamate on membrane potential and discharge rate of suprachiasmatic neurons.
Brain. Res.
603: 284–290.
- 5
Lawrence, M. S. & R. M. Sapolsky.
1994. Glucocorticoids accelerate ATP loss following metabolic insults in cultured hippocampal neurons.
Brain Res.
646: 303–306.
- 6
Boisvert, D. P. 1992. In vivo generation of hydroxyl radicals during glutamate exposure. In The Role of Neurotransmitters in Brain Injury. (M. Globus & W. E. Dietrich, Eds.: 361-366. Plenum Press. New York.
- 7
Joseph, J.A., M. Gupta, Z. Han, et al.
1991. The deleterious effects of aging and kainic acid may be selective for similar striatal neuronal populations.
Aging
3: 361–371.
- 8
Palkovits, M., T. Lang, A. Patthy, et al.
1986. Distribution and stress-induced increase of glutamate and aspartate levels in discrete brain nuclei of rats.
Brain Res.
373: 252–257.
- 9
Dickens, B. F., W. B. Weglicki, Y-S. Li, et al.
1992. Magnesium deficiency in vitro enhances free radical-induced intracellular oxidation and cytotoxicity in endothelial cells.
FEBS Lett.
311: 187–191.
- 10
Reiter, R. J., B. Poeggeler, D-X. Tan, et al.
1993. Antioxidant capacity of melatonin: A novel action not requiring a receptor.
Neuroendocrinol. Lett.
15: 103–116.
- 11
Hoyer, S.
1995. Age-related changes in cerebral oxidative metabolism.
Implications for drug therapy. Drugs Aging
6: 210–218.
- 12
Pettegrew, J. W., K. Panchalingam, W. E. Klunk, et al.
1994. Alterations of cerebral metabolism in probable Alzheimer's disease: A preliminary study.
Neurobiol. Aging
15: 117–132.
- 13
Hoyer, S.
1994. Age as risk factor for sporadic dementia of the Alzheimer type? Ann.
N.Y. Acad. Sci.
719: 248–256.
- 14
Coyle, J. T. & P. Puttfarcken.
1993. Oxidative stress, glutamate, and neurodegenerative disorders.
Science
262: 689–695.
- 15
Beal, M. F.
1992. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann.
Neurol.
31: 119–130.
- 16
Kedziora, J. & G. Bartosz.
1988. Down's syndrome: a pathology involving a lack of balance of reactive oxygen species.
Free Radic. Biol. Med.
4: 317–330.
- 17
Brooksbank, B. W. L. & R. Balazs.
1984. Superoxide dismutase, gluthatione peroxidase and lipoperoxidation in Down's syndrome fetal brain.
Dev. Brain Res.
16: 37–44.
- 18
Reynolds, G. & A. Cutts.
1993. Free radical damage in Down's syndrome brain.
Biochem. Soc. Trans.
21: 221S.
- 19
Busciglio, J. & B. A. Yankner.
1995. Apoptosis and increased generation of reactive oxigen species in Down's syndrome neurons in vitro.
Nature
378: 776–779.
- 20
Mecocci, P., U. MacGarvey & M. Flint Beal.
1994. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease.
Ann. Neurol.
36: 747–751.
- 21
Hensley, K.,
et al.
1995. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation.
J. Neurochem.
65: 2146–2156.
- 22
Smith, M., P. Richey Harris, L. Sayre, J. Beckman & G. Perry.
1997. Widespread peroxynitrite-mediated damage in Alzheimer's disease.
J. Neurosci.
17: 2653–2657.
- 23
Mann, D.
1988. The pathological association between Down's syndrome and Alzheimer disease.
Mech. Ageing Dev.
43: 99–136.
- 24
Lemere, A., J. K. Blusztajn, H. Yamaguchi, T. Wisniewski, T. C. Saido & D. Selkoe.
1996. Sequence of deposition of heterogeneous amyloid beta-peptides and apo E in Down syndrome.
Neurobiol. Dis.
3: 16–21.
- 25
Dyrks, T., E. Dyrks, T. Hartmann, C. Masters & K. Beyreuther.
1992. Amyloidogenicity of β/A4 and β/A4-bearing amyloid protein precursor fragments by metal-catalyzed oxidation.
J. Biol. Chem.
267: 18210–18217.
- 26
Behl, C., J. B. Davis, R. Lesley & D. Shubert.
1994. Hydrogen peroxide mediates amyloid b protein toxicity.
Cell
77: 817–827.
- 27
Pachter, J.
1997. Inflammatory mechanisms in Alzheimer disease: The role of beta-amyloid/glial interactions.
Mol. Psychiatry
2: 91–95.
- 28
Carney, J. & A. Carney.
1994. Role of protein oxidation in aging and in age-associated neurodegenerative diseases.
Life Sci.
55: 2097–2103.
- 29
Selkoe, D.
1997. Amyloid β-protein and the genetics of Alzheimer's disease.
J. Biol. Chem.
271: 18295–18298.
- 30
Flint Beal, M.
1992. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann.
Neurol.
31: 119–130.
- 31
Gabuzda, D., J. Busciglio, L. B. Chen, P. Matsudaira & B. A. Yankner.
1994. Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative.
J. Biol. Chem.
269: 13623–13628.
- 32
McGeer, P. L., M. Schulzer & E. G. McGeer.
1996. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease.
Neurology
47: 425–432.
- 33
Sano, M.,
et al.
1997. A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease.
N. Engl. J. Med.
336: 1216–1222.
- 34
Perry, T. L. & D. V. Godin.
1982. Parkinson's disease: A disorder due to nigral glutathione deficiency? Neurosci.
Lett.
33: 305–310.
- 35
Kish, S. J. & C. Morito.
1985. Glutathione peroxidase activity in Parkinson's disease brain.
Neurosci. Lett.
58: 343–346.
- 36
Dexter, D. T, C. J. Carter, F. R. Wells, F. Javoy-Agid, Y. Agid, A. Lees, P. Jenner & C. D. Marsden.
1989. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease.
J. Neurochem.
52: 381–389.
- 37
Sanchez-Ramos, J. R., E. Overik & B. N. Ames.
1994. A marker of oxyradical-mediated DNA-damage is increased in nigro-striatum of Parkinson disease brain.
Neurodegeneration
3: 197–204.
- 38
Andersen, J. K, J. Q. Mo, D. G. Hom, et al.
1996. Effect of buthionine sulfoximine, a synthesis inhibitor of the antioxidant glutathione on the murine nigrostriatal neurons.
J. Neurochem.
67: 2164–2171.
- 39
Yamada, T., P. L. McGeer, K. G. Baimbridge & E. G. McGeer.
1990. Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K.
Brain Res.
526: 303–307.
- 40
Mizuro, Y., S. Ohta, M. Tanaka, et al.
1989. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease.
Biochem. Biophys. Res. Comm.
163: 1450–1455.
- 41
Schapira, A. H.
1993. Mitochondrial complex I deficiency in Parkinson's disease.
Adv. Neurol.
60: 288–291.
- 42
Jenner, P. & A. H. Schapira.
1992. New insights into the cause of Parkinson's disease.
Neurology
42: 2241–2250.
- 43
Youdim, M. B. H. 1994. In Neurodegenerative Diseases. D. B. Calne, Ed.: 251-276. Saunders. Philadelphia.
- 44
Schipper, H. M.
1996. Astrocytes, brain aging and neurodegeneration.
Neurobiol. Aging
17: 467–480.
- 45
Mydlarski, M. B., J. J. Liang & H. M. Schipper.
1993. Role of the cellular stress response in the biogenesis of cysteamine-induced astrocytic inclusions in primary culture.
J. Neurochem.
65: 1755–1765.
- 46
Schipper, H. M., M. B. Mydlarski & X. Wang.
1993. Cysteamine gliopathy in situ: A cellular stress model for the biogenesis of astrocytic inclusions.
J. Neuropathol. Exp. Neurol.
52: 399–410.
- 47
Mydlarski, M. B. & H. M. Schipper.
1993. Stress protein co-localization to autofluorescent astrocytic inclusions in situ and in cysteamine-treated glial cultures.
Brain Res.
627: 113–121.
- 48
Manganaro, F., V. S. Chopra, M. B. Mydlarski, G. Bernatchez & H. M. Schipper.
1995. Redox perturbations in cysteamine-stressed astroglia: Implications for inclusion formation and gliosis in the aging brain.
Free Radic. Biol. Med.
19: 823–835.
- 49
Wang, X., F. Manganaro & H. M. Schipper.
1995. A cellular stress model for the sequestration of redox-active glial iron in the aging and degenerating nervous system.
J. Neurochem.
64: 1868–1877.
- 50
Faucheux, B. A., N. Nillese, P. Damier, et al.
1995. Expression of lactoferrin receptors is increased in the mesencephalon of patients with Parkinson disease.
Proc. Natl. Acad. Sci. USA
92: 9603–9607.
- 51
Leveugle, B., B. A. Faucheux, C. Bouras, et al.
1996. Cellular distribution of the iron-binding protein lactotransferrin in the mesencephalon of Parkinson's disease cases.
Acta Neuropathol.
91: 566–572.
- 52
Bernier, L., G. Bernatchez & H. M. Schipper. 1996. Oxidative stress promotes mitochondrial iron sequestration in cultured astroglia. [abstract]. 593.6. 22nd Society for Neuroscience, Nov. 16-21, 1996. Washington, DC.
- 53
Schipper, H. M., L. Bernier & G. Bernchatez. 1996. Pathological glial-neuronal interaction in Parkinson disease. [abstract] 90. 22nd Society for Neuroscience, Nov. 16-21, 1996. Washington, DC.
- 54
Schipper, H. M., S. Cisse & E. G. Stoppa.
1995. Expression of heme oxygensase-1 in the senescent and Alzheimer-diseased brain.
Ann. Neurol.
37: 758–768.
- 55
Stocker, R.
1990. Induction of heme oxygenase as a defence against oxidative stress.
Free Radic. Res. Comm.
9: 101–112.
- 56
Zhang, J. & C. A. Piantadosi. 1992. Mitochondrial oxidative stress after carbon monoxide hypoxia in the rat brain. J. Clin. Invest. 90: 1193-1199.
- 57
Schipper, H. M., Y. Kotake & E. G. Janzen.
1991. Catechol oxidation by peroxidase-positive astrocytes in primary culture: An electron spin resonance study.
J. Neurosc.
11: 2170–2176.
- 58
Gilad, G. M. & V. H. Gilad.
1992. Polyamines in neurntrauma; ubiquitous molecules in search of a function.
Biochem. Pharmacol.
44: 401–407.
- 59
Gilad, G. M., K. Salame, J. M. Rabey & V. H. Gilad.
1995. Agmatine treatment is neuroprotective in rodent brain injury models.
Life Sci.
58: 41–46.
- 60
Hightower, L. E.
1991. Heat shock, stress proteins, chaperons and proteotoxicity.
Cell
66: 191–197.
- 61
Li, G., S. Regunathan, C. J. Barrow, J. Eshraghi, R. Cooper & D. J. Reis.
1994. Agmatine: An endogenous clonidine-displacing substance in the brain.
Science.
263: 966–969.
- 62
Seiler, N. & F. Dezeure.
1990. Polyamine transport in mammalian cells.
Int. J. Biochem.
22: 211–218.
- 63
Selye, H.
1936. A syndrome produced by diverse nocuous agents.
Nature.
138: 32–37.
- 64
Gallagher, M. & P. R. Rapp.
1997. The use of animal models to study the effects of aging on cognition.
Annu. Rev. Psychol.
48: 339–370.
- 65
Gold, P. E. & W. S. Stone.
1988. Neuroendocrine factors in age-related memory dysfunctions: Studies in animals and humans.
Neurobiol. Aging
9: 709–717.
- 66
Mabry, T. R., P. E. Gold & R. McCarty.
1995. Age-related changes in plasma catecholamine and glucose responses of F-344 rats to a single footshock as used in inhibitory avoidance in training.
Neurobiol. Learning Memory
64: 146–155.
- 67
Mabry, T. R., P. E. Gold & R. McCarty.
1995. Age-related changes in plasma catecholamine responses to acute swim stress.
Neurobiol. Learning Memory
63: 260–268.
- 68
Mabry, T. R., P. E. Gold & R. McCarty.
1996. Age and stress history effects on spatial performance in a swim task in Fischer-344 rats.
Neurobiol. Learning Memory.
66: 1–10.
- 69
McGaugh, J. L.
1989. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage.
Ann. Rev. Neurosc.
12: 255–287.
- 70
Elliott, E. M., & R. M. Sapolsky.
1993. Corticosterone impairs hippocampal neuronal calcium regulation: Possible mediating mechanisms.
Brain Res.
602: 84–90.
- 71
Liu, J. & A. Mori.
1994. Involvement of reactive oxygen species in emotional stress: A hypotesis based on the immobilisation stress-induced oxidative damage and antioxidant defense changes in rat brain, and the effect of antioxidant treatment with reduced glutathione.
Int. J. Stress Manag.
1: 249–263.
- 72
Meaney, M. J., D. H. Aitken, S. Bhatnagar & R. M. Sapolsky.
1991. Postnatal handling attenuates certain neuroendocrine, anatomical, and cognitive dysfunctions associated with aging in female rats.
Neurobiol. Aging
12: 31–38.
- 73
Mullan, M.
1993. The molecular pathology of Alzheimer's disease.
Int. Rev. Psychiatry
5: 351–362.
- 74
Sapolsky, R. M.
1985. A mechanism for glucocorticoid toxicity in the hippocampus: Increased neuronal vulnerability to metabolic insults.
J. Neurosci.
5: 1228–1232.
- 75
Sapolsky, R. M., C. K. Lewis & B. S. McEwen.
1986. The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis.
Endocr. Rev.
7: 285–301.
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