Abstract
This review aims to point out that chronic stress is able to accelerate the appearance of Alzheimer’s disease (AD), proposing the former as a risk factor for the latter. Firstly, in the introduction we describe some human epidemiological studies pointing out the possibility that chronic stress could increase the incidence, or the rate of appearance of AD. Afterwards, we try to justify these epidemiological results with some experimental data. We have reviewed the experiments studying the effect of various stressors on different features in AD animal models. Moreover, we also point out the data obtained on the effect of chronic stress on some processes that are known to be involved in AD, such as inflammation and glucose metabolism. Later, we relate some of the processes known to be involved in aging and AD, such as accumulation of β-amyloid, TAU hyperphosphorylation, oxidative stress and impairement of mitochondrial function, emphasizing how they are affected by chronic stress/glucocorticoids and comparing with the description made for these processes in AD. All these data support the idea that chronic stress could be considered a risk factor for AD.
Acknowledgments
This work was supported by grant SAF-2012-39029 from the Spanish Ministry of Economy and Competitiveness and P10-CTS-6494 (Proyecto de Excelencia of Junta de Andalucia).
Conflicts of interest statement: The authors declare that they have no conflicts of interest.
References
Abercrombie, H.C., Jahn, A.L., Davidson, R.J., Kern, S., Kirschbaum, C., and Halverson, J. (2011). Cortisol’s effects on hippocampal activation in depressed patients are related to alterations in memory formation. J. Psychiatr. Res. 45, 15–23.10.1016/j.jpsychires.2010.10.005Search in Google Scholar PubMed PubMed Central
Abrahám, I., Harkany, T., Horvath, K.M., Veenema, A.H., Penke, B., Nyakas, C., and Luiten P.G. (2000). Chronic corticosterone administration dose-dependently modulates Aβ(1-42)- and NMDA-induced neurodegeneration in rat magnocellular nucleus basalis. J. Neuroendocrinol. 12, 486–494.10.1046/j.1365-2826.2000.00475.xSearch in Google Scholar PubMed
Abramov, A.Y. and Duchen, M.R. (2005). The role of an astrocytic NADPH oxidase in the neurotoxicity of amyloid β peptides. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360, 2309–2314.10.1098/rstb.2005.1766Search in Google Scholar PubMed PubMed Central
Adachi, N., Chen, J., Liu, K., Tsubota, S., and Arai, T. (1998). Dexamethasone aggravates ischemia induced neuronal damage by facilitating the onset of anoxic depolarization and the increase in the intracellular Ca2+ concentration in gerbil hippocampus. J. Cereb. Blood Flow Metab. 18, 274–280.10.1097/00004647-199803000-00005Search in Google Scholar PubMed
Aisa, B., Tordera, R., Lasheras, B., Del Río, J., and Ramírez, M.J. (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32, 256–266.10.1016/j.psyneuen.2006.12.013Search in Google Scholar PubMed
Amatruda, J.M., Livingston, J.N., and Lockwood, D.H. (1985). Cellular mechanisms in selected states of insulin resistance: human obesity, glucocorticoid excess, and chronic renal failure. Diabetes Metab. Rev. 1, 293–317.10.1002/dmr.5610010304Search in Google Scholar PubMed
Argüelles, S., Herrera, A.J., Carreño-Müller, E., de Pablos, R.M., Villarán, R.F., Espinosa-Oliva, A.M., Machado, A., and Cano, J. (2010). Degeneration of dopaminergic neurons induced by thrombin injection in the substantia nigra of the rat is enhanced by dexamethasone: role of monoamine oxidase enzyme. Neurotoxicology 31, 55–66.10.1016/j.neuro.2009.12.001Search in Google Scholar PubMed
Atamna, H. and Frey, W.H. 2nd. (2007). Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimer’s disease. Mitochondrion 7, 297–310.10.1016/j.mito.2007.06.001Search in Google Scholar PubMed
Atif, F., Yousuf, S., and Agrawal, S.K. (2008). Restraint stress-induced oxidative damage and its amelioration with selenium. Eur. J. Pharmacol. 600, 59–63.10.1016/j.ejphar.2008.09.029Search in Google Scholar PubMed
Baglietto-Vargas, D., Medeiros, R., Martinez-Coria, H., LaFerla, F.M., and Green, K.N. (2013). Mifepristone alters amyloid precursor protein processing to preclude amyloid beta and also reduces tau pathology. Biol Psychiatry 74, 357–366.10.1016/j.biopsych.2012.12.003Search in Google Scholar PubMed PubMed Central
Baker, A.F., Briehl, M.M., Dorr, R., and Powis, P. (1996). Decreased antioxidant defence and increased oxidant stress during dexamethasone-induced apoptosis: bcl-2 prevents the loss of antioxidant enzyme activity. Cell Death Diff. 3, 207–213.Search in Google Scholar
Behl, C., Trapp, T., Skutella, T., and Holsboer, F. (1997). Protection against oxidative stress-induced neuronal cell death – a novel role for RU486. Eur. J. Neurosci. 9, 912–920.10.1111/j.1460-9568.1997.tb01442.xSearch in Google Scholar
Belanoff, J.K., Gross, K., Yager, A., and Schatzberg, A.F. (2001). Corticosteroids and cognition. J. Psychiatr. Res. 35, 127–145.10.1016/S0022-3956(01)00018-8Search in Google Scholar
Berent, S., Giordani, B., Foster, N., Minoshima, S., Lajiness-O’Neill, R., Koeppe, R., and Kuhl, D.E. (1999). Neuropsychological function and cerebral glucose utilization in isolated memory impairment and Alzheimer’s disease. J. Psychiatr. Res. 33, 7–16.10.1016/S0022-3956(98)90048-6Search in Google Scholar
Bertram, L. and Tanzi, R.E. (2008). Thirty years of Alzheimer’s disease genetics: the implications of systematic meta-analyses. Nature Rev. Neurosci. 9, 768–778.10.1038/nrn2494Search in Google Scholar
Bishop, N.A., Lu, T., and Yankner, B.A. (2010). Neural mechanisms of ageing and cognitive decline. Nature 464, 529– 535.10.1038/nature08983Search in Google Scholar
Blasko, I., Marx, F., Steiner, E., Hartmann, T., and Grubeck-Loebenstein, B. (1999). TNFalpha plus IFNgamma induce the production of Alzheimer β-amyloid peptides and decrease the secretion of APPs. FASEB J. 13, 63–68.10.1096/fasebj.13.1.63Search in Google Scholar
Bons, N., Jallageas, V., Mestre-Francés, N., Silhol, S., Petter, A., and Delacourte, A. (1995). Microcebus murinus, a convenient laboratory animal model for the study of Alzheimer’s disease. Alzheimer’s Res. 1, 83–87.Search in Google Scholar
Braak, H., Braak, E., and Strothjohann, M. (1994). Abnormally phosphorylated tau protein related to the formation of neurofibrillary tangles and neuropil threads in the cerebral cortex of sheep and goat. Neurosci. Lett. 171, 1–4.10.1016/0304-3940(94)90589-4Search in Google Scholar
Briones, T.L. and Darwish, H. (2014). Decrease in age-related tau hyperphosphorylation and cognitive improvement following vitamin D supplementation are associated with modulation of brain energy metabolism and redox state. Neuroscience 262, 143–55.10.1016/j.neuroscience.2013.12.064Search in Google Scholar
Brunetti, A., Fulham, M.J., Aloj, L., De Souza, B., Nieman, L., Oldfield, E.H., and Di Chiro, G. (1998). Decreased brain glucose utilization in patients with Cushing’s disease. J. Nucl. Med. 39, 786–790.Search in Google Scholar
Burnes, D.P. and Burnette, D.J. (2013). Broadening the etiological discourse on Alzheimer’s disease to include trauma and posttraumatic stress disorder as psychosocial risk factors. Aging Stud. 27, 218–224.10.1016/j.jaging.2013.03.002Search in Google Scholar
Butterfield, D.A., Drake, J., Pocernich, C., and Castegna, A. (2001). Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid β-peptide. Trends Mol. Med. 7, 548–554.10.1016/S1471-4914(01)02173-6Search in Google Scholar
Buxbaum, J.D., Oishi, M., Chen, H.I., Pinkas-Kramarski, R., Jaffe, E.A., Gandy, S.E., and Greengard, P. (1992). Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer β/A4 amyloid protein precursor. Proc. Natl. Acad. Sci. USA 89, 10075–10078.10.1073/pnas.89.21.10075Search in Google Scholar
Calingasan, N.Y., Uchida, K., and Gibson, G.E. (1999). Protein-bound acrolein: a novel marker of oxidative stress in Alzheimer’s disease, J. Neurochem. 72, 751–756.10.1046/j.1471-4159.1999.0720751.xSearch in Google Scholar
Cao, K., Chen-Plotkin, A.S., Plotkin, J.B., and Wang, L-S. (2010). Age-correlated gene expression in normal and neurodegenerative human brain tissues. PLoS One 5, pii:e13098.Search in Google Scholar
Cardoso, S.M., Santana, I., Swerdlow, R.H., and Oliveira, C.R. (2004). Mitochondria dysfunction of Alzheimer’s disease cybrids enhances Aβ toxicity. J. Neurochem. 89, 1417–1426.10.1111/j.1471-4159.2004.02438.xSearch in Google Scholar
Carlo, P., Violani, E., Del Rio, M., Olasmaa, M., Santagati, S., Maggi, A., and Picotti, G.B. (1996). Monoamine oxidase B expression is selectively regulated by dexamethasone in cultured rat astrocytes. Brain Res. 711, 175–183.10.1016/0006-8993(95)01353-9Search in Google Scholar
Carreño-Müller, E., Herrera, A.J., de Pablos, R.M., Tomás-Camardiel, M., Venero, J.L., Cano, J., and Machado, A. (2003). Thrombin induces in vivo degeneration of nigral dopaminergic neurones along with the activation of microglia. J. Neurochem. 84, 1201–1214.10.1046/j.1471-4159.2003.01634.xSearch in Google Scholar
Carroll, J.C., Iba, M., Bangasser, D.A., Valentino, R.J., James, M.J., Brunden, K.R., Lee, V.M., and Trojanowski, J.Q. (2011). Chronic stress exacerbates tau pathology, neurodegeneration, and cognitive performance through a corticotropin-releasing factor receptor-dependent mechanism in a transgenic mouse model of tauopathy. J Neurosci. 31, 14436–14449.10.1523/JNEUROSCI.3836-11.2011Search in Google Scholar
Castaño, A., Herrera, A.J., Cano, J., and Machado, A. (1998). Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J. Neurochem. 70, 1584–1592.10.1046/j.1471-4159.1998.70041584.xSearch in Google Scholar
Castaño, A., Herrera, A.J., Cano, J., and Machado, A. (2002). The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-α, IL-1β and IFN-γ. J. Neurochem. 81, 150–157.10.1046/j.1471-4159.2002.00799.xSearch in Google Scholar
Catania, C., Sotiropoulos, I., Silva, R., Onofri, C., Breen, K.C., Sousa, N., and Almeida, O.F. (2009). The amyloidogenic potential and behavioral correlates of stress. Mol. Psychiatry 14, 95–105.10.1038/sj.mp.4002101Search in Google Scholar
Ceballos-Picot, I., Nicole, A., Clement, M., Bourre, J.M., and Sinet, P.M. (1992). Age-related changes in antioxidant enzymes and lipid peroxidation in brains of control and transgenic mice overexpressing copper-zinc superoxide dismutase, Mutat. Res. 275, 281–293.10.1016/0921-8734(92)90032-KSearch in Google Scholar
Coluccia, D., Wolf, O.T., Kollias, S., Roozendaal, B., Forster, A., and de Quervain D.J. (2008). Glucocorticoid therapy-induced memory deficits: acute versus chronic effects. J. Neurosci. 28, 3474–3478.10.1523/JNEUROSCI.4893-07.2008Search in Google Scholar PubMed PubMed Central
Copeland, J.M., Cho, J., Lo, T. Jr., Hur, J.H., Bahadorani, S., Arabyan, T., Rabie, J., Soh, J., and Walker, D.W. (2009). Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 19, 1591–1598.10.1016/j.cub.2009.08.016Search in Google Scholar PubMed
Cork, L.C., Powers, R.E., Selkoe, D.J., Davies, P., Geyer, J.J., and Price, D.L. (1988). Neurofibrillary tangles and senile plaques in aged bears. J. Neuropathol. Exp. Neurol. 47, 629–641.10.1097/00005072-198811000-00006Search in Google Scholar PubMed
Croisier, E., Moran, L.B., Dexter, D.T., Pearce, R.K., and Graeber, M.B. (2005). Microglial inflammation in the parkinsonian substantia nigra: relationship to α-synuclein deposition. J. Neuroinflammation. 3, 2–14.10.1186/1742-2094-2-14Search in Google Scholar PubMed PubMed Central
Csernansky, J.G., Dong, H., Fagan, A.M., Wang, L., Xiong, C., Holtzman, D.M., and Morris, J.C. (2006). Plasma cortisol and progression of dementia in subjects with Alzheimer-type dementia. Am. J. Psychiatry 163, 2164–2169.10.1176/ajp.2006.163.12.2164Search in Google Scholar PubMed PubMed Central
Cuadrado-Tejedor, M., Cabodevilla, J.F., Zamarbide, M., Gómez-Isla, T., Franco, R. and Perez-Mediavilla, A. (2013). Age-related mitochondrial alterations without neuronal loss in the hippocampus of a transgenic model of Alzheimer’s disease. Curr Alzheimer Res. 10, 390–405.10.2174/1567205011310040005Search in Google Scholar PubMed
Cui, B., Zhu, L. She, X., Wu, M., Ma, Q., Wang, T., Zhang, N., Xu, C., Chen, X., An, G., et al. (2012). Chronic noise exposure causes persistence of tau hyperphosphorylation and formation of NFT tau in the rat hippocampus and prefrontal cortex. Exp Neurol. 238, 122–129.10.1016/j.expneurol.2012.08.028Search in Google Scholar PubMed
de Leon, M.J., Ferris, S.H., George, A.E., Reisberg, B., Christman, D.R., Kricheff, I.I., and Wolf, A.P. (1983a). Computed tomography and positron emission transaxial tomography evaluations of normal aging and Alzheimer’s disease. J. Cereb. Blood Flow Metab. 3, 391–394.10.1038/jcbfm.1983.57Search in Google Scholar PubMed
de Leon, M.J., Ferris, S.H., George, A.E., Christman, D.R., Fowler, J.S., Gentes, C., Reisberg, B., Gee, B., Emmerich, M., Yonekura, Y., et al. (1983b). Positron emission tomographic studies of aging and Alzheimer disease. AJNR Am. J. Neuroradiol. 4, 568–571.Search in Google Scholar
de Leon, M.J., McRae, T., Rusinek, H., Convit, A., De Santi, S., Tarshish, C., Golomb, J., Volkow, N., Daisley, K., Orentreich, N., et al. (1997). Cortisol reduces hippocampal glucose metabolism in normal elderly, but not in Alzheimer’s disease. J. Clin. Endocrinol. Metab. 82, 3251–3259.Search in Google Scholar
de Pablos, R.M., Herrera, A.J., Villarán, R.F., Cano, J., and Machado, A. (2005). Dopamine-dependent neurotoxicity of lipopolysaccharide in substantia nigra. FASEB J. 19, 407–409.10.1096/fj.04-2153fjeSearch in Google Scholar PubMed
de Pablos, R.M., Villarán, R.F., Argüelles, S., Herrera, A.J., Venero, J.L., Ayala, A., Cano, J., and Machado, A. (2006). Stress increases vulnerability to inflammation in the rat prefrontal cortex. J. Neurosci. 26, 5709–5719.10.1523/JNEUROSCI.0802-06.2006Search in Google Scholar PubMed PubMed Central
de Pablos, R.M., Herrera, A.J., Espinosa-Oliva, A.M., Sarmiento, M., Muñoz, M.F., Machado, A., and Venero, J.L. (2014). Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation. J Neuroinflammation 11, 34.10.1186/1742-2094-11-34Search in Google Scholar
de Quervain, D.J., Poirier, R., Wollmer, M.A., Grimaldi, L.M., Tsolaki, M., Streffer, J.R., Hock, C., Nitsch, R.M., Mohajeri, M.H., and Papassotiropoulos, A. (2004). Glucocorticoid-related genetic susceptibility for Alzheimer’s disease. Hum. Mol. Genet. 13, 47–52.10.1093/hmg/ddg361Search in Google Scholar
Desgranges, B., Baron, J.C., de la Sayette, V., Petit-Taboué, M.C., Benali, K., Landeau, B., Lechevalier, B., and Eustache, F. (1998). The neural substrate of memory systems impairment in Alzheimer’s disease. A PET study of resting brain glucose utilization. Brain 121, 611–631.10.1093/brain/121.4.611Search in Google Scholar
Dhikav, V. and Anand, K.S. (2007). Glucocorticoids may initiate Alzheimer’s disease: a potential therapeutic role for mifepristone (RU-486). Med. Hypotheses 68, 1088–1092.10.1016/j.mehy.2006.09.038Search in Google Scholar
Dodart, J.C., Mathis, C., Bales, K.R., Paul, S.M., and Ungerer, A. (1999). Early regional cerebral glucose hypometabolism in transgenic mice overexpressing the V717F beta-amyloid precursor protein. Neurosci. Lett. 277, 49–52.10.1016/S0304-3940(99)00847-2Search in Google Scholar
Dong, H., Goico, B., Martin, M., Csernansky, C.A., Bertchume, A., and Csernansky, J.G. (2004). Modulation of hipocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress. Neuroscience 127, 601–609.10.1016/j.neuroscience.2004.05.040Search in Google Scholar PubMed
Dong, H., Yuede, C.M., Yoo, H.S., Martin, M.V., Deal, C., Mace, A.G., and Csernansky, J.G. (2008). Corticosterone and related receptor expression are associated with increased β-amyloid plaques in isolated Tg2576 mice. Neuroscience 155, 154–163.10.1016/j.neuroscience.2008.05.017Search in Google Scholar PubMed PubMed Central
Du, J., Wang, Y., Hunter, R., Wei, Y., Blumenthal, R., Falke, C., Khairova, R., Zhou, R., Yuan, P., Machado-Vieira, R., et al. (2009). Dynamic regulation of mitochondrial function by glucocorticoids. Proc. Natl. Acad. Sci. USA 106, 3543–3548.10.1073/pnas.0812671106Search in Google Scholar PubMed PubMed Central
Dunn, A.J., Wang, J., and Ando, T. (1999). Effects of cytokines on cerebral neurotransmission. Comparison with the effects of stress. Adv. Exp. Med. Biol. 461, 117–127.10.1007/978-0-585-37970-8_8Search in Google Scholar PubMed
Edenfield, T.M. and Saeed, S.A. (2012). An update on mindfulness meditation as a self-help treatment for anxiety and depression. Psychol. Res. Behav. Manag. 5, 131–141.10.2147/PRBM.S34937Search in Google Scholar PubMed PubMed Central
Endo, Y., Nishimura, J., and Kimura, F. (1994). Adrenalectomy increases local cerebral blood flow in the rat hippocampus. Pflüger’s Arch. 426, 83–88.10.1007/BF00374770Search in Google Scholar
Epel, E.S., Blackburn, E.H., Lin, J., Dhabhar, F.S., Adler, N.E., Morrow, J.D., and Cawthon, R.M. (2004). Accelerated telomere shortening in response to life stress. Proc. Natl. Acad. Sci. USA 101, 17312–17315.10.1073/pnas.0407162101Search in Google Scholar
Espinosa-Oliva, A.M., de Pablos, R.M., Villarán, R.F., Argüelles, S., Venero, J.L., Machado, A., and Cano, J. (2011). Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol. Aging 32, 85–102.10.1016/j.neurobiolaging.2009.01.012Search in Google Scholar
Filipcik, P., Novak, P., Mravec, B., Ondicova, K., Krajciova, G., Novak, M., and Kvetnansky, R. (2012). Tau protein phosphorylation in diverse brain areas of normal and CRH deficient mice: up-regulation by stress. Cell Mol. Neurobiol. 32, 837–845.10.1007/s10571-011-9788-9Search in Google Scholar
Fontella, F.U., Siqueira, I.R., Vasconcellos, A.P., Tabajara, A.S., Netto, C.A., and Dalmaz, C. (2005). Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem. Res. 30, 105–111.10.1007/s11064-004-9691-6Search in Google Scholar
Freo, U., Holloway, H.W., Kalogeras, K., Rapoport, S.I., and Soncrant, T.T. (1992). Adrenalectomy or metyrapone-pretreatment abolishes cerebral metabolic responses to the serotonin agonist 1-(2,5-dimethoxy-4-iodophenyl)-2-aminopropane (DOI) in the hippocampus. Brain Res. 586, 256–264.10.1016/0006-8993(92)91634-QSearch in Google Scholar
Fulham, M.J., Brunetti, A., Aloj, L., Raman, R., Dwyer, A.J., and Di Chiro, G. (1995). Decreased cerebral glucose metabolism in patients with brain tumors: an effect of corticosteroids. J. Neurosurg. 83, 657–664.10.3171/jns.1995.83.4.0657Search in Google Scholar PubMed
Fuster-Matanzo, A., Llorens-Martin, M., Jurado-Arjona, J., Avila, J., and Hernandez, F. (2012). Tau protein and adult hippocampal neurogenesis. Front. Neurosci. 6, 104.10.3389/fnins.2012.00104Search in Google Scholar PubMed PubMed Central
Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F., et al. (1995). Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373, 523–527.10.1038/373523a0Search in Google Scholar PubMed
Ghoumari, A.M., Dusart, I., El-Etr, M., Tronche, F., Sotelo, C., Schumacher, M., and Baulieu, E.E. (2003). Mifepristone (RU486) protects Purkinje cells from cell death in organotypic slice cultures of postnatal rat and mouse cerebellum. Proc. Natl. Acad. Sci. USA 100, 7953–7958.10.1073/pnas.1332667100Search in Google Scholar PubMed PubMed Central
Gibson, G.E., Ratan, R.R., and Beal, M.F. (2008). Mitochondria and oxidative stress in neurodegenerative disorders. Preface. Ann. NY Acad. Sci. 1147, xi-xii.Search in Google Scholar
Gillardon, F., Rist, W., Kussmaul, L., Vogel, J., Berg, M., Danzer, K., Kraut, N., and Hengerer, B. (2007). Proteomics 7, 605–616.10.1002/pmic.200600728Search in Google Scholar
Goodman, Y., Bruce, A.J., Cheng, B., and Mattson, M.P. (1996). Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid β-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836–1844.10.1046/j.1471-4159.1996.66051836.xSearch in Google Scholar
Goosens, K.A. and Sapolsky, R.M. (2007). Stress and Glucocorticoid Contributions to Normal and Pathological Aging, in Brain Aging: Models, Methods, and Mechanisms.D. R. Riddle ed., chapter 13. (CRC Press, Boca Raton).Search in Google Scholar
Gotz, J., Xia, D., Leinenga, G., Chew, Y.L., and Nicholas, H. (2013). What renders TAU toxic. Front. Neurol. 4, 72.10.3389/fneur.2013.00072Search in Google Scholar
Green, K.N., Billings, L.M., Roozendaal, B., McGaugh, J.L., and LaFerla, F.M. (2006). Glucocorticoids increase amyloid-β and tau pathology in a mouse model of Alzheimer’s disease. J. Neurosci. 26, 9047–9056.10.1523/JNEUROSCI.2797-06.2006Search in Google Scholar
Guo, J.T., Yu, J., Grass, D., de Beer, F.C., and Kindy, M.S. (2002). Inflammation-dependent cerebral deposition of serum amyloid a protein in a mouse model of amyloidosis. J. Neurosci. 22, 5900–5909.10.1523/JNEUROSCI.22-14-05900.2002Search in Google Scholar
Harris-White, M.E., Chu, T., Miller, S.A., Simmons, M., Teter, B., Nash, D., Cole, G.M., and Frautschy, S.A. (2001). Estrogen (E2) and glucocorticoid (Gc) effects on microglia and Aβ clearance in vitro and in vivo. Neurochem. Int. 39, 435–448.10.1016/S0197-0186(01)00051-1Search in Google Scholar
Härtig, W., Klein, C., Brauer, K.,. Schüppel, K.F, Arendt, T., Brückner, G., and Bigl, V. (2000). Abnormally phosphorylated protein tau in the cortex of aged individuals of various mammalian orders. Acta Neuropathol. 100, 305–312.10.1007/s004010000183Search in Google Scholar
Härtig, W., Klein, C., Brauer, K., Schüppel, K.F., Arendt, T., Bigl, V., and Brückner, G. (2001). Hyperphosphorylated protein tau is restricted to neurons devoid of perineuronal nets in the cortex of aged bison. Neurobiol. Aging, 22, 25–33.10.1016/S0197-4580(00)00179-2Search in Google Scholar
Härtig, W., Oklejewicz, M., Strijkstra, A.M, Boerema, A.S., Stieler, J., and Arendt, T. (2005). Phosphorylation of the tau protein sequence 199-205 in the hippocampal CA3 region of Syrian hamsters in adulthood and during aging. Brain Res. 1056, 100–104.10.1016/j.brainres.2005.07.017Search in Google Scholar PubMed
Hashiguchi, M. and Hashiguchi, Y. (2013). Kinase-kinase interaction and modulation of tau phosphorylation. Int. Rev. Cell. Mol. Biol. 300, 121–160.10.1016/B978-0-12-405210-9.00004-7Search in Google Scholar PubMed
Hebert, L.E., Scherr, P.A., Bienias, J.L., Bennett, D.A., and Evans, D.A. (2003). Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch. Neurol. 60, 1119–1122.10.1001/archneur.60.8.1119Search in Google Scholar PubMed
Hensley, K., Carney, J.M., Mattson, M.P., Aksenova, M., Harris, M., Wu, J.F., Floyd, R.A., and Butterfield, D.A. (1994). A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 3270–3274.10.1073/pnas.91.8.3270Search in Google Scholar PubMed PubMed Central
Hernández-Romero, M.C., Argüelles, S., Villarán, R.F., de Pablos, R.M., Delgado-Cortés, M.J., Santiago, M., Herrera, A.J., Cano, J., and Machado, A. (2008). Simvastatin prevents the inflammatory process and the dopaminergic degeneration induced by the intranigral injection of lipopolysaccharide. J. Neurochem. 105, 445–459.10.1111/j.1471-4159.2007.05148.xSearch in Google Scholar PubMed
Herrera, A.J., Castaño, A., Venero, J.L., Cano, J., and Machado, A. (2000). The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol. Dis. 7, 429–447.10.1006/nbdi.2000.0289Search in Google Scholar PubMed
Herrera, A. J., Tomás-Camardiel, M., Venero, J.L., Cano, J., and Machado, A. (2005). Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J. Neural. Transm. 112, 111–119.10.1007/s00702-004-0121-3Search in Google Scholar PubMed
Herrera, A.J., de Pablos, R.M., Carreño-Müller, E., Villarán, R.F., Venero, J.L., Tomás-Camardiel, M., Cano, J., and Machado, A. (2008). The intrastriatal injection of thrombin in rat induced a retrograde apoptotic degeneration of nigral dopaminergic neurons through synaptic elimination. J. Neurochem. 105, 750–762.10.1111/j.1471-4159.2007.05170.xSearch in Google Scholar PubMed
Hirai, K., Aliev, G., Nunomura, A., Fujioka, H., Russell, R.L., Atwood, C.S., Johnson, A.B., Kress, Y., Vinters, H.V., Tabaton, M., et al. (2001). Mitochondrial abnormalities in Alzheimer’s disease. J. Neurosci. 21, 3017–3023.10.1523/JNEUROSCI.21-09-03017.2001Search in Google Scholar
Hirose, Y., Imai, Y., Nakajima, K., Takemoto, N., Toya, S., and Kohsaka, S. (1994). Glial conditioned medium alters the expression of amyloid precursor protein in SH-SY5Y neuroblastoma cells. Biochem. Biophys. Res. Commun. 198, 504–509.10.1006/bbrc.1994.1074Search in Google Scholar PubMed
Horner, H.C., Packan, D.R., and Sapolsky, R.M. (1990). Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology 52, 57–64.10.1159/000125539Search in Google Scholar PubMed
Ibáñez, V., Pietrini, P., Alexander, G.E., Furey, M.L., Teichberg, D., Rajapakse, J.C., Rapoport, S.I., Schapiro, M.B., and Horwitz, B. (1998). Regional glucose metabolic abnormalities are not the result of atrophy in Alzheimer’s disease. Neurology 50, 1585–1593.10.1212/WNL.50.6.1585Search in Google Scholar
Iqbal, K. and Grundke-Iqbal, I. (2008). Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention. J. Cell Mol. Med. 12, 38–55.10.1111/j.1582-4934.2008.00225.xSearch in Google Scholar
Iuchi, T., Akaike, M., Mitsui, T., Ohshima, Y., Shintani, Y., Azuma, H., and Matsumoto, T. (2003). Glucocorticoid excess induces superoxide production in vascular endothelial cells and elicits vascular endothelial dysfunction. Circ. Res. 92, 81–87.10.1161/01.RES.0000050588.35034.3CSearch in Google Scholar
Jang, Y.C. and Remmen, V.H. (2009). The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp. Gerontol. 44, 256–260.10.1016/j.exger.2008.12.006Search in Google Scholar
Jeong, Y.H., Park, C.H., Yoo, J., Shin, K.Y., Ahn, S.M., Kim, H.S., Lee, S.H., Emson, P.C., and Suh, Y.H. (2006). Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APPV717I-CT100 transgenic mice, an Alzheimer’s disease model. FASEB J. 20, 729–731.10.1096/fj.05-4265fjeSearch in Google Scholar
Johansson, L., Guo, X., Waern, M., Ostling, S., Gustafson, D., Bengtsson, C., and Skoog, I. (2010). Midlife psychological stress and risk of dementia: a 35-year longitudinal population study. Brain 133, 2217–2224.10.1093/brain/awq116Search in Google Scholar
Jorm, A.F. and Jolley, D. (1998). The incidence of dementia: a meta-analysis. Neurology 51, 728–733.10.1212/WNL.51.3.728Search in Google Scholar
Kadekaro, M., Ito, M., and Gross, P.M. (1988). Local cerebral glucose utilization is increased in acutely adrenalectomized rats. Neuroendocrinology 47, 329–334.10.1159/000124933Search in Google Scholar
Kang, J.E., Cirrito, J.R., Dong, H., Csernansky, J.G., and Holtzman, D.M. (2007). Acute stress increases interstitial fluid amyloid-β via corticotropin-releasing factor and neuronal activity. Proc. Natl. Acad. Sci. USA 104, 10673–10678.10.1073/pnas.0700148104Search in Google Scholar
Kashif, S.M., Zaidi, R., Al-Qirim, T.M, Hoda, M.N., and Banu, N. (2003). Modulation of restraint stress induced oxidative changes in rats by antioxidant vitamins. J. Nutrition Biochem. 14, 633–636.10.1016/S0955-2863(03)00117-7Search in Google Scholar
Kennedy, A.M., Rossor, M.N., and Frackowiak, R.S. (1995). Positron emission tomography in familial Alzheimer disease. Alzheimer Dis. Assoc. Disord. 9, 17–20.10.1097/00002093-199505000-00005Search in Google Scholar PubMed
Khan, S.M., Cassarino, D.S., Abramova, N.N., Keeney, P.M., Borland, M.K., Trimmer, P.A., Krebs, C.T., Bennett, J.C., Parks, J.K., Swerdlow, R.H., et al. (2000). Alzheimer’s disease cybrids replicate β-amyloid abnormalities through cell death pathways. Ann. Neurol. 48, 148–155.10.1002/1531-8249(200008)48:2<148::AID-ANA3>3.0.CO;2-7Search in Google Scholar
Kim, J.J., Foy, M.R., and Thompson, R.F. (1996). Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. USA 93, 4750–4753.10.1073/pnas.93.10.4750Search in Google Scholar
Kim, W.G., Mohney, R.P., Wilson, B., Jeohn, G.H., Liu, B., and Hong, J.S. (2000). Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20, 6309–6316.10.1523/JNEUROSCI.20-16-06309.2000Search in Google Scholar
Kimura, T., Yamashita, S., Fukuda, T., Park, J.M., Murayama, M., Mizoroki, T.,Yoshiike, Y., Sahara, N., and Takashima, A. (2007). Hyperphosphorylated TAU in parahippocampal cortex impairs place learning in aged mice expressing wild-type human TAU. EMBO J. 26, 5143–5152.10.1038/sj.emboj.7601917Search in Google Scholar
Kitazawa, M., Oddo, S., Yamasaki, T.R., Green, K.N., and LaFerla, F.M. (2005). Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer’s disease. J. Neurosci. 25, 8843–8853.10.1523/JNEUROSCI.2868-05.2005Search in Google Scholar
Kuhl, D.E., Metter, E.J., Riege, W.H., and Phelps, M.E. (1982). Effects of human aging on patterns of local cerebral glucose utilization determined by the [18F]fluorodeoxyglucose method. J. Cereb. Blood Flow Metab. 2, 163–171.10.1038/jcbfm.1982.15Search in Google Scholar
Kulstad, J.J., McMillan, P.J., Leverenz, J.B., Cook, D.G., Green, P.S., Peskind, E.R., Wilkinson, C.W., Farris, W., Mehta, P.D., and Craft, S. (2005). Effects of chronic glucocorticoid administration on insulin-degrading enzyme and amyloid-β peptide in the aged macaque. J. Neuropathol. Exp. Neurol. 64, 139–146.10.1093/jnen/64.2.139Search in Google Scholar
Landfield, P.W., Blalock, E.M., Chen, K-C., and Porter, N.M. (2007). A new glucocorticoid hypothesis of brain aging: implications for Alzheimer’s disease. Curr. Alzheimer Res. 4, 205–212.10.2174/156720507780362083Search in Google Scholar
Landgraf, R., Mitro, A., and Hess, J. (1978). Regional net uptake of 14C-glucose by rat brain under the influence of corticosterone. Endocrinol. Exp. 12, 119–129.Search in Google Scholar
Lee, K.W., Kim, J.B., Seo, J.S., Kim, T.K., Im, J.Y., Baek, I.S., Kim, K.S., Lee, J.K., and Han, P.L. (2009). Behavioral stress accelerates plaque pathogenesis in the brain of Tg2576 mice via generation of metabolic oxidative stress. J. Neurochem. 108, 165–175.10.1111/j.1471-4159.2008.05769.xSearch in Google Scholar
Leza, J.C., Salas, E., Sawicki, G., Russell, J.C., and Radomski, M.W. (1998). The effects of stress on homeostasis in JCR-LA-cp rats: the role of nitric oxide. J. Pharmacol. Exp. Ther. 286, 1397–1403.Search in Google Scholar
Li, W.Z., Li, W.P., Yao, Y.Y., Zhang, W., Yin, Y.Y., Wu, G.C., and Gong, H.L. (2010). Glucocorticoids increase impairments in learning and memory due to elevated amyloid precursor protein expression and neuronal apoptosis in 12-month old mice. Eur. J. Pharmacol. 628, 108–115.10.1016/j.ejphar.2009.11.045Search in Google Scholar
Li, Z., Ma, L., Kulesskaya, N., Võikar, V., and Tian, L. (2014). Microglia are polarized to M1 type in high-anxiety inbred mice in response to lipopolysaccharide challenge. Brain Behav Immun 38, 237–248.10.1016/j.bbi.2014.02.008Search in Google Scholar
Liang, W.S., Reiman, E.M., Valla, J., Dunckley, T., Beach, T.G., Grover, A., Niedzielko, T.L., Schneider, L.E., Mastroeni, D., Caselli, R., et al. (2008). Alzheimer’s disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl Acad. Sci. USA 105, 4441–4446.10.1073/pnas.0709259105Search in Google Scholar
Liu, J., Wang, X., Shigenaga, M., Yeo, H., Mori, A., and Ames, B. (1996). Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J. 10, 1532–1538.10.1096/fasebj.10.13.8940299Search in Google Scholar
Loerch, P.M., Lu, T., Dakin, K.A., Vann, J.M., Isaacs, A., Geula, C., Wang, J., Pan, Y., Gabuzda, D.H., Li, C., et al. (2008). Evolution of the aging brain transcriptome and synaptic regulation. PLoS One 3, e3329.10.1371/journal.pone.0003329Search in Google Scholar
Lovell, M.A. and Markesbery, W.R. (2007). Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer’s disease. Nucleic Acids Res. 35, 7497–7504.10.1093/nar/gkm821Search in Google Scholar
Lu, T., Pan, Y., Kao, S.Y., Li, C., Kohane, I., Chan, J., and Yankner, B.A. (2004). Gene regulation and DNA damage in the ageing human brain. Nature 429, 883–891.10.1038/nature02661Search in Google Scholar
MacPherson, A., Dinkel, K., and Sapolsky, R. (2005). Glucocorticoids worsen excitotoxin-induced expression of pro-inflammatory cytokines in hipocampal cultures. Exp. Neurol. 194, 376–383.10.1016/j.expneurol.2005.02.021Search in Google Scholar
Madrigal, J.L., Hurtado, O., Moro, M.A., Lizasoain, I., Lorenzo, P., Castrillo, A., Boscá, L., and Leza, J.C. (2002). The increase in TNF-α levels is implicated in NF-κB activation and inducible nitric oxide synthase expression in brain cortex after immobilization stress. Neuropsychopharmacology 26, 155–163.10.1016/S0893-133X(01)00292-5Search in Google Scholar
Madrigal, J.L, Garcia-Bueno, B., Caso, J.R., Perez-Nievas, B.G., and Leza, J.C. (2006). Stress-induced oxidative changes in brain. CNS Neurol. Disord. Drug Targets 5, 561–568.10.2174/187152706778559327Search in Google Scholar
Magarinos, A.M. and McEwen, B.S. (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement ofglucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69, 89–98.10.1016/0306-4522(95)00259-LSearch in Google Scholar
Mailliet, F., Qi, H., Rocher, C., Spedding, M., Svenningsson, P., and Jay, T.M. (2008). Protection of stress-induced impairment of hippocampal/prefrontal LTP through blockade of glucocorticoid receptors: implication of MEK signaling. Exp. Neurol. 211, 593–596.10.1016/j.expneurol.2008.02.030Search in Google Scholar
Mancuso, M., Orsucci, D., Siciliano, G., and Murri, L. (2008). Mitochondria, mitochondrial DNA and Alzheimer’s disease. What comes first? Curr. Alzheimer Res. 5, 457–468.10.2174/156720508785908946Search in Google Scholar
Manoli, I., Le, H., Alesci, S., McFann, K.K., Su, Y.A., Kino, T., Chrousos, G.P., and Blackman, M.R. (2005). Monoamine oxidase-A is a major target gene for glucocorticoids in human skeletal muscle cells. FASEB J. 19, 1359–1361.10.1096/fj.04-3660fjeSearch in Google Scholar
Marcus, D.L. and Freedman, M.L. (1997). Decreased brain glucose metabolism in microvessels from patients with Alzheimer’s disease. Ann. NY Acad. Sci. 826, 248–253.10.1111/j.1749-6632.1997.tb48476.xSearch in Google Scholar
Mark, R.J., Pang, Z., Geddes, J.W., Uchida, K., and Mattson, M.P. (1997). Amyloid beta-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046–1054.10.1523/JNEUROSCI.17-03-01046.1997Search in Google Scholar
Masters, C.L. and Beyreuther, K. (1998). Alzheimer’s disease. Br. Med. J. 316, 446–448.10.1136/bmj.316.7129.446Search in Google Scholar
Matsuoka, Y., Picciano, M., La Francois, J., and Duff, K. (2001). Fibrillar β-amyloid evokes oxidative damage in a transgenic mouse model of Alzheimer’s disease. Neuroscience 104, 609–613.10.1016/S0306-4522(01)00115-4Search in Google Scholar
Mazanetz, M.P. and Fischer, P.M. (2007). Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases. Nat. Rev. Drug Discov. 6, 464–479.10.1038/nrd2111Search in Google Scholar
McClelland, D.C., Patel, V., Brown, D., and Kelner, S.P. Jr. (1991). The role of affiliative loss in the recruitment of helper cells among insulin-dependent diabetics. Behav Med. 17, 5–14.10.1080/08964289.1991.9937547Search in Google Scholar
McCullers, D.L., Sullivan, P.G., Scheff, S.W., and Herman, J.P. (2002). Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat. Neuroscience 109, 219–230.10.1016/S0306-4522(01)00477-8Search in Google Scholar
McGeer, E.G. and McGeer, P.L. (1998). The importance of inflammatory mechanisms in Alzheimer disease. Exp. Gerontol. 33, 371–378.10.1016/S0531-5565(98)00013-8Search in Google Scholar
Medina, M. and Avila, J. (2014). The role of extracellular Tau in the spreading of neurofibrillary pathology. Front Cell Neurosci. 8:113.Search in Google Scholar
Meguro, K., LeMestric, C., Landeau, B., Desgranges, B., Eustache, F., and Baron, J.C. (2001). Relations between hypometabolism in the posterior association neocortex and hippocampal atrophy in Alzheimer’s disease: a PET/MRI correlative study. J. Neurol. Neurosurg. Psychiatry 71, 315–321.10.1136/jnnp.71.3.315Search in Google Scholar
Mehta, P.D., Mehta, S.P., Fedor, B., Patrick, B.A., Emmerling, M., and Dalton, A.J. (2003). Plasma amyloid protein 1–42 levels are increased in old Down syndrome but not in young Down syndrome. Neurosci. Lett. 342, 155–158.10.1016/S0304-3940(03)00275-1Search in Google Scholar
Meier-Ruge, W. and Bertoni-Freddari, C. (1996). The significance of glucose turnover in the brain in the pathogenetic mechanisms of Alzheimer’s disease. Rev. Neurosci. 7, 1–19.10.1515/REVNEURO.1996.7.1.1Search in Google Scholar
Meier-Ruge, W.A. and Bertoni-Freddari, C. (1997). Pathogenesis of decreased glucose turnover and oxidative phosphorylation in ischemic and trauma-induced dementia of the Alzheimer type. Ann. NY Acad.Sci. 826, 229–241.10.1111/j.1749-6632.1997.tb48474.xSearch in Google Scholar
Mesulam, M.M. (1999). Neuroplasticity failure in Alzheimer’s disease: bridging the gap between plaques and tangles. Neuron 24, 521–529.10.1016/S0896-6273(00)81109-5Search in Google Scholar
Miller, J.A., Oldham, M.C., and Geschwind, D.H. (2008). A systems level analysis of transcriptional changes in Alzheimer’s disease and normal aging. J. Neurosci. 28, 1410–1420.10.1523/JNEUROSCI.4098-07.2008Search in Google Scholar
Moreira, P.I., Santos, M.S., and Oliveira, C.R. (2007). Alzheimer’s disease: a lesson from mitochondrial dysfunction. Antioxid. Redox Signal 9, 1621–1630.10.1089/ars.2007.1703Search in Google Scholar
Morishima-Kawashima, M., Oshima, N., Ogata, H., Yamaguchi, H., Yoshimura, M., Sugihara, S., and Ihara, Y. (2000). Effect of apolipoprotein E allele e4 on the initial phase of amyloid β-protein accumulation in the human brain. Am. J. Pathol. 157, 2093–2099.10.1016/S0002-9440(10)64847-XSearch in Google Scholar
Mosconi, L., Tsui, W.H., De Santi, S., Li, J., Rusinek, H., Convit, A., Li, Y., Boppana, M., and de Leon, M.J. (2005). Reduced hippocampal metabolism in MCI and AD: automated FDG-PET image analysis. Neurology 64, 1860–1867.10.1212/01.WNL.0000163856.13524.08Search in Google Scholar PubMed
Murphy, A.N., Bredesen, D.E., Cortopassi, G., Wang, E., and Fiskum, G. (1996). Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc. Natl. Acad. Sci. USA 93, 9893–9898.10.1073/pnas.93.18.9893Search in Google Scholar PubMed PubMed Central
Nater, U.M., Skoluda, N., and Strahler, J. (2013). Biomarkers of stress in behavioural medicine. Curr Opin Psychiatry 26, 440–445.10.1097/YCO.0b013e328363b4edSearch in Google Scholar PubMed
Nitta, A., Fukuta, T., Hasegawa, T., and Nabeshima, T. (1997). Continuous infusion of β-amyloid protein into the rat cerebral ventricle induces learning impairment and neuronal and morphological degeneration. Jpn. J. Pharmacol. 73, 51–57.10.1254/jjp.60.51Search in Google Scholar PubMed
Nunomura, A., Perry, G., Aliev, G., Hirai, K., Takeda, A., Balraj, E.K., Jones, P.K, Ghanbari, H., Wataya,T., Shimohama, S., et al. (2001). Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60, 759–767.10.1093/jnen/60.8.759Search in Google Scholar PubMed
Orzechowski, A., Grizard, J., Jank, M., Gajkowska, B., Lokociejewska, M., Zaron-Teperek, M., and Godlewski, M. (2002). Dexamethasone-mediated regulation of death and differentiation of muscle cells. Is hydrogen peroxide involved in the process? Reprod. Nutr. Dev. 42, 197–216.10.1051/rnd:2002018Search in Google Scholar
Orzechowski, A., Jank, M., Gajkowska, B., Sadkowski, T., Godlewski, M.M., and Ostaszewski, P. (2003). Delineation of signalling pathway leading to antioxidant-dependent inhibition of dexamethasone-mediated muscle cell death. J. Muscle Res. Cell Motil. 24, 33–53.10.1023/A:1024887431768Search in Google Scholar
Oshima, Y., Kuroda, Y., Kunishige, M., Matsumoto, T., and Mitsui, T. (2004). Oxidative stress-associated mitochondrial dysfunction in corticosteroid-treated muscle cells. Muscle Nerve 30, 49–54.10.1002/mus.20036Search in Google Scholar PubMed
Pace, T.W., Hu, F., and Miller, A.H. (2007). Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav. Immun. 21, 9–19.10.1016/j.bbi.2006.08.009Search in Google Scholar PubMed PubMed Central
Pajović, S.B., Pejić, S., Stojiljković, V., Gavrilović, L., Dronjak, S., and Kanazir, D.T. (2006). Alterations in hippocampal antioxidant enzyme activities and sympatho-adrenomedullary system of rats in response to different stress models. Physiol. Res. 55, 453–460.10.33549/physiolres.930807Search in Google Scholar PubMed
Pamplona, R. and Barja, G. (2007). Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Res. Rev. 6, 189–210.10.1016/j.arr.2007.06.002Search in Google Scholar PubMed
Pecori Giraldi, F., Moro, M., and Cavagnini, F. (2003). Gender-related differences in the presentation and course of Cushing’s disease. J. Clin. Endocrinol. Metab. 88, 1554–1558.10.1210/jc.2002-021518Search in Google Scholar
Pedersen, W.A. and Flynn, E.R. (2004). Insulin resistance contributes to aberrant stress responses in the Tg2576 mouse model of Alzheimer’s disease. Neurobiol. Dis. 17, 500–506.10.1016/j.nbd.2004.08.003Search in Google Scholar
Pedersen, W.A., Culmsee, C., Ziegler, D., Herman, J.P., and Mattson, M.P. (1999). Aberrant stress response associated with severe hypoglycemia in a transgenic mouse model of Alzheimer’s disease. J. Mol. Neurosci. 13, 159–165.10.1385/JMN:13:1-2:159Search in Google Scholar
Pedersen, W.A., Wan, R., and Mattson, M.P. (2001). Impact of aging on stress-responsive neuroendocrine systems. Mech. Ageing Dev. 122, 963–983.10.1016/S0047-6374(01)00250-0Search in Google Scholar
Perani, D., Bressi, S., Cappa, S.F., Vallar, G., Alberoni, M., Grassi, F., Caltagirone, C., Cipolotti, L., Franceschi, M., Lenzi, G.L., and Fazio, F. (1993). Evidence of multiple memory systems in the human brain. A [18F]FDG PET metabolic study. Brain 116, 903–199.10.1093/brain/116.4.903Search in Google Scholar
Petrie, E.C., Cross, D.J., Galasko, D., Schellenberg, G.D., Raskind, M.A., Peskind, E.R., and Minoshima, S. (2009). Preclinical evidence of Alzheimer changes: convergent cerebrospinal fluid biomarker and fluorodeoxyglucose positron emission tomography findings. Arch. Neurol. 66, 632–637.10.1001/archneurol.2009.59Search in Google Scholar PubMed PubMed Central
Piroli, G.G., Grillo, C.A., Reznikov, L.R., Adams, S., McEwen, B.S., Charron, M.J., and Reagan, L.P. (2007). Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology 85, 71–80.10.1159/000101694Search in Google Scholar PubMed
Praticò, D., MY Lee, V., Trojanowski, J.Q., Rokach, J., and Fitzgerald, G.A. (1998). Increased F2-isoprostanes in Alzheimer’s disease: evidence for enhanced lipid peroxidation in vivo. FASEB J. 12, 1777–1783.10.1096/fasebj.12.15.1777Search in Google Scholar PubMed
Praticò, D., Uryu, K., Leight, S., Trojanoswki, J.Q., and Lee, V. M. (2001). Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 21,4183–4187.10.1523/JNEUROSCI.21-12-04183.2001Search in Google Scholar
Qin, L., Wu, X., Block, M.L., Liu, Y., Breese, G.R., Hong, J.S., Knapp, D.J., and Crews, F.T. (2007). Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55, 453–462.10.1002/glia.20467Search in Google Scholar PubMed PubMed Central
Radak, Z., Sasvari, M., Nyakas, C., Kaneko, T., Ohno, H., and Goto, S. (2001). Single bout of exercise eliminates the immobilization-induced oxidative stress in rat brain. Neurochem. Int. 39, 33–38.10.1016/S0197-0186(01)00003-1Search in Google Scholar
Rapoport, S.I. (1999). In vivo PET imaging and postmortem studies suggest potentially reversible and irreversible stages of brain metabolic failure in Alzheimer’s disease. Eur. Arch. Psychiatry Clin. Neurosci. 249 Suppl 3, 46–55.Search in Google Scholar
Rea, S.L., Ventura, N., and Johnson, T.E. (2007). Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5, e259.10.1371/journal.pbio.0050259Search in Google Scholar PubMed PubMed Central
Reul, J.M. and de Kloet, E.R. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117, 2505–2511.10.1210/endo-117-6-2505Search in Google Scholar PubMed
Ricci, S., Fuso, A., Ippoliti, F., and Businaro, R.J. (2012). Stress-induced cytokines and neuronal dysfunction in Alzheimer’s disease. Alzheimers Dis. 28, 11–24. Review.10.3233/JAD-2011-110821Search in Google Scholar PubMed
Rockenstein, E.M., McConlogue, L., Tan, H., Power, M., Masliah, E., and Mucke, L. (1995). Levels and alternative splicing of amyloid β protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer’s disease. J. Biol. Chem. 270, 28257–28267.10.1074/jbc.270.47.28257Search in Google Scholar PubMed
Ros-Bernal, F., Hunot, S., Herrero, M.T., Parnadeau, S., Corvol, J.C., Lu, L., Alvarez-Fischer, D., Carrillo-de Sauvage, M.A., Saurini, F., Coussieu, C., et al. (2011). Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proc. Natl. Acad. Sci. USA 108, 6632–6637.10.1073/pnas.1017820108Search in Google Scholar PubMed PubMed Central
Rothman, S.M. and Mattson, M.P. (2010). Adverse stress, hippocampal networks, and Alzheimer’s disease. Neuromolecular Med. 12, 56–70.10.1007/s12017-009-8107-9Search in Google Scholar PubMed PubMed Central
Rothman, S.M., Herdener, N., Camandola, S., Texel, S.J., Mughal, M.R., Cong, W.N., Martin, B., and Mattson, M.P. (2012). 3xTgAD mice exhibit altered behavior and elevated Aβ after chronic mild social stress. Neurobiol. Aging 33, 830.e1–12.10.1016/j.neurobiolaging.2011.07.005Search in Google Scholar PubMed PubMed Central
Rowan, M.J., Klyubin, I., Cullen, W.K., and Anwyl, R. (2003). Synaptic plasticity in animal models of early Alzheimer’s disease. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 821–828.10.1098/rstb.2002.1240Search in Google Scholar PubMed PubMed Central
Sahin, E. and Gumuslu, S. (2007a). Immobilization stress in rat tissues: alterations in protein oxidation, lipid peroxidation and antioxidant defense system. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 144, 342–347.10.1016/j.cbpc.2006.10.009Search in Google Scholar PubMed
Sahin, E. and Gumuslu, S. (2007b). Stress-dependent induction of protein oxidation, lipid peroxidation and anti-oxidants in peripheral tissues of rats: comparison of three stress models (immobilization, cold and immobilization-cold). Clin. Exp. Pharmacol. Physiol. 34, 425–431.10.1111/j.1440-1681.2007.04584.xSearch in Google Scholar PubMed
Sanz, A., Pamplona, R., and Barja, G. (2006). Is the mitochondrial free radical theory of aging intact? Antioxid. Redox Signal 8, 582–599.10.1089/ars.2006.8.582Search in Google Scholar PubMed
Sapolsky, R.M., Krey, L.C., and McEwen, B.S. (1985). Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5, 1222–1227.10.1523/JNEUROSCI.05-05-01222.1985Search in Google Scholar
Sastre, M., Dewatcher, I., Landreth, G. E., Willson, T. M., Klockgether, T., van Leuven, F., and Heneka M. T. (2003). Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-γ agonists modulate immunostimulated processing of amyloid precursor protein through regulation of β-secretase. J. Neurosci. 23, 9796–9804.10.1523/JNEUROSCI.23-30-09796.2003Search in Google Scholar
Schatzberg, A.F. and Lindley, S. (2008). Glucocorticoid antagonists in neuropsychotic disorders. Eur. J. Pharmacol. 583, 358–364.10.1016/j.ejphar.2008.01.001Search in Google Scholar PubMed
Schriner, S.E., Linford, N.J., Martin, G.M., Treuting, P., Ogburn, C.E., Emond, M., Coskun, P.E., Ladiges, W., Wolf, N., Van Remmen, H., et al. (2005). Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308, 1909–1911.10.1126/science.1106653Search in Google Scholar PubMed
Schultz, C., Dehghani, F., Hubbard, G.B., Thal, D.R., Struckhoff, G., Braak, E., and Braak, H. (2000). Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons. J. Neuropathol. Exp. Neurol. 59, 39–52.10.1093/jnen/59.1.39Search in Google Scholar PubMed
Selkoe, D.J. (2002). Alzheimer’s disease is a synaptic failure. Science 298, 789–791.10.1126/science.1074069Search in Google Scholar PubMed
Selvatici, R., Marani, L., Marino, S., and Siniscalchi, A. (2013) In vitro mitochondrial failure and oxidative stress mimic biochemical features of Alzheimer disease. Neurochem. Int. 63, 112–120.Search in Google Scholar
Shao, C., Xiong, S., Li, G.M., Gu, L., Mao, G., Markesbery, W.R., and Lovell, M.A. (2008). Altered 8-oxoguanine glycosylase in mild cognitive impairment and late-stage Alzheimer’s disease brain. Free Radic. Biol. Med. 45, 813–819.10.1016/j.freeradbiomed.2008.06.003Search in Google Scholar PubMed PubMed Central
Singh, A. and Kumar, A. (2008). Protective effect of alprazolam against sleep deprivation-induced behavior alterations and oxidative damage in mice. Neurosci. Res. 60, 372–379.10.1016/j.neures.2007.12.003Search in Google Scholar PubMed
Smith, J. (2003). Stress and aging: theoretical and empirical challenges for interdisciplinary research. Neurobiol. Aging 24 (Suppl 1), 77–80; discussion 81–82.10.1016/S0197-4580(03)00049-6Search in Google Scholar
Solas, M., Aisa, B., Tordera, R.M., Mugueta, M.C., Ramírez, M.J. (2013). Stress contributes to the development of central insulin resistance during aging: implications for Alzheimer’s disease. Biochim Biophys Acta 1832, 2332–2339.10.1016/j.bbadis.2013.09.013Search in Google Scholar PubMed
Sorrells, S.F, Caso, J.R, Munhoz, C.D., and Sapolsky, R.M. (2009). The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64, 33–39.10.1016/j.neuron.2009.09.032Search in Google Scholar PubMed PubMed Central
Sotiropoulos, I., Catania, C., Riedemann, T., Fry, J.P., Breen, K.C., Michaelidis, T.M., and Almeida, O.F. (2008). Glucocorticoids trigger Alzheimer disease-like pathobiochemistry in rat neuronal cells expressing human tau. J. Neurochem. 107, 385–397.10.1111/j.1471-4159.2008.05613.xSearch in Google Scholar PubMed
Sotiropoulos, I., Catania, C., Pinto, L.G., Silva, R., Pollerberg, G.E., Takashima, A., Sousa, N., and Almeida, O.F. (2011). stress acts cumulatively to precipitate Alzheimer’s disease-like tau pathology and cognitive deficits. J. Neurosci. 31, 7840–7847.10.1523/JNEUROSCI.0730-11.2011Search in Google Scholar PubMed PubMed Central
Srivareerat, M., Tran, T.T., Alzoubi, K.H., and Alkadhi, K.A. (2009). Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in β-amyloid rat model of Alzheimer’s disease. Biol. Psychiatry 65, 918–926.10.1016/j.biopsych.2008.08.021Search in Google Scholar PubMed
Starkov, A.A. (2008). The role of mitochondria in reactive oxygen species metabolism and signaling. Ann. NY Acad. Sci. 1147, 37–52.10.1196/annals.1427.015Search in Google Scholar PubMed PubMed Central
Stephan, A. and Phillips, A.G. (2005). A case for a non-transgenic animal model of Alzheimer’s disease. Genes Brain Behav. 4, 157–172.10.1111/j.1601-183X.2004.00113.xSearch in Google Scholar PubMed
Sultana, R. and Butterfield, D.A. (2009). Oxidatively modified, mitochondria-relevant brain proteins in subjects with Alzheimer disease and mild cognitive impairment. J. Bioenerg. Biomembr. 41, 441–446.10.1007/s10863-009-9241-7Search in Google Scholar PubMed PubMed Central
Tanzi, R.E. (2005). The synaptic abeta hypothesis of Alzheimer disease. Nat. Neurosci. 8, 977–979.10.1038/nn0805-977Search in Google Scholar PubMed
Tomás-Camardiel, M., Rite, I., Herrera, A.J., de Pablos, R.M., Cano, J., Machado, A., and Venero, J.L. (2004). Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol. Dis. 16, 190–201.10.1016/j.nbd.2004.01.010Search in Google Scholar
Tran, T.T., Srivareerat, M., and Alkadhi, K.A. (2010). Chronic psychosocial stress triggers cognitive impairment in a novel at-risk model of Alzheimer’s disease. Neurobiol. Dis. 37, 756–763.10.1016/j.nbd.2009.12.016Search in Google Scholar
Tsolaki, M., Pantazi, C., Stiliou, F., Aminta, M., Diudi, P., Karasoulas Kazis, A., and Pollen, D. (2003). Prevalence of dementia in Greek Orthodox Monasteries: the role of diet poor in lipids. Brain Aging 3, 13–17.Search in Google Scholar
Tsolaki, M., Papaliagkas, V., Kounti, F., Messini, C., Boziki, M., Anogianakis, G., and Vlaikidis, N. (2010). Severely stressful events and dementia: a study of an elderly Greek demented population. Psychiatry Res. 176, 51–54.10.1016/j.psychres.2009.06.001Search in Google Scholar
Vassar, R. (2001). The β-secretase, BACE: a prime drug target for Alzheimer’s disease. J. Mol. Neurosci. 17, 157–170.10.1385/JMN:17:2:157Search in Google Scholar
Velliquette, R.A., O’Connor, T., and Vassar, R. (2005). Energy inhibition elevates β-secretase levels and activity and is potentially amyloidogenic in APP transgenic mice: possible early events in Alzheimer’s disease pathogenesis, J. Neurosci. 25, 10874–10883.10.1523/JNEUROSCI.2350-05.2005Search in Google Scholar PubMed PubMed Central
Velliquette, R.A., O’Connor, T., and Vassar, R. (2006). Energy inhibition elevates β-secretase levels and activity and is potentially amyloidogenic in APP transgenic mice: possible early events in Alzheimer’s disease pathogenesis. J. Neurosci. 26, 2140–2142.Search in Google Scholar
Villarán, R.F., de Pablos, R.M., Argüelles, S., Espinosa-Oliva, A.M., Tomás-Camardiel, M., Herrera, A.J., Cano, J., and Machado, A. (2009). The intranigral injection of tissue plasminogen activator induced blood-brain barrier disruption, inflammatory process and degeneration of the dopaminergic system of the rat. Neurotoxicology 30, 403–413.10.1016/j.neuro.2009.02.011Search in Google Scholar PubMed
Virgin, C.E.Jr., Ha, T.P., Packan, D.R., Tombaugh, G.C., Yang, S.H., Horner, H.C., and Sapolsky, R.M. (1991). Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J. Neurochem. 57, 1422–1428.10.1111/j.1471-4159.1991.tb08309.xSearch in Google Scholar PubMed
Wang, J., Dickson, D. W., Trojanowski, J. Q., and Lee V. M. (1999). The levels of soluble versus insoluble brain Aβ distinguish Alzheimer’s disease from normal and pathologic aging. Exp. Neurol. 158, 328–337.10.1006/exnr.1999.7085Search in Google Scholar PubMed
Ward, P.A. and Till, G.O. (1990). Pathophysiologic events related to thermal injury of skin. J. Trauma. 30, 75–79.10.1097/00005373-199012001-00018Search in Google Scholar PubMed
Wilson, R.S., Evans, D.A., Bienias, J.L., Mendes de Leon, C.F., Schneider, J.A., and Bennett, D.A. (2003). Proneness to psychological distress is associated with risk of Alzheimer’s disease. Neurology 61, 1468–1469.10.1212/01.WNL.0000096167.56734.59Search in Google Scholar
Wilson, R.S., Barnes, L.L., Bennett, D.A., Li, Y., Bienias, J.L., Mendes de Leon, C.F., and Evans, D.A. (2005). Proneness to psychological distress and risk of Alzheimer disease in a biracial community. Neurology 64, 380–382.10.1212/01.WNL.0000149525.53525.E7Search in Google Scholar PubMed
Wilson, R.S., Arnold, S.E., Schneider, J.A., Kelly, J.F., Tang, Y., and Bennett, D.A. (2006). Chronic psychological distress and risk of Alzheimer’s disease in old age. Neuroepidemiology 27, 143–53.10.1159/000095761Search in Google Scholar PubMed
Yamaguchi, S., Meguro, K., Itoh, M., Hayasaka, C., Shimada, M., Yamazaki, H., and Yamadori, A. (1997). Decreased cortical glucose metabolism correlates with hippocampal atrophy in Alzheimer’s disease as shown by MRI and PET. J. Neurol. Neurosurg. Psychiatry 62, 596–600.10.1136/jnnp.62.6.596Search in Google Scholar PubMed PubMed Central
Yankner, B.A. and Lu, T. (2009). Amyloid β-protein toxicity and the pathogenesis of Alzheimer disease. J. Biol. Chem. 284, 4755–4759.10.1074/jbc.R800018200Search in Google Scholar PubMed PubMed Central
Yankner, B.A., Lu, T., and Loerch, P. (2008). The aging brain. Annu. Rev. Pathol. 3, 41–66.10.1146/annurev.pathmechdis.2.010506.092044Search in Google Scholar PubMed
Yasuno, F., Imamura, T., Hirono, N., Ishii, K., Sasaki, M., Ikejiri, Y., Hashimoto, M., Shimomura, T., Yamashita, H., and Mori, E. (1998). Age at onset and regional cerebral glucose metabolism in Alzheimer’s disease. Dement. Geriatr. Cogn. Disord. 9, 63–67.10.1159/000017024Search in Google Scholar PubMed
Youdim, M.B., Banerjee, D.K, Kelner, K., Offutt, L., and Pollard, H.B. (1989). Steroid regulation of monoamine oxidase activity in the adrenal medulla. FASEB J. 3, 1753–1759.10.1096/fasebj.3.6.2495232Search in Google Scholar PubMed
Zafir, A. and Banu, N. (2009). Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats. Stress 12, 167–177.10.1080/10253890802234168Search in Google Scholar PubMed
Zamzami, N., Marzo, I., Susin, S.A., Brenner, C., Larochette, N., Marchetti, P., Reed, J., Kofler, R., and Kroemer, G. (1998). The thiol crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene 26, 1055–1063.10.1038/sj.onc.1201864Search in Google Scholar PubMed
©2014 by De Gruyter