Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Mini-Review Article

Early Chronic Stress Induced Changes within the Locus Coeruleus in Sporadic Alzheimer’s Disease

Author(s): Donné Minné*, Jeanine L. Marnewick and Penelope Engel-Hills

Volume 20, Issue 5, 2023

Published on: 20 September, 2023

Page: [301 - 317] Pages: 17

DOI: 10.2174/1567205020666230811092956

Price: $65

Abstract

Chronic exposure to stress throughout the lifespan has been the focus of many studies on Alzheimer's disease (AD) because of the similarities between the biological mechanisms involved in chronic stress and the pathophysiology of AD. In fact, the earliest abnormality associated with the disease is the presence of phosphorylated tau protein in locus coeruleus neurons, a brain structure highly responsive to stress and perceived threat. Here, we introduce allostatic load as a useful concept for understanding many of the complex, interacting neuropathological changes involved in the AD degenerative process. In response to chronic stress, aberrant tau proteins that begin to accumulate within the locus coeruleus decades prior to symptom onset appear to represent a primary pathological event in the AD cascade, triggering a wide range of interacting brain changes involving neuronal excitotoxicity, endocrine alterations, inflammation, oxidative stress, and amyloid plaque exacerbation. While it is acknowledged that stress will not necessarily be the major precipitating factor in all cases, early tau-induced changes within the locus coeruleus-norepinephrine pathway suggests that a therapeutic window might exist for preventative measures aimed at managing stress and restoring balance within the HPA axis.

Next »
[1]
Niu, H.; Álvarez-Álvarez, I.; Guillén-Grima, F.; Aguinaga-Ontoso, I. Prevalence and incidence of Alzheimer’s disease in Europe: A meta-analysis. Neurologia, 2017, 32(8), 523-532.
[http://dx.doi.org/10.1016/j.nrl.2016.02.016] [PMID: 27130306]
[2]
James, B.D.; Leurgans, S.E.; Hebert, L.E.; Scherr, P.A.; Yaffe, K.; Bennett, D.A. Contribution of Alzheimer disease to mortality in the United States. Neurology, 2014, 82(12), 1045-1050.
[http://dx.doi.org/10.1212/WNL.0000000000000240] [PMID: 24598707]
[3]
Fox, N.C.; Freeborough, P.A.; Rossor, M.N. Visualisation and quantification of rates of atrophy in Alzheimer’s disease. Lancet, 1996, 348(9020), 94-97.
[http://dx.doi.org/10.1016/S0140-6736(96)05228-2] [PMID: 8676724]
[4]
van Hoesen, G.W.; Hyman, B.T.; Damasio, A.R.; Tosakulwong, N.; Buciuc, M.; Murray, M.E.; Petrucelli, L.; Senjem, M.L.; Spychalla, A.J.; Knopman, D.S.; Boeve, B.F. Entorhinal cortex pathology in Alzheimer’s disease. Hippocampus, 1991, 1(1), 1-8.
[http://dx.doi.org/10.1002/hipo.450010102] [PMID: 1669339]
[5]
Hoesen, V.; Hyman, B.T.; Damasio, A.R. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus, 1991, 1(1), 1-8.
[6]
Iqbal, K.; Liu, F.; Gong, C.X.; Grundke-Iqbal, I. Tau in Alzheimer disease and related tauopathies. Curr. Alzheimer Res., 2010, 7(8), 656-664.
[http://dx.doi.org/10.2174/156720510793611592] [PMID: 20678074]
[7]
Serrano-Pozo, A.; Frosch, M.P.; Masliah, E.; Hyman, B.T. Neuropathological alterations in Alzheimer disease. Cold Spring Harb. Perspect. Med., 2011, 1(1), a006189.
[http://dx.doi.org/10.1101/cshperspect.a006189] [PMID: 22229116]
[8]
Hardy, J; Selkoe, DJ The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science, 2002, 297(5580), 353-6.
[9]
Tanzi, R.E.; Bertram, L. Twenty years of the Alzheimer’s disease amyloid hypothesis: A genetic perspective. Cell, 2005, 120(4), 545-555.
[http://dx.doi.org/10.1016/j.cell.2005.02.008] [PMID: 15734686]
[10]
Goodson, H.V.; Jonasson, E.M. Microtubules and microtubule-associated proteins. Cold Spring Harb. Perspect. Biol., 2018, 10(6), a022608.
[http://dx.doi.org/10.1101/cshperspect.a022608] [PMID: 29858272]
[11]
Mondragón-Rodríguez, S.; Trillaud-Doppia, E.; Dudilot, A.; Bourgeois, C.; Lauzon, M.; Leclerc, N.; Boehm, J. Interaction of endogenous tau protein with synaptic proteins is regulated by N-methyl-D-aspartate receptor-dependent tau phosphorylation. J. Biol. Chem., 2012, 287(38), 32040-32053.
[http://dx.doi.org/10.1074/jbc.M112.401240] [PMID: 22833681]
[12]
Ferreira, S.T.; Lourenco, M.V.; Oliveira, M.M.; De Felice, F.G. Soluble amyloid-β oligomers as synaptotoxins leading to cognitive impairment in Alzheimer's disease. Front. Cell. Neurosci., 2015, 9, 191.
[http://dx.doi.org/10.3389/fncel.2015.00191] [PMID: 26074767]
[13]
Leuner, K.; Schütt, T.; Kurz, C.; Eckert, S.H.; Schiller, C.; Occhipinti, A.; Mai, S.; Jendrach, M.; Eckert, G.P.; Kruse, S.E.; Palmiter, R.D.; Brandt, U.; Dröse, S.; Wittig, I.; Willem, M.; Haass, C.; Reichert, A.S.; Müller, W.E. Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid. Redox Signal., 2012, 16(12), 1421-1433.
[http://dx.doi.org/10.1089/ars.2011.4173] [PMID: 22229260]
[14]
Cirrito, J.R.; May, P.C.; O’Dell, M.A.; Taylor, J.W.; Parsadanian, M.; Cramer, J.W.; Audia, J.E.; Nissen, J.S.; Bales, K.R.; Paul, S.M.; DeMattos, R.B.; Holtzman, D.M. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-β metabolism and half-life. J. Neurosci., 2003, 23(26), 8844-8853.
[http://dx.doi.org/10.1523/JNEUROSCI.23-26-08844.2003] [PMID: 14523085]
[15]
Rapoport, M.; Dawson, H.N.; Binder, L.I.; Vitek, M.P.; Ferreira, A. Tau is essential to β-amyloid-induced neurotoxicity. Proc. Natl. Acad. Sci. USA, 2002, 99(9), 6364-6369.
[http://dx.doi.org/10.1073/pnas.092136199] [PMID: 11959919]
[16]
Arnsten, A.F.T.; Datta, D.; Del Tredici, K.; Braak, H. Hypothesis: Tau pathology is an initiating factor in sporadic Alzheimer’s disease. Alzheimers Dement., 2021, 17(1), 115-124.
[http://dx.doi.org/10.1002/alz.12192] [PMID: 33075193]
[17]
Maccioni, R.B.; Farías, G.; Morales, I.; Navarrete, L. The revitalized tau hypothesis on Alzheimer’s disease. Arch. Med. Res., 2010, 41(3), 226-231.
[http://dx.doi.org/10.1016/j.arcmed.2010.03.007] [PMID: 20682182]
[18]
Mondragón-Rodríguez, S.; Salgado-Burgos, H.; Peña-Ortega, F. Circuitry and synaptic dysfunction in Alzheimer’s disease: A new tau hypothesis. Neural Plast., 2020, 2020, 1-11.
[http://dx.doi.org/10.1155/2020/2960343] [PMID: 32952546]
[19]
Pooler, A.M.; Noble, W.; Hanger, D.P. A role for tau at the synapse in Alzheimer’s disease pathogenesis. Neuropharmacology, 2014, 76(Pt A), 1-8.
[http://dx.doi.org/10.1016/j.neuropharm.2013.09.018] [PMID: 24076336]
[20]
Bhat, R; Crowe, EP; Bitto, A; Moh, M; Katsetos, CD; Garcia, FU; Johnson, FB; Trojanowski, JQ; Sell, C; Torres, C Astrocyte senescence as a component of Alzheimer’s disease. PLoS One, 2012, 7(9), e45069.
[http://dx.doi.org/10.1371/journal.pone.0045069]
[21]
Murray, I.V.J.; Proza, J.F.; Sohrabji, F.; Lawler, J.M. Vascular and metabolic dysfunction in Alzheimer’s disease: A review. Exp. Biol. Med., 2011, 236(7), 772-782.
[http://dx.doi.org/10.1258/ebm.2011.010355] [PMID: 21680755]
[22]
Kinney, J.W.; Bemiller, S.M.; Murtishaw, A.S.; Leisgang, A.M.; Salazar, A.M.; Lamb, B.T. Inflammation as a central mechanism in Alzheimer’s disease. Alzheimers Dement., 2018, 4(1), 575-590.
[http://dx.doi.org/10.1016/j.trci.2018.06.014] [PMID: 30406177]
[23]
Maccioni, R.B.; Rojo, L.E.; Fernández, J.A.; Kuljis, R.O. The role of neuroimmunomodulation in Alzheimer’s disease. Ann. N. Y. Acad. Sci., 2009, 1153(1), 240-246.
[http://dx.doi.org/10.1111/j.1749-6632.2008.03972.x] [PMID: 19236346]
[24]
Hooijmans, C.R.; Kiliaan, A.J. Fatty acids, lipid metabolism and Alzheimer pathology. Eur. J. Pharmacol., 2008, 585(1), 176-196.
[http://dx.doi.org/10.1016/j.ejphar.2007.11.081] [PMID: 18378224]
[25]
Castellani, R.; Hirai, K.; Aliev, G.; Drew, K.L.; Nunomura, A.; Takeda, A.; Cash, A.D.; Obrenovich, M.E.; Perry, G.; Smith, M.A. Role of mitochondrial dysfunction in Alzheimer’s disease. J. Neurosci. Res., 2002, 70(3), 357-360.
[http://dx.doi.org/10.1002/jnr.10389] [PMID: 12391597]
[26]
Mosconi, L. Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging, 2005, 32(4), 486-510.
[http://dx.doi.org/10.1007/s00259-005-1762-7] [PMID: 15747152]
[27]
Steen, E.; Terry, B.M.J.; Rivera, E.J.; Cannon, J.L.; Neely, T.R.; Tavares, R.; Xu, X.J.; Wands, J.R.; de la Monte, S.M. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer’s disease--is this type 3 diabetes? J. Alzheimers Dis., 2005, 7(1), 63-80.
[http://dx.doi.org/10.3233/JAD-2005-7107] [PMID: 15750215]
[28]
Smith, M.A.; Rottkamp, C.A.; Nunomura, A.; Raina, A.K.; Perry, G. Oxidative stress in Alzheimer’s disease. Biochim. Biophys. Acta Mol. Basis Dis., 2000, 1502(1), 139-144.
[http://dx.doi.org/10.1016/S0925-4439(00)00040-5]
[29]
Uddin, M.S.; Tewari, D.; Mamun, A.A.; Kabir, M.T.; Niaz, K.; Wahed, M.I.I.; Barreto, G.E.; Ashraf, G.M. Circadian and sleep dysfunction in Alzheimer’s disease. Ageing Res. Rev., 2020, 60, 101046.
[http://dx.doi.org/10.1016/j.arr.2020.101046] [PMID: 32171783]
[30]
Vest, R.S.; Pike, C.J. Gender, sex steroid hormones, and Alzheimer’s disease. Horm. Behav., 2013, 63(2), 301-307.
[http://dx.doi.org/10.1016/j.yhbeh.2012.04.006] [PMID: 22554955]
[31]
Tan, Z.S.; Vasan, R.S. Thyroid function and Alzheimer’s disease. J. Alzheimers Dis., 2009, 16(3), 503-507.
[http://dx.doi.org/10.3233/JAD-2009-0991] [PMID: 19276542]
[32]
Piirainen, S.; Youssef, A.; Song, C.; Kalueff, A.V.; Landreth, G.E.; Malm, T.; Tian, L. Psychosocial stress on neuroinflammation and cognitive dysfunctions in Alzheimer’s disease: The emerging role for microglia? Neurosci. Biobehav. Rev., 2017, 77, 148-164.
[http://dx.doi.org/10.1016/j.neubiorev.2017.01.046] [PMID: 28185874]
[33]
Kim, J.; Basak, J.M.; Holtzman, D.M. The role of apolipoprotein E in Alzheimer’s disease. Neuron, 2009, 63(3), 287-303.
[http://dx.doi.org/10.1016/j.neuron.2009.06.026] [PMID: 19679070]
[34]
Strittmatter, W.J.; Roses, A.D. Apolipoprotein E and Alzheimer’s Disease. Annu. Rev. Neurosci., 1996, 19(1), 53-77.
[http://dx.doi.org/10.1146/annurev.ne.19.030196.000413] [PMID: 8833436]
[35]
Wheeler, M.J.; Dempsey, P.C.; Grace, M.S.; Ellis, K.A.; Gardiner, P.A.; Green, D.J.; Dunstan, D.W. Sedentary behavior as a risk factor for cognitive decline? A focus on the influence of glycemic control in brain health. Alzheimers Dement., 2017, 3(3), 291-300.
[http://dx.doi.org/10.1016/j.trci.2017.04.001] [PMID: 29067335]
[36]
de la Monte, S.M.; Longato, L.; Tong, M.; Wands, J.R. Insulin resistance and neurodegeneration: Roles of obesity, type 2 diabetes mellitus and non-alcoholic steatohepatitis. Curr. Opin. Investig. Drugs, 2009, 10(10), 1049-60.
[37]
Skoog, I.; Gustafson, D. Update on hypertension and Alzheimer’s disease. Neurol. Res., 2006, 28(6), 605-611.
[http://dx.doi.org/10.1179/016164106X130506] [PMID: 16945211]
[38]
Puglielli, L.; Tanzi, R.E.; Kovacs, D.M. Alzheimer’s disease: The cholesterol connection. Nat. Neurosci., 2003, 6(4), 345-351.
[http://dx.doi.org/10.1038/nn0403-345] [PMID: 12658281]
[39]
Casserly, I.; Topol, E.J. Convergence of atherosclerosis and Alzheimer’s disease: Inflammation, cholesterol, and misfolded proteins. Lancet, 2004, 363(9415), 1139-1146.
[http://dx.doi.org/10.1016/S0140-6736(04)15900-X] [PMID: 15064035]
[40]
Sivanandam, T.M.; Thakur, M.K. Traumatic brain injury: A risk factor for Alzheimer’s disease. Neurosci. Biobehav. Rev., 2012, 36(5), 1376-1381.
[http://dx.doi.org/10.1016/j.neubiorev.2012.02.013] [PMID: 22390915]
[41]
Burke, S.L.; Cadet, T.; Alcide, A.; O’Driscoll, J.; Maramaldi, P. Psychosocial risk factors and Alzheimer’s disease: The associative effect of depression, sleep disturbance, and anxiety. Aging Ment. Health, 2018, 22(12), 1577-1584.
[http://dx.doi.org/10.1080/13607863.2017.1387760] [PMID: 29077487]
[42]
Stern, Y.; Gurland, B.; Tatemichi, T.K.; Tang, M.X.; Wilder, D.; Mayeux, R. Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA, 1994, 271(13), 1004-1010.
[http://dx.doi.org/10.1001/jama.1994.03510370056032] [PMID: 8139057]
[43]
Diniz, B.S.; Butters, M.A.; Albert, S.M.; Dew, M.A.; Reynolds, C.F., III Late-life depression and risk of vascular dementia and Alzheimer’s disease: Systematic review and meta-analysis of community-based cohort studies. Br. J. Psychiatry, 2013, 202(5), 329-335.
[http://dx.doi.org/10.1192/bjp.bp.112.118307] [PMID: 23637108]
[44]
Edwards, G.A., III; Gamez, N.; Escobedo, G., Jr; Calderon, O.; Moreno-Gonzalez, I. Modifiable risk factors for Alzheimer’s disease. Front. Aging Neurosci., 2019, 11, 146.
[http://dx.doi.org/10.3389/fnagi.2019.00146] [PMID: 31293412]
[45]
Sala Frigerio, C.; Wolfs, L.; Fattorelli, N.; Thrupp, N.; Voytyuk, I.; Schmidt, I.; Mancuso, R.; Chen, W.T.; Woodbury, M.E.; Srivastava, G.; Möller, T.; Hudry, E.; Das, S.; Saido, T.; Karran, E.; Hyman, B.; Perry, V.H.; Fiers, M.; De Strooper, B. The major risk factors for Alzheimer’s disease: Age, sex, and genes modulate the microglia response to Aβ plaques. Cell Rep., 2019, 27(4), 1293-1306.e6.
[http://dx.doi.org/10.1016/j.celrep.2019.03.099] [PMID: 31018141]
[46]
Lindsay, J.; Laurin, D.; Verreault, R.; Hébert, R.; Helliwell, B.; Hill, G.B.; McDowell, I. Risk factors for Alzheimer’s disease: A prospective analysis from the Canadian Study of Health and Aging. Am. J. Epidemiol., 2002, 156(5), 445-453.
[http://dx.doi.org/10.1093/aje/kwf074] [PMID: 12196314]
[47]
Sharma, V.K.; Mehta, V.; Singh, T.G. Alzheimer’s disorder: Epigenetic connection and associated risk factors. Curr. Neuropharmacol., 2020, 18(8), 740-753.
[http://dx.doi.org/10.2174/1570159X18666200128125641] [PMID: 31989902]
[48]
Fish, P.V.; Steadman, D.; Bayle, E.D.; Whiting, P. New approaches for the treatment of Alzheimer’s disease. Bioorg. Med. Chem. Lett., 2019, 29(2), 125-133.
[http://dx.doi.org/10.1016/j.bmcl.2018.11.034] [PMID: 30501965]
[49]
Betts, M.J.; Kirilina, E.; Otaduy, M.C.G.; Ivanov, D.; Acosta-Cabronero, J.; Callaghan, M.F.; Lambert, C.; Cardenas-Blanco, A.; Pine, K.; Passamonti, L.; Loane, C.; Keuken, M.C.; Trujillo, P.; Lüsebrink, F.; Mattern, H.; Liu, K.Y.; Priovoulos, N.; Fliessbach, K.; Dahl, M.J.; Maaß, A.; Madelung, C.F.; Meder, D.; Ehrenberg, A.J.; Speck, O.; Weiskopf, N.; Dolan, R.; Inglis, B.; Tosun, D.; Morawski, M.; Zucca, F.A.; Siebner, H.R.; Mather, M.; Uludag, K.; Heinsen, H.; Poser, B.A.; Howard, R.; Zecca, L.; Rowe, J.B.; Grinberg, L.T.; Jacobs, H.I.L.; Düzel, E.; Hämmerer, D. Locus coeruleus imaging as a biomarker for noradrenergic dysfunction in neurodegenerative diseases. Brain, 2019, 142(9), 2558-2571.
[http://dx.doi.org/10.1093/brain/awz193] [PMID: 31327002]
[50]
Gandy, S.; Bartfai, T.; Lees, G.V.; Sano, M. Midlife interventions are critical in prevention, delay, or improvement of Alzheimer’s disease and vascular cognitive impairment and dementia. F1000 Res., 2017, 6, 413.
[http://dx.doi.org/10.12688/f1000research.11140.1] [PMID: 28491285]
[51]
Kremen, W.S.; Panizzon, M.S.; Elman, J.A.; Granholm, E.L.; Andreassen, O.A.; Dale, A.M.; Gillespie, N.A.; Gustavson, D.E.; Logue, M.W.; Lyons, M.J.; Neale, M.C.; Reynolds, C.A.; Whitsel, N.; Franz, C.E. Pupillary dilation responses as a midlife indicator of risk for Alzheimer’s disease: Association with Alzheimer’s disease polygenic risk. Neurobiol. Aging, 2019, 83, 114-121.
[http://dx.doi.org/10.1016/j.neurobiolaging.2019.09.001] [PMID: 31585363]
[52]
Rasmussen, J.; Langerman, H. Alzheimer’s disease–why we need early diagnosis. Degener. Neurol. Neuromuscul. Dis., 2019, 9, 123-130.
[http://dx.doi.org/10.2147/DNND.S228939] [PMID: 31920420]
[53]
Braak, H.; Thal, D.R.; Ghebremedhin, E.; Del Tredici, K. Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years. J. Neuropathol. Exp. Neurol., 2011, 70(11), 960-969.
[http://dx.doi.org/10.1097/NEN.0b013e318232a379] [PMID: 22002422]
[54]
Kelly, S.C.; He, B.; Perez, S.E.; Ginsberg, S.D.; Mufson, E.J.; Counts, S.E. Locus coeruleus cellular and molecular pathology during the progression of Alzheimer’s disease. Acta Neuropathol. Commun., 2017, 5(1), 8.
[http://dx.doi.org/10.1186/s40478-017-0411-2] [PMID: 28109312]
[55]
Matchett, B.J.; Grinberg, L.T.; Theofilas, P.; Murray, M.E. The mechanistic link between selective vulnerability of the locus coeruleus and neurodegeneration in Alzheimer’s disease. Acta Neuropathol., 2021, 141(5), 631-650.
[http://dx.doi.org/10.1007/s00401-020-02248-1] [PMID: 33427939]
[56]
Olivieri, P.; Lagarde, J.; Lehericy, S.; Valabrègue, R.; Michel, A.; Macé, P.; Caillé, F.; Gervais, P.; Bottlaender, M.; Sarazin, M. Early alteration of the locus coeruleus in phenotypic variants of Alzheimer’s disease. Ann. Clin. Transl. Neurol., 2019, 6(7), 1345-1351.
[http://dx.doi.org/10.1002/acn3.50818] [PMID: 31353860]
[57]
Mather, M.; Harley, C.W. The locus coeruleus: Essential for maintaining cognitive function and the aging brain. Trends Cogn. Sci., 2016, 20(3), 214-226.
[http://dx.doi.org/10.1016/j.tics.2016.01.001] [PMID: 26895736]
[58]
Sara, S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci., 2009, 10(3), 211-223.
[http://dx.doi.org/10.1038/nrn2573] [PMID: 19190638]
[59]
Levine, E.S.; Joseph Litto, W.; Jacobs, B.L. Activity of cat locus coeruleus noradrenergic neurons during the defense reaction. Brain Res., 1990, 531(1-2), 189-195.
[http://dx.doi.org/10.1016/0006-8993(90)90773-5] [PMID: 2289120]
[60]
Sara, S.J.; Bouret, S. Orienting and reorienting: The locus coeruleus mediates cognition through arousal. Neuron, 2012, 76(1), 130-141.
[http://dx.doi.org/10.1016/j.neuron.2012.09.011] [PMID: 23040811]
[61]
Bouret, S.; Sara, S.J. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci., 2005, 28(11), 574-582.
[http://dx.doi.org/10.1016/j.tins.2005.09.002] [PMID: 16165227]
[62]
Vazey, E.M.; Moorman, D.E.; Aston-Jones, G. Phasic locus coeruleus activity regulates cortical encoding of salience information. Proc. Natl. Acad. Sci. USA, 2018, 115(40), E9439-E9448.
[http://dx.doi.org/10.1073/pnas.1803716115] [PMID: 30232259]
[63]
Ghosh, A.; Massaeli, F.; Power, K.D.; Omoluabi, T.; Torraville, S.E.; Pritchett, J.B.; Sepahvand, T.; Strong, V.D.; Reinhardt, C.; Chen, X.; Martin, G.M.; Harley, C.W.; Yuan, Q. Locus coeruleus activation patterns differentially modulate odor discrimination learning and odor valence in rats. Cerebral Cortex Communications, 2021, 2(2), tgab026.
[http://dx.doi.org/10.1093/texcom/tgab026] [PMID: 34296171]
[64]
Aston-Jones, G.; Cohen, J.D. An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu. Rev. Neurosci., 2005, 28(1), 403-450.
[http://dx.doi.org/10.1146/annurev.neuro.28.061604.135709] [PMID: 16022602]
[65]
Berridge, C.W.; Waterhouse, B.D. The locus coeruleus–noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev., 2003, 42(1), 33-84.
[http://dx.doi.org/10.1016/S0165-0173(03)00143-7] [PMID: 12668290]
[66]
Dayan, P.; Yu, A.J. Expected and unexpected uncertainty: ACh and NE in the neocortex. Adv. Neural Inf. Process. Syst., 2002, 2002, 15.
[67]
Llorca-Torralba, M.; Suárez-Pereira, I.; Bravo, L.; Camarena-Delgado, C.; Garcia-Partida, J.A.; Mico, J.A.; Berrocoso, E. Chemogenetic silencing of the locus coeruleus–basolateral amygdala pathway abolishes pain-induced anxiety and enhanced aversive learning in rats. Biol. Psychiatry, 2019, 85(12), 1021-1035.
[http://dx.doi.org/10.1016/j.biopsych.2019.02.018] [PMID: 30987747]
[68]
McCall, J.G.; Siuda, E.R.; Bhatti, D.L.; Lawson, L.A.; McElligott, Z.A.; Stuber, G.D.; Bruchas, M.R. Locus Coeruleus to basolateral amygdala noradrenergic projections promote anxiety-like behavior. eLife, 2017, 6, e18247.
[http://dx.doi.org/10.7554/eLife.18247] [PMID: 28708061]
[69]
Andrés-Benito, P.; Fernández-Dueñas, V.; Carmona, M.; Escobar, L.A.; Torrejón-Escribano, B.; Asó, E.; Ciruela, F.; Ferrer, I. Locus coeruleus at asymptomatic early and middle Braak stages of neurofibrillary tangle pathology. Neuropathol. Appl. Neurobiol., 2017, 43(5), 373-392.
[http://dx.doi.org/10.1111/nan.12386] [PMID: 28117912]
[70]
Ehrenberg, A.J.; Nguy, A.K.; Theofilas, P.; Dunlop, S.; Suemoto, C.K.; Di Lorenzo Alho, A.T.; Leite, R.P.; Diehl Rodriguez, R.; Mejia, M.B.; Rüb, U.; Farfel, J.M.; Lucena Ferretti-Rebustini, R.E.; Nascimento, C.F.; Nitrini, R.; Pasquallucci, C.A.; Jacob-Filho, W.; Miller, B.; Seeley, W.W.; Heinsen, H.; Grinberg, L.T. Quantifying the accretion of hyperphosphorylated tau in the locus coeruleus and dorsal raphe nucleus: The pathological building blocks of early Alzheimer’s disease. Neuropathol. Appl. Neurobiol., 2017, 43(5), 393-408.
[http://dx.doi.org/10.1111/nan.12387] [PMID: 28117917]
[71]
Attems, J.; Thal, D.R.; Jellinger, K.A. The relationship between subcortical tau pathology and Alzheimer’s disease. Biochem. Soc. Trans., 2012, 40(4), 711-715.
[http://dx.doi.org/10.1042/BST20120034] [PMID: 22817721]
[72]
Kang, S.S.; Ahn, E.H.; Liu, X.; Bryson, M.; Miller, G.W.; Weinshenker, D.; Ye, K. ApoE4 inhibition of VMAT2 in the locus coeruleus exacerbates Tau pathology in Alzheimer’s disease. Acta Neuropathol., 2021, 142(1), 139-158.
[http://dx.doi.org/10.1007/s00401-021-02315-1] [PMID: 33895869]
[73]
Sanders, D.W.; Kaufman, S.K.; DeVos, S.L.; Sharma, A.M.; Mirbaha, H.; Li, A.; Barker, S.J.; Foley, A.C.; Thorpe, J.R.; Serpell, L.C.; Miller, T.M.; Grinberg, L.T.; Seeley, W.W.; Diamond, M.I. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron, 2014, 82(6), 1271-1288.
[http://dx.doi.org/10.1016/j.neuron.2014.04.047] [PMID: 24857020]
[74]
Cao, S.; Fisher, D.W.; Rodriguez, G.; Yu, T.; Dong, H. Comparisons of neuroinflammation, microglial activation, and degeneration of the locus coeruleus- mice. J. Neuroinflammation, 2021, 18(1), 1-16.
[http://dx.doi.org/10.1186/s12974-020-02054-2] [PMID: 33407625]
[75]
Wilson, R.S.; Nag, S.; Boyle, P.A.; Hizel, L.P.; Yu, L.; Buchman, A.S.; Schneider, J.A.; Bennett, D.A. Neural reserve, neuronal density in the locus ceruleus, and cognitive decline. Neurology, 2013, 80(13), 1202-1208.
[http://dx.doi.org/10.1212/WNL.0b013e3182897103] [PMID: 23486878]
[76]
Marcyniuk, B.; Mann, D.M.A.; Yates, P.O. The topography of cell loss from locus caeruleus in Alzheimer’s disease. J. Neurol. Sci., 1986, 76(2-3), 335-345.
[http://dx.doi.org/10.1016/0022-510X(86)90179-6] [PMID: 3794754]
[77]
Pamphlett, R.; Kum Jew, S. Different populations of human locus ceruleus neurons contain heavy metals or hyperphosphorylated Tau: Implications for amyloid-β and tau pathology in Alzheimer’s disease. J. Alzheimers Dis., 2015, 45(2), 437-447.
[http://dx.doi.org/10.3233/JAD-142445] [PMID: 25547633]
[78]
Bakulski, K.M.; Seo, Y.A.; Hickman, R.C.; Brandt, D.; Vadari, H.S.; Hu, H.; Park, S.K. Heavy metals exposure and Alzheimer’s disease and related dementias. J. Alzheimers Dis., 2020, 76(4), 1215-1242.
[http://dx.doi.org/10.3233/JAD-200282] [PMID: 32651318]
[79]
Filosa, J.A.; Putnam, R.W. Multiple targets of chemosensitive signaling in locus coeruleus neurons: Role of K+ and Ca2+ channels. Am. J. Physiol. Cell Physiol., 2003, 284(1), C145-C155.
[http://dx.doi.org/10.1152/ajpcell.00346.2002] [PMID: 12388081]
[80]
Sanchez-Padilla, J.; Guzman, J.N.; Ilijic, E.; Kondapalli, J.; Galtieri, D.J.; Yang, B.; Schieber, S.; Oertel, W.; Wokosin, D.; Schumacker, P.T.; Surmeier, D.J. Mitochondrial oxidant stress in locus coeruleus is regulated by activity and nitric oxide synthase. Nat. Neurosci., 2014, 17(6), 832-840.
[http://dx.doi.org/10.1038/nn.3717] [PMID: 24816140]
[81]
Williams, J.T.; North, R.A.; Shefner, S.A.; Nishi, S.; Egan, T.M. Membrane properties of rat locus coeruleus neurones. Neuroscience, 1984, 13(1), 137-156.
[http://dx.doi.org/10.1016/0306-4522(84)90265-3] [PMID: 6493483]
[82]
Melov, S.; Adlard, P.A.; Morten, K.; Johnson, F.; Golden, T.R.; Hinerfeld, D.; Schilling, B.; Mavros, C.; Masters, C.L.; Volitakis, I.; Li, Q.X.; Laughton, K.; Hubbard, A.; Cherny, R.A.; Gibson, B.; Bush, A.I. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One, 2007, 2(6), e536.
[http://dx.doi.org/10.1371/journal.pone.0000536] [PMID: 17579710]
[83]
Omoluabi, T.; Torraville, S.E.; Maziar, A.; Ghosh, A.; Power, K.D.; Reinhardt, C.; Harley, C.W.; Yuan, Q. Novelty-like activation of locus coeruleus protects against deleterious human pretangle tau effects while stress-inducing activation worsens its effects. Alzheimers Dement., 2021, 7(1), e12231.
[http://dx.doi.org/10.1002/trc2.12231] [PMID: 35005208]
[84]
Jedema, H.P.; Grace, A.A. Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J. Neurosci., 2004, 24(43), 9703-9713.
[http://dx.doi.org/10.1523/JNEUROSCI.2830-04.2004] [PMID: 15509759]
[85]
Ziegler, D.R.; Cass, W.A.; Herman, J.P. Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J. Neuroendocrinol., 1999, 11(5), 361-369.
[http://dx.doi.org/10.1046/j.1365-2826.1999.00337.x] [PMID: 10320563]
[86]
Valentino, R.J.; Foote, S.L.; Aston-Jones, G. Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res., 1983, 270(2), 363-367.
[http://dx.doi.org/10.1016/0006-8993(83)90615-7] [PMID: 6603889]
[87]
Charmandari, E.; Tsigos, C.; Chrousos, G. Endocrinology of the stress response. Annu. Rev. Physiol., 2005, 67(1), 259-284.
[http://dx.doi.org/10.1146/annurev.physiol.67.040403.120816] [PMID: 15709959]
[88]
Dunn, A.J.; Swiergiel, A.H.; Palamarchouk, V. Brain circuits involved in corticotropin-releasing factor-norepinephrine interactions during stress. Ann. N. Y. Acad. Sci., 2004, 1018(1), 25-34.
[http://dx.doi.org/10.1196/annals.1296.003] [PMID: 15240349]
[89]
Cibelli, G.; Corsi, P.; Diana, G.; Vitiello, F.; Thiel, G. Corticotropin-releasing factor triggers neurite outgrowth of a catecholaminergic immortalized neuron via cAMP and MAP kinase signalling pathways. Eur. J. Neurosci., 2001, 13(7), 1339-1348.
[http://dx.doi.org/10.1046/j.0953-816x.2001.01510.x] [PMID: 11298794]
[90]
Mamalaki, E.; Kvetnansky, R.; Brady, L.S.; Gold, P.W.; Herkenham, M. Repeated immobilization stress alters tyrosine hydroxylase, corticotropin-releasing hormone and corticosteroid receptor messenger ribonucleic Acid levels in rat brain. J. Neuroendocrinol., 1992, 4(6), 689-699.
[http://dx.doi.org/10.1111/j.1365-2826.1992.tb00220.x] [PMID: 21554656]
[91]
Salim, S.; Hite, B.; Eikenburg, D.C. Activation of the CRF 1 receptor causes ERK1/2 mediated increase in GRK3 expression in CATH.a cells. FEBS Lett., 2007, 581(17), 3204-3210.
[http://dx.doi.org/10.1016/j.febslet.2007.06.006] [PMID: 17583697]
[92]
Swinny, J.D.; Valentino, R.J. Corticotropin-releasing factor promotes growth of brain norepinephrine neuronal processes through Rho GTPase regulators of the actin cytoskeleton in rat. Eur. J. Neurosci., 2006, 24(9), 2481-2490.
[http://dx.doi.org/10.1111/j.1460-9568.2006.05129.x] [PMID: 17100837]
[93]
Swinny, J.D.; O’Farrell, E.; Bingham, B.C.; Piel, D.A.; Valentino, R.J.; Beck, S.G. Neonatal rearing conditions distinctly shape locus coeruleus neuronal activity, dendritic arborization, and sensitivity to corticotrophin-releasing factor. Int. J. Neuropsychopharmacol., 2010, 13(4), 515-525.
[http://dx.doi.org/10.1017/S146114570999037X] [PMID: 19653930]
[94]
Bornstein, S.R.; Chrousos, G.P. Clinical review 104: Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: Neural and immune inputs. J. Clin. Endocrinol. Metab., 1999, 84(5), 1729-1736.
[http://dx.doi.org/10.1210/jcem.84.5.5631] [PMID: 10323408]
[95]
Tseilikman, V.; Dremencov, E.; Tseilikman, O.; Pavlovicova, M.; Lacinova, L.; Jezova, D. Role of glucocorticoid- and monoamine-metabolizing enzymes in stress-related psychopathological processes. Stress, 2020, 23(1), 1-12.
[http://dx.doi.org/10.1080/10253890.2019.1641080] [PMID: 31322459]
[96]
Matos, T.M.; Souza-Talarico, J.N.D. How stress mediators can cumulatively contribute to Alzheimer’s disease An allostatic load approach. Dement. Neuropsychol., 2019, 13(1), 11-21.
[http://dx.doi.org/10.1590/1980-57642018dn13-010002] [PMID: 31073376]
[97]
McEWEN, B.S. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci., 1998, 840(1), 33-44.
[http://dx.doi.org/10.1111/j.1749-6632.1998.tb09546.x] [PMID: 9629234]
[98]
McEwen, B.S.; Rasgon, N.L. The brain and body on stress: Allostatic load and mechanisms for depression and dementia. Depression as a systemic illness; Oxford University Press: United Kingdom, 2018, pp. 18-36.
[99]
Myers, B.; McKlveen, J.M.; Herman, J.P. Neural regulation of the stress response: The many faces of feedback. Cell. Mol. Neurobiol., 2012, 32(5), 683-694.
[http://dx.doi.org/10.1007/s10571-012-9801-y] [PMID: 22302180]
[100]
Bhatnagar, S.; Vining, C.; Denski, K. Regulation of chronic stress-induced changes in hypothalamic-pituitary-adrenal activity by the basolateral amygdala. Ann. N. Y. Acad. Sci., 2004, 1032(1), 315-319.
[http://dx.doi.org/10.1196/annals.1314.050] [PMID: 15677440]
[101]
Jie, F.; Yin, G.; Yang, W.; Yang, M.; Gao, S.; Lv, J.; Li, B. Stress in regulation of GABA amygdala system and relevance to neuropsychiatric diseases. Front. Neurosci., 2018, 12, 562.
[http://dx.doi.org/10.3389/fnins.2018.00562] [PMID: 30154693]
[102]
Öhman, A. The role of the amygdala in human fear: Automatic detection of threat. Psychoneuroendocrinology, 2005, 30(10), 953-958.
[http://dx.doi.org/10.1016/j.psyneuen.2005.03.019] [PMID: 15963650]
[103]
Herman, J.P.; McKlveen, J.M.; Ghosal, S.; Kopp, B.; Wulsin, A.; Makinson, R.; Scheimann, J.; Myers, B. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr. Physiol., 2016, 6(2), 603-621.
[http://dx.doi.org/10.1002/cphy.c150015] [PMID: 27065163]
[104]
Rohleder, N. Stress and inflammation – The need to address the gap in the transition between acute and chronic stress effects. Psychoneuroendocrinology, 2019, 105, 164-171.
[http://dx.doi.org/10.1016/j.psyneuen.2019.02.021] [PMID: 30826163]
[105]
Makino, S.; Smith, M.A.; Gold, P.W. Regulatory role of glucocorticoids and glucocorticoid receptor mRNA levels on tyrosine hydroxylase gene expression in the Locus coeruleus during repeated immobilization stress. Brain Res., 2002, 943(2), 216-223.
[http://dx.doi.org/10.1016/S0006-8993(02)02647-1] [PMID: 12101044]
[106]
Myhrer, T. Adverse psychological impact, glutamatergic dysfunction, and risk factors for Alzheimer’s disease. Neurosci. Biobehav. Rev., 1998, 23(1), 131-139.
[http://dx.doi.org/10.1016/S0149-7634(98)00039-6] [PMID: 9861617]
[107]
Sapolsky, R.M.; Romero, L.M.; Munck, A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev., 2000, 21(1), 55-89.
[PMID: 10696570]
[108]
Jedema, H.P.; Gold, S.J.; Gonzalez-Burgos, G.; Sved, A.F.; Tobe, B.J.; Wensel, T.G.; Grace, A.A. Chronic cold exposure increases RGS7 expression and decreases α 2 -autoreceptor-mediated inhibition of noradrenergic Locus coeruleus neurons. Eur. J. Neurosci., 2008, 27(9), 2433-2443.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06208.x] [PMID: 18461718]
[109]
Janitzky, K. Impaired phasic discharge of locus coeruleus neurons based on persistent high tonic discharge—a new hypothesis with potential implications for neurodegenerative diseases. Front. Neurol., 2020, 11, 371.
[http://dx.doi.org/10.3389/fneur.2020.00371] [PMID: 32477246]
[110]
Florin-Lechner, S.M.; Druhan, J.P.; Aston-Jones, G.; Valentino, R.J. Enhanced norepinephrine release in prefrontal cortex with burst stimulation of the Locus coeruleus. Brain Res., 1996, 742(1-2), 89-97.
[http://dx.doi.org/10.1016/S0006-8993(96)00967-5] [PMID: 9117425]
[111]
Jhang, K.A.; Lee, E.O.; Kim, H.S.; Chong, Y.H. Norepinephrine provides short-term neuroprotection against Aβ1–42 by reducing oxidative stress independent of Nrf2 activation. Neurobiol. Aging, 2014, 35(11), 2465-2473.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.05.020] [PMID: 24954831]
[112]
Madrigal, J.L.M.; Feinstein, D.L.; Russo, C.D. Norepinephrine protects cortical neurons against microglial-induced cell death. J. Neurosci. Res., 2005, 81(3), 390-396.
[http://dx.doi.org/10.1002/jnr.20481] [PMID: 15948176]
[113]
Bader, V.; Winklhofer, K.F. Mitochondria at the interface between neurodegeneration and neuroinflammation. Semin. Cell Dev. Biol., 2020, 99, 163-171.
[http://dx.doi.org/10.1016/j.semcdb.2019.05.028] [PMID: 31154011]
[114]
Gárate, I.; Garcia-Bueno, B.; Madrigal, J.L.M.; Caso, J.R.; Alou, L.; Gomez-Lus, M.L.; Micó, J.A.; Leza, J.C. Stress-induced neuroinflammation: Role of the Toll-like receptor-4 pathway. Biol. Psychiatry, 2013, 73(1), 32-43.
[http://dx.doi.org/10.1016/j.biopsych.2012.07.005] [PMID: 22906518]
[115]
Munhoz, C.D.; García-Bueno, B.; Madrigal, J.L.M.; Lepsch, L.B.; Scavone, C.; Leza, J.C. Stress-induced neuroinflammation: Mechanisms and new pharmacological targets. Braz. J. Med. Biol. Res., 2008, 41(12), 1037-1046.
[http://dx.doi.org/10.1590/S0100-879X2008001200001] [PMID: 19148364]
[116]
Ghosh, S.; Wu, M.D.; Shaftel, S.S.; Kyrkanides, S.; LaFerla, F.M.; Olschowka, J.A.; O’Banion, M.K. Sustained interleukin-1β overexpression exacerbates tau pathology despite reduced amyloid burden in an Alzheimer’s mouse model. J. Neurosci., 2013, 33(11), 5053-5064.
[http://dx.doi.org/10.1523/JNEUROSCI.4361-12.2013] [PMID: 23486975]
[117]
Hopp, S.C.; Lin, Y.; Oakley, D.; Roe, A.D.; DeVos, S.L.; Hanlon, D.; Hyman, B.T. The role of microglia in processing and spreading of bioactive tau seeds in Alzheimer’s disease. J. Neuroinflammation, 2018, 15(1), 269.
[http://dx.doi.org/10.1186/s12974-018-1309-z] [PMID: 30227881]
[118]
Leyns, C.E.G.; Holtzman, D.M. Glial contributions to neurodegeneration in tauopathies. Mol. Neurodegener., 2017, 12(1), 50.
[http://dx.doi.org/10.1186/s13024-017-0192-x] [PMID: 28662669]
[119]
Metcalfe, M.J.; Figueiredo-Pereira, M.E. Relationship between tau pathology and neuroinflammation in Alzheimer's disease. Mt. Sinai. J. Med., 2010, 77(1), 50-8.
[http://dx.doi.org/10.1002/msj.20163]
[120]
Quintanilla, R.A.; Orellana, D.I.; González-Billault, C.; Maccioni, R.B. Interleukin-6 induces Alzheimer-type phosphorylation of tau protein by deregulating the cdk5/p35 pathway. Exp. Cell. Res., 2004, 295(1), 245-57.
[121]
Finnell, J.E.; Lombard, C.M.; Melson, M.N.; Singh, N.P.; Nagarkatti, M.; Nagarkatti, P.; Fadel, J.R.; Wood, C.S.; Wood, S.K. The protective effects of resveratrol on social stress-induced cytokine release and depressive-like behavior. Brain Behav. Immun., 2017, 59, 147-157.
[http://dx.doi.org/10.1016/j.bbi.2016.08.019] [PMID: 27592314]
[122]
Finnell, J.E.; Moffitt, C.M.; Hesser, L.A.; Harrington, E.; Melson, M.N.; Wood, C.S.; Wood, S.K. The contribution of the locus coeruleus-norepinephrine system in the emergence of defeat-induced inflammatory priming. Brain Behav. Immun., 2019, 79, 102-113.
[http://dx.doi.org/10.1016/j.bbi.2019.01.021] [PMID: 30707932]
[123]
Borodovitsyna, O.; Joshi, N.; Chandler, D. Persistent stress-induced neuroplastic changes in the locus coeruleus/norepinephrine system. Neural Plast., 2018, 2018, 1-14.
[http://dx.doi.org/10.1155/2018/1892570] [PMID: 30008741]
[124]
Dias-Santagata, D.; Fulga, T.A.; Duttaroy, A.; Feany, M.B. Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J. Clin. Invest., 2007, 117(1), 236-245.
[http://dx.doi.org/10.1172/JCI28769] [PMID: 17173140]
[125]
Filipcik, P.; Novak, P.; Mravec, B.; Ondicova, K.; Krajciova, G.; Novak, M.; Kvetnansky, R. Tau protein phosphorylation in diverse brain areas of normal and CRH deficient mice: Up-regulation by stress. Cell. Mol. Neurobiol., 2012, 32(5), 837-845.
[http://dx.doi.org/10.1007/s10571-011-9788-9] [PMID: 22222439]
[126]
Kvetnansky, R.; Novak, P.; Vargovic, P.; Lejavova, K.; Horvathova, L.; Ondicova, K.; Manz, G.; Filipcik, P.; Novak, M.; Mravec, B. Exaggerated phosphorylation of brain tau protein in CRH KO mice exposed to repeated immobilization stress. Stress, 2016, 19(4), 395-405.
[http://dx.doi.org/10.1080/10253890.2016.1183119] [PMID: 27484105]
[127]
Lopes, S.; Vaz-Silva, J.; Pinto, V.; Dalla, C.; Kokras, N.; Bedenk, B.; Mack, N.; Czisch, M.; Almeida, O.F.X.; Sousa, N.; Sotiropoulos, I. Tau protein is essential for stress-induced brain pathology. Proc. Natl. Acad. Sci. USA, 2016, 113(26), E3755-E3763.
[http://dx.doi.org/10.1073/pnas.1600953113] [PMID: 27274066]
[128]
Okawa, Y.; Ishiguro, K.; Fujita, S.C. Stress-induced hyperphosphorylation of tau in the mouse brain. FEBS Lett., 2003, 535(1-3), 183-189.
[http://dx.doi.org/10.1016/S0014-5793(02)03883-8] [PMID: 12560101]
[129]
Sotiropoulos, I.; Catania, C.; Pinto, L.G.; Silva, R.; Pollerberg, G.E.; Takashima, A.; Sousa, N.; Almeida, O.F.X. Stress acts cumulatively to precipitate Alzheimer’s disease-like tau pathology and cognitive deficits. J. Neurosci., 2011, 31(21), 7840-7847.
[http://dx.doi.org/10.1523/JNEUROSCI.0730-11.2011] [PMID: 21613497]
[130]
Carroll, J.C.; Iba, M.; Bangasser, D.A.; Valentino, R.J.; James, M.J.; Brunden, K.R.; Lee, V.M.Y.; Trojanowski, J.Q. 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., 2011, 31(40), 14436-14449.
[http://dx.doi.org/10.1523/JNEUROSCI.3836-11.2011] [PMID: 21976528]
[131]
Chalermpalanupap, T.; Weinshenker, D.; Rorabaugh, J.M. Down but not out: The consequences of pretangle tau in the locus coeruleus. Neural Plast., 2017, 2017, 1-9.
[http://dx.doi.org/10.1155/2017/7829507] [PMID: 29038736]
[132]
Weinshenker, D. Long road to ruin: Noradrenergic dysfunction in neurodegenerative disease. Trends Neurosci., 2018, 41(4), 211-223.
[http://dx.doi.org/10.1016/j.tins.2018.01.010] [PMID: 29475564]
[133]
Kang, S.S.; Liu, X.; Ahn, E.H.; Xiang, J.; Manfredsson, F.P.; Yang, X.; Luo, H.R.; Liles, L.C.; Weinshenker, D.; Ye, K. Norepinephrine metabolite DOPEGAL activates AEP and pathological Tau aggregation in locus coeruleus. J. Clin. Invest., 2019, 130(1), 422-437.
[http://dx.doi.org/10.1172/JCI130513] [PMID: 31793911]
[134]
Zhang, Z.; Song, M.; Liu, X.; Kang, S.S.; Kwon, I.S.; Duong, D.M.; Seyfried, N.T.; Hu, W.T.; Liu, Z.; Wang, J.Z.; Cheng, L.; Sun, Y.E.; Yu, S.P.; Levey, A.I.; Ye, K. Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer’s disease. Nat. Med., 2014, 20(11), 1254-1262.
[http://dx.doi.org/10.1038/nm.3700] [PMID: 25326800]
[135]
Liu, H.; Yang, Z.; Yu, C.; Dong, H.; Wang, S.; Wang, G.; Wang, D. Tau aggravates stress-induced anxiety by inhibiting adult ventral hippocampal neurogenesis in mice. Cereb. Cortex, 2022.
[PMID: 36047921]
[136]
Chen, S.D.; Lu, J.Y.; Li, H.Q.; Yang, Y.X.; Jiang, J.H.; Cui, M.; Zuo, C.T.; Tan, L.; Dong, Q.; Yu, J.T.; Weiner, M.W.; Aisen, P.; Petersen, R.; Jack, C.R., Jr; Jagust, W.; Trojanowki, J.Q.; Toga, A.W.; Beckett, L.; Green, R.C.; Saykin, A.J.; Morris, J.C.; Perrin, R.J.; Shaw, L.M.; Carrillo, M.; Potter, W.; Barnes, L.; Bernard, M.; González, H.; Ho, C.; Hsiao, J.K.; Jackson, J.; Masliah, E.; Masterman, D.; Okonkwo, O.; Perrin, R.; Ryan, L.; Silverberg, N.; Fleisher, A.; Sacrey, D.T.; Fockler, J.; Conti, C.; Veitch, D.; Neuhaus, J.; Jin, C.; Nosheny, R.; Ashford, M.; Flenniken, D.; Kormos, A.; Rafii, M.; Raman, R.; Jimenez, G.; Donohue, M.; Gessert, D.; Salazar, J.; Zimmerman, C.; Cabrera, Y.; Walter, S.; Miller, G.; Coker, G.; Clanton, T.; Hergesheimer, L.; Smith, S.; Adegoke, O.; Mahboubi, P.; Moore, S.; Pizzola, J.; Shaffer, E.; Sloan, B.; Harvey, D.; Forghanian-Arani, A.; Borowski, B.; Ward, C.; Schwarz, C.; Jones, D.; Gunter, J.; Kantarci, K.; Senjem, M.; Vemuri, P.; Reid, R.; Fox, N.C.; Malone, I.; Thompson, P.; Thomopoulos, S.I.; Nir, T.M.; Jahanshad, N.; DeCarli, C.; Knaack, A.; Fletcher, E.; Tosun-Turgut, D.; Chen, S.R.; Choe, M.; Crawford, K.; Yushkevich, P.A.; Das, S.; Koeppe, R.A.; Reiman, E.M.; Chen, K.; Mathis, C.; Landau, S.; Cairns, N.J.; Householder, E.; Franklin, E.; Bernhardt, H.; Taylor-Reinwald, L.; Shaw, L.M.; Trojanowki, J.Q.; Korecka, M.; Figurski, M.; Crawford, K.; Neu, S.; Saykin, A.J.; Nho, K.; Risacher, S.L.; Apostolova, L.G.; Shen, L.; Foroud, T.M.; Nudelman, K.; Faber, K.; Wilmes, K.; Thal, L.; Khachaturian, Z.; Hsiao, J.K.; Silbert, L.C.; Lind, B.; Crissey, R.; Kaye, J.A.; Carter, R.; Dolen, S.; Quinn, J.; Schneider, L.S.; Pawluczyk, S.; Becerra, M.; Teodoro, L.; Dagerman, K.; Spann, B.M.; Brewer, J.; Vanderswag, H.; Fleisher, A.; Ziolkowski, J.; Heidebrink, J.L.; Zbizek-Nulph, L.; Lord, J.L.; Mason, S.S.; Albers, C.S.; Knopman, D.; Johnson, K.; Villanueva-Meyer, J.; Pavlik, V.; Pacini, N.; Lamb, A.; Kass, J.S.; Doody, R.S.; Shibley, V.; Chowdhury, M.; Rountree, S.; Dang, M.; Stern, Y.; Honig, L.S.; Mintz, A.; Ances, B.; Winkfield, D.; Carroll, M.; Stobbs-Cucchi, G.; Oliver, A.; Creech, M.L.; Mintun, M.A.; Schneider, S.; Geldmacher, D.; Love, M.N.; Griffith, R.; Clark, D.; Brockington, J.; Marson, D.; Grossman, H.; Goldstein, M.A.; Greenberg, J.; Mitsis, E.; Shah, R.C.; Lamar, M.; Samuels, P.; Duara, R.; Greig-Custo, M.T.; Rodriguez, R.; Albert, M.; Onyike, C.; Farrington, L.; Rudow, S.; Brichko, R.; Kielb, S.; Smith, A.; Raj, B.A.; Fargher, K.; Sadowski, M.; Wisniewski, T.; Shulman, M.; Faustin, A.; Rao, J.; Castro, K.M.; Ulysse, A.; Chen, S.; Sheikh, M.O.; Singleton-Garvin, J.; Doraiswamy, P.M.; Petrella, J.R.; James, O.; Wong, T.Z.; Borges-Neto, S.; Karlawish, J.H.; Wolk, D.A.; Vaishnavi, S.; Clark, C.M.; Arnold, S.E.; Smith, C.D.; Jicha, G.A.; El Khouli, R.; Raslau, F.D.; Lopez, O.L.; Oakley, M.A.; Simpson, D.M.; Porsteinsson, A.P.; Martin, K.; Kowalski, N.; Keltz, M.; Goldstein, B.S.; Makino, K.M.; Ismail, M.S.; Brand, C.; Thai, G.; Pierce, A.; Yanez, B.; Sosa, E.; Witbracht, M.; Kelley, B.; Nguyen, T.; Womack, K.; Mathews, D.; Quiceno, M.; Levey, A.I.; Lah, J.J.; Hajjar, I.; Cellar, J.S.; Burns, J.M.; Swerdlow, R.H.; Brooks, W.M.; Silverman, D.H.S.; Kremen, S.; Apostolova, L.; Tingus, K.; Lu, P.H.; Bartzokis, G.; Woo, E.; Teng, E.; Graff-Radford, N.R.; Parfitt, F.; Poki-Walker, K.; Farlow, M.R.; Hake, A.M.; Matthews, B.R.; Brosch, J.R.; Herring, S.; van Dyck, C.H.; Mecca, A.P.; Good, S.P.; MacAvoy, M.G.; Carson, R.E.; Varma, P.; Chertkow, H.; Vaitekunis, S.; Hosein, C.; Black, S.; Stefanovic, B.; Heyn, C.; Hsiung, G-Y.R.; Kim, E.; Mudge, B.; Sossi, V.; Feldman, H.; Assaly, M.; Finger, E.; Pasternak, S.; Rachinsky, I.; Kertesz, A.; Drost, D.; Rogers, J.; Grant, I.; Muse, B.; Rogalski, E.; Robson, J.; Mesulam, M-M.; Kerwin, D.; Wu, C-K.; Johnson, N.; Lipowski, K.; Weintraub, S.; Bonakdarpour, B.; Pomara, N.; Hernando, R.; Sarrael, A.; Rosen, H.J.; Miller, B.L.; Perry, D.; Turner, R.S.; Johnson, K.; Reynolds, B.; MCCann, K.; Poe, J.; Sperling, R.A.; Johnson, K.A.; Marshall, G.A.; Belden, C.M.; Atri, A.; Spann, B.M.; Clark, K.A.; Zamrini, E.; Sabbagh, M.; Killiany, R.; Stern, R.; Mez, J.; Kowall, N.; Budson, A.E.; Obisesan, T.O.; Ntekim, O.E.; Wolday, S.; Khan, J.I.; Nwulia, E.; Nadarajah, S.; Lerner, A.; Ogrocki, P.; Tatsuoka, C.; Fatica, P.; Fletcher, E.; Maillard, P.; Olichney, J.; DeCarli, C.; Carmichael, O.; Bates, V.; Capote, H.; Rainka, M.; Borrie, M.; Lee, T-Y.; Bartha, R.; Johnson, S.; Asthana, S.; Carlsson, C.M.; Perrin, A.; Burke, A.; Scharre, D.W.; Kataki, M.; Tarawneh, R.; Kelley, B.; Hart, D.; Zimmerman, E.A.; Celmins, D.; Miller, D.D.; Boles Ponto, L.L.; Smith, K.E.; Koleva, H.; Shim, H.; Nam, K.W.; Schultz, S.K.; Williamson, J.D.; Craft, S.; Cleveland, J.; Yang, M.; Sink, K.M.; Ott, B.R.; Drake, J.; Tremont, G.; Daiello, L.A.; Drake, J.D.; Sabbagh, M.; Ritter, A.; Bernick, C.; Munic, D.; Mintz, A.; O’Connelll, A.; Mintzer, J.; Wiliams, A.; Masdeu, J.; Shi, J.; Garcia, A.; Sabbagh, M.; Newhouse, P.; Potkin, S.; Salloway, S.; Malloy, P.; Correia, S.; Kittur, S.; Pearlson, G.D.; Blank, K.; Anderson, K.; Flashman, L.A.; Seltzer, M.; Hynes, M.L.; Santulli, R.B.; Relkin, N.; Chiang, G.; Lin, M.; Ravdin, L.; Lee, A.; Petersen, R.; Neylan, T.; Grafman, J.; Montine, T.; Petersen, R.; Hergesheimer, L.; Danowski, S.; Nguyen-Barrera, C.; Hayes, J.; Finley, S.; Donohue, M.; Bernstein, M.; Senjem, M.; Ward, C.; Chen, S.R.; Koeppe, R.A.; Foster, N.; Foroud, T.M.; Potkin, S.; Shen, L.; Faber, K.; Kim, S.; Nho, K.; Wilmes, K.; Spann, B.M.; Vanderswag, H.; Fleisher, A.; Sood, A.; Blanchard, K.S.; Fleischman, D.; Arfanakis, K.; Varon, D.; Greig, M.T.; Goldstein, B.; Martin, K.S.; Thai, G.; Pierce, A.; Reist, C.; Yanez, B.; Sosa, E.; Witbracht, M.; Sadowsky, C.; Martinez, W.; Villena, T.; Rosen, H.; Marshall, G.; Nadarajah, S.; Peskind, E.R.; Petrie, E.C.; Li, G.; Yesavage, J.; Taylor, J.L.; Chao, S.; Coleman, J.; White, J.D.; Lane, B.; Rosen, A.; Tinklenberg, J.; Chiang, G.; Mackin, S.; Raman, R.; Jimenez-Maggiora, G.; Gessert, D.; Salazar, J.; Zimmerman, C.; Walter, S.; Adegoke, O.; Mahboubi, P.; Drake, E.; Donohue, M.; Nelson, C.; Bickford, D.; Butters, M.; Zmuda, M.; Borowski, B.; Gunter, J.; Senjem, M.; Kantarci, K.; Ward, C.; Reyes, D.; Faber, K.M.; Nudelman, K.N.; Au, Y.H.; Scherer, K.; Catalinotto, D.; Stark, S.; Ong, E.; Fernandez, D.; Zmuda, M. Staging tau pathology with tau PET in Alzheimer’s disease: A longitudinal study. Transl. Psychiatry, 2021, 11(1), 483.
[http://dx.doi.org/10.1038/s41398-021-01602-5] [PMID: 34537810]
[137]
Weldemichael, D.A.; Grossberg, G.T. Circadian rhythm disturbances in patients with Alzheimer’s disease: A review. Int. J. Alzheimers Dis., 2010, 2010, 1-9.
[http://dx.doi.org/10.4061/2010/716453] [PMID: 20862344]
[138]
Guidi, J.; Lucente, M.; Sonino, N.; Fava, G.A. Allostatic load and its impact on health: A systematic review. Psychother. Psychosom., 2021, 90(1), 11-27.
[http://dx.doi.org/10.1159/000510696] [PMID: 32799204]
[139]
Letra, L.; Santana, I.; Seiça, R. Obesity as a risk factor for Alzheimer’s disease: The role of adipocytokines. Metab. Brain Dis., 2014, 29(3), 563-568.
[http://dx.doi.org/10.1007/s11011-014-9501-z] [PMID: 24553879]
[140]
Jorm, A.F.; Van Duijn, C.M.; Chandra, V.; Fratiglioni, L.; Graves, A.B.; Heyman, A.; Kokmen, E.; Kondo, K.; Mortimer, J.A.; Rocca, W.A.; Shalat, S.L.; Soininen, H. Psychiatric history and related exposures as risk factors for Alzheimer’s disease: A collaborative re-analysis of case-control studies. Int. J. Epidemiol., 1991, 20(Suppl. 2), S43-S47.
[http://dx.doi.org/10.1093/ije/20.Supplement_2.S43] [PMID: 1917269]
[141]
Bekar, L.K.; Wei, H.S.; Nedergaard, M. The locus coeruleus-norepinephrine network optimizes coupling of cerebral blood volume with oxygen demand. J. Cereb. Blood Flow Metab., 2012, 32(12), 2135-2145.
[http://dx.doi.org/10.1038/jcbfm.2012.115] [PMID: 22872230]
[142]
Raichle, M.E.; Hartman, B.K.; Eichling, J.O.; Sharpe, L.G. Central noradrenergic regulation of cerebral blood flow and vascular permeability. Proc. Natl. Acad. Sci. USA, 1975, 72(9), 3726-3730.
[http://dx.doi.org/10.1073/pnas.72.9.3726] [PMID: 810805]
[143]
Toussay, X.; Basu, K.; Lacoste, B.; Hamel, E. Locus coeruleus stimulation recruits a broad cortical neuronal network and increases cortical perfusion. J. Neurosci., 2013, 33(8), 3390-3401.
[http://dx.doi.org/10.1523/JNEUROSCI.3346-12.2013] [PMID: 23426667]
[144]
Follesa, P.; Biggio, F.; Gorini, G.; Caria, S.; Talani, G.; Dazzi, L.; Puligheddu, M.; Marrosu, F.; Biggio, G. Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Res., 2007, 1179, 28-34.
[http://dx.doi.org/10.1016/j.brainres.2007.08.045] [PMID: 17920573]
[145]
Heneka, M.T.; Nadrigny, F.; Regen, T.; Martinez-Hernandez, A.; Dumitrescu-Ozimek, L.; Terwel, D.; Jardanhazi-Kurutz, D.; Walter, J.; Kirchhoff, F.; Hanisch, U.K.; Kummer, M.P. Locus ceruleus controls Alzheimer’s disease pathology by modulating microglial functions through norepinephrine. Proc. Natl. Acad. Sci. USA, 2010, 107(13), 6058-6063.
[http://dx.doi.org/10.1073/pnas.0909586107] [PMID: 20231476]
[146]
Liu, H.; Leak, R.K.; Hu, X. Neurotransmitter receptors on microglia. BMJ, 2016, 1(2), 52-58.
[http://dx.doi.org/10.1136/svn-2016-000012] [PMID: 28959464]
[147]
Johnson, J.D.; Campisi, J.; Sharkey, C.M.; Kennedy, S.L.; Nickerson, M.; Greenwood, B.N.; Fleshner, M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience, 2005, 135(4), 1295-1307.
[http://dx.doi.org/10.1016/j.neuroscience.2005.06.090] [PMID: 16165282]
[148]
Mori, K.; Ozaki, E.; Zhang, B.; Yang, L.; Yokoyama, A.; Takeda, I.; Maeda, N.; Sakanaka, M.; Tanaka, J. Effects of norepinephrine on rat cultured microglial cells that express α1, α2, β1 and β2 adrenergic receptors. Neuropharmacology, 2002, 43(6), 1026-1034.
[http://dx.doi.org/10.1016/S0028-3908(02)00211-3] [PMID: 12423672]
[149]
Muresan, Z.; Muresan, V. Seeding neuritic plaques from the distance: A possible role for brainstem neurons in the development of Alzheimer’s disease pathology. Neurodegener. Dis., 2008, 5(3-4), 250-253.
[http://dx.doi.org/10.1159/000113716] [PMID: 18322404]
[150]
Amadoro, G.; Corsetti, V.; Ciotti, M.T.; Florenzano, F.; Capsoni, S.; Amato, G.; Calissano, P. Endogenous Aβ causes cell death via early tau hyperphosphorylation. Neurobiol. Aging, 2011, 32(6), 969-990.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.06.005] [PMID: 19628305]
[151]
Greenberg, S.M.; Koo, E.H.; Selkoe, D.J.; Qiu, W.Q.; Kos, I.K. Secreted beta-amyloid precursor protein stimulates mitogen-activated protein kinase and enhances tau phosphorylation. Proc. Natl. Acad. Sci., 1994, 91, pp. 7104-7108.
[http://dx.doi.org/10.1073/pnas.91.15.7104]
[152]
He, Z.; Guo, J.L.; McBride, J.D.; Narasimhan, S.; Kim, H.; Changolkar, L.; Zhang, B.; Gathagan, R.J.; Yue, C.; Dengler, C.; Stieber, A.; Nitla, M.; Coulter, D.A.; Abel, T.; Brunden, K.R.; Trojanowski, J.Q.; Lee, V.M.Y. Amyloid-β plaques enhance Alzheimer’s brain tau-seeded pathologies by facilitating neuritic plaque tau aggregation. Nat. Med., 2018, 24(1), 29-38.
[http://dx.doi.org/10.1038/nm.4443] [PMID: 29200205]
[153]
Shin, W.S.; Di, J.; Cao, Q.; Li, B.; Seidler, P.M.; Murray, K.A.; Bitan, G.; Jiang, L. Amyloid β-protein oligomers promote the uptake of tau fibril seeds potentiating intracellular tau aggregation. Alzheimers Res. Ther., 2019, 11(1), 86.
[http://dx.doi.org/10.1186/s13195-019-0541-9] [PMID: 31627745]
[154]
Reynolds, C.H.; Garwood, C.J.; Wray, S.; Price, C.; Kellie, S.; Perera, T.; Zvelebil, M.; Yang, A.; Sheppard, P.W.; Varndell, I.M.; Hanger, D.P.; Anderton, B.H. Phosphorylation regulates tau interactions with Src homology 3 domains of phosphatidylinositol 3-kinase, phospholipase Cgamma1, Grb2, and Src family kinases. J. Biol. Chem., 2008, 283(26), 18177-18186.
[http://dx.doi.org/10.1074/jbc.M709715200] [PMID: 18467332]
[155]
Gonçalves, R.A.; Wijesekara, N.; Fraser, P.E.; De Felice, F.G. The link between tau and insulin signaling: Implications for Alzheimer’s disease and other tauopathies. Front. Cell. Neurosci., 2019, 13, 17.
[http://dx.doi.org/10.3389/fncel.2019.00017] [PMID: 30804755]
[156]
De Felice, F.G.; Gonçalves, R.A.; Ferreira, S.T. Impaired insulin signalling and allostatic load in Alzheimer disease. Nat. Rev. Neurosci., 2022, 23(4), 215-230.
[http://dx.doi.org/10.1038/s41583-022-00558-9] [PMID: 35228741]
[157]
Ohta, Y.; Kinugawa, S.; Matsushima, S.; Ono, T.; Sobirin, M.A.; Inoue, N.; Yokota, T.; Hirabayashi, K.; Tsutsui, H. Oxidative stress impairs insulin signal in skeletal muscle and causes insulin resistance in postinfarct heart failure. Am. J. Physiol. Heart Circ. Physiol., 2011, 300(5), H1637-H1644.
[http://dx.doi.org/10.1152/ajpheart.01185.2009] [PMID: 21335475]
[158]
Zardooz, H.; Sadeghimahalli, F.; Khodagholi, F. Early postnatal stress impairs insulin secretion in response to psychological stress in adult rats. J. Endocrinol. Invest., 2021, 44(2), 277-286.
[http://dx.doi.org/10.1007/s40618-020-01291-9] [PMID: 32458408]
[159]
Rogers, J.; Strohmeyer, R.; Kovelowski, C.J.; Li, R. Microglia and inflammatory mechanisms in the clearance of amyloid β peptide. Glia, 2002, 40(2), 260-269.
[http://dx.doi.org/10.1002/glia.10153] [PMID: 12379913]
[160]
Bona, D.; Scapagnini, G.; Candore, G.; Castiglia, L.; Colonna-Romano, G.; Duro, G.; Nuzzo, D.; Iemolo, F.; Lio, D.; Pellicanò, M.; Scafidi, V.; Caruso, C.; Vasto, S. Immune-inflammatory responses and oxidative stress in Alzheimer’s disease: Therapeutic implications. Curr. Pharm. Des., 2010, 16(6), 684-691.
[http://dx.doi.org/10.2174/138161210790883769] [PMID: 20388078]
[161]
Blasko, I.; Stampfer-Kountchev, M.; Robatscher, P.; Veerhuis, R.; Eikelenboom, P.; Grubeck-Loebenstein, B. How chronic inflammation can affect the brain and support the development of Alzheimer’s disease in old age: The role of microglia and astrocytes. Aging Cell, 2004, 3(4), 169-176.
[http://dx.doi.org/10.1111/j.1474-9728.2004.00101.x] [PMID: 15268750]
[162]
Bright, J.; Hussain, S.; Dang, V.; Wright, S.; Cooper, B.; Byun, T.; Ramos, C.; Singh, A.; Parry, G.; Stagliano, N.; Griswold-Prenner, I. Human secreted tau increases amyloid-beta production. Neurobiol. Aging, 2015, 36(2), 693-709.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.09.007] [PMID: 25442111]
[163]
Butterfield, D.A.; Lauderback, C.M. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: Potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic. Biol. Med., 2002, 32(11), 1050-1060.
[http://dx.doi.org/10.1016/S0891-5849(02)00794-3] [PMID: 12031889]
[164]
Eikelenboom, P.; Veerhuis, R.; van Exel, E.; Hoozemans, J.J.; Rozemuller, A.J.; van Gool, W.A. The early involvement of the innate immunity in the pathogenesis of late-onset Alzheimer’s disease: Neuropathological, epidemiological and genetic evidence. Curr. Alzheimer Res., 2011, 8(2), 142-150.
[http://dx.doi.org/10.2174/156720511795256080] [PMID: 21345167]
[165]
Heneka, M.; Obanion, M. Inflammatory processes in Alzheimer’s disease. J. Neuroimmunol., 2007, 184(1-2), 69-91.
[http://dx.doi.org/10.1016/j.jneuroim.2006.11.017] [PMID: 17222916]
[166]
Devi, L.; Prabhu, B.M.; Galati, D.F.; Avadhani, N.G.; Anandatheerthavarada, H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer’s disease brain is associated with mitochondrial dysfunction. J. Neurosci., 2006, 26(35), 9057-9068.
[http://dx.doi.org/10.1523/JNEUROSCI.1469-06.2006] [PMID: 16943564]
[167]
Zhao, Y.; Zhao, B. Oxidative stress and the pathogenesis of Alzheimer’s disease. Oxid. Med. Cell. Longev., 2013, 2013, 1-10.
[http://dx.doi.org/10.1155/2013/316523] [PMID: 23983897]
[168]
Cheng, Y.; Bai, F. The association of tau with mitochondrial dysfunction in Alzheimer’s disease. Front. Neurosci., 2018, 12, 163.
[http://dx.doi.org/10.3389/fnins.2018.00163] [PMID: 29623026]
[169 ]
Uddin, M.S.; Kabir, M.T.; Al Mamun, A.; Abdel-Daim, M.M.; Barreto, G.E.; Ashraf, G.M. APOE and Alzheimer’s disease: Evidence mounts that targeting APOE4 may combat Alzheimer’s pathogenesis. Mol. Neurobiol., 2019, 56(4), 2450-2465.
[http://dx.doi.org/10.1007/s12035-018-1237-z] [PMID: 30032423]
[170]
Hoeijmakers, L.; Lesuis, S.L.; Krugers, H.; Lucassen, P.J.; Korosi, A. A preclinical perspective on the enhanced vulnerability to Alzheimer’s disease after early-life stress. Neurobiol. Stress, 2018, 8, 172-185.
[http://dx.doi.org/10.1016/j.ynstr.2018.02.003] [PMID: 29888312]
[171]
Lemche, E. Early life stress and epigenetics in late-onset Alzheimer’s dementia: A systematic review. Curr. Genomics, 2018, 19(7), 522-602.
[http://dx.doi.org/10.2174/1389202919666171229145156] [PMID: 30386171]
[172]
Hoeijmakers, L.; Ruigrok, S.R.; Amelianchik, A.; Ivan, D.; van Dam, A.M.; Lucassen, P.J.; Korosi, A. Early-life stress lastingly alters the neuroinflammatory response to amyloid pathology in an Alzheimer’s disease mouse model. Brain Behav. Immunol., 2017, 63, 160-175.
[http://dx.doi.org/10.1016/j.bbi.2016.12.023] [PMID: 28027926]
[173]
Kloske, C.M.; Wilcock, D.M. The important interface between apolipoprotein E and neuroinflammation in Alzheimer’s disease. Front. Immunol., 2020, 11, 754.
[http://dx.doi.org/10.3389/fimmu.2020.00754] [PMID: 32425941]
[174]
Gale, S.C.; Gao, L.; Mikacenic, C.; Coyle, S.M.; Rafaels, N.; Murray Dudenkov, T.; Madenspacher, J.H.; Draper, D.W.; Ge, W.; Aloor, J.J.; Azzam, K.M.; Lai, L.; Blackshear, P.J.; Calvano, S.E.; Barnes, K.C.; Lowry, S.F.; Corbett, S.; Wurfel, M.M.; Fessler, M.B. APOε4 is associated with enhanced in vivo innate immune responses in human subjects. J. Allergy Clin. Immunol., 2014, 134(1), 127-134.e9.
[http://dx.doi.org/10.1016/j.jaci.2014.01.032] [PMID: 24655576]
[175]
Shi, Y.; Yamada, K.; Liddelow, S.A.; Smith, S.T.; Zhao, L.; Luo, W.; Tsai, R.M.; Spina, S.; Grinberg, L.T.; Rojas, J.C.; Gallardo, G.; Wang, K.; Roh, J.; Robinson, G.; Finn, M.B.; Jiang, H.; Sullivan, P.M.; Baufeld, C.; Wood, M.W.; Sutphen, C.; McCue, L.; Xiong, C.; Del-Aguila, J.L.; Morris, J.C.; Cruchaga, C.; Fagan, A.M.; Miller, B.L.; Boxer, A.L.; Seeley, W.W.; Butovsky, O.; Barres, B.A.; Paul, S.M.; Holtzman, D.M. ApoE4 markedly exacerbates tau-mediated neurodegeneration in a mouse model of tauopathy. Nature, 2017, 549(7673), 523-527.
[http://dx.doi.org/10.1038/nature24016] [PMID: 28959956]
[176]
Montal, V.; Diez, I.; Kim, C.M.; Orwig, W.; Bueichekú, E.; Gutiérrez-Zúñiga, R.; Bejanin, A.; Pegueroles, J.; Dols-Icardo, O.; Vannini, P.; El-Fakhri, G.; Johnson, K.A.; Sperling, R.A.; Fortea, J.; Sepulcre, J. Network Tau spreading is vulnerable to the expression gradients of APOE and glutamatergic-related genes. Sci. Transl. Med., 2022, 14(655), eabn7273.
[http://dx.doi.org/10.1126/scitranslmed.abn7273] [PMID: 35895837]
[177]
Robertson, J.; Curley, J.; Kaye, J.; Quinn, J.; Pfankuch, T.; Raber, J. apoE isoforms and measures of anxiety in probable AD patients and Apoe−/− mice. Neurobiol. Aging, 2005, 26(5), 637-643.
[http://dx.doi.org/10.1016/j.neurobiolaging.2004.06.003] [PMID: 15708438]
[178]
Villasana, L.E.; Weber, S.; Akinyeke, T.; Raber, J. Genotype differences in anxiety and fear learning and memory of WT and ApoE4 mice associated with enhanced generation of hippocampal reactive oxygen species. J. Neurochem., 2016, 138(6), 896-908.
[http://dx.doi.org/10.1111/jnc.13737] [PMID: 27412623]
[179]
Lin, L.; Zhang, J.; Dai, X.; Xiao, N.; Wu, X.; Wei, Z.; Fang, W.; Zhu, Y.; Chen, X. Early-life stress leads to impaired spatial learning and memory in middle-aged ApoE4-TR mice. Mol. Neurodegener., 2016, 11(1), 51.
[http://dx.doi.org/10.1186/s13024-016-0107-2] [PMID: 27406263]
[180]
Fang, W.; Xiao, N.; Zeng, G.; Bi, D.; Dai, X.; Mi, X.; Ye, Q.; Chen, X.; Zhang, J. APOE4 genotype exacerbates the depression-like behavior of mice during aging through ATP decline. Transl. Psychiatry, 2021, 11(1), 1-9.
[PMID: 33414379]
[181]
Yen, Y.C.; Rebok, G.W.; Gallo, J.J.; Yang, M.J.; Lung, F.W.; Shih, C.H. ApoE4 allele is associated with late-life depression: A population-based study. Am. J. Geriatr. Psychiatry, 2007, 15(10), 858-868.
[http://dx.doi.org/10.1097/JGP.0b013e3180f63373] [PMID: 17911363]
[182]
Bisht, K.; Sharma, K.; Tremblay, M.È. Chronic stress as a risk factor for Alzheimer’s disease: Roles of microglia-mediated synaptic remodeling, inflammation, and oxidative stress. Neurobiol. Stress, 2018, 9, 9-21.
[http://dx.doi.org/10.1016/j.ynstr.2018.05.003] [PMID: 29992181]
[183]
Caruso, A.; Nicoletti, F.; Mango, D.; Saidi, A.; Orlando, R.; Scaccianoce, S. Stress as risk factor for Alzheimer’s disease. Pharmacol. Res., 2018, 132, 130-134.
[http://dx.doi.org/10.1016/j.phrs.2018.04.017] [PMID: 29689315]
[184]
Machado, A.; Herrera, A.J.; de Pablos, R.M.; Espinosa-Oliva, A.M.; Sarmiento, M.; Ayala, A.; Venero, J.L.; Santiago, M.; Villarán, R.F.; Delgado-Cortés, M.J.; Argüelles, S.; Cano, J. Chronic stress as a risk factor for Alzheimer’s disease. Rev. Neurosci., 2014, 25(6), 785-804.
[http://dx.doi.org/10.1515/revneuro-2014-0035] [PMID: 25178904]
[185]
Escher, C.M.; Sannemann, L.; Jessen, F. Stress and Alzheimer’s disease. J. Neural Transm. (Vienna), 2019, 126(9), 1155-1161.
[http://dx.doi.org/10.1007/s00702-019-01988-z] [PMID: 30788601]
[186]
Ennis, G.E.; An, Y.; Resnick, S.M.; Ferrucci, L.; O’Brien, R.J.; Moffat, S.D. Long-term cortisol measures predict Alzheimer disease risk. Neurology, 2017, 88(4), 371-378.
[http://dx.doi.org/10.1212/WNL.0000000000003537] [PMID: 27986873]
[187]
Wilson, R.S.; Fleischman, D.A.; Myers, R.A.; Bennett, D.A.; Bienias, J.L.; Gilley, D.W.; Evans, D.A. Premorbid proneness to distress and episodic memory impairment in Alzheimer’s disease. J. Neurol. Neurosurg. Psychiatry, 2004, 75(2), 191-195.
[PMID: 14742585]
[188]
Wilson, R.S.; Begeny, C.T.; Boyle, P.A.; Schneider, J.A.; Bennett, D.A. Vulnerability to stress, anxiety, and development of dementia in old age. Am. J. Geriatr. Psychiatry, 2011, 19(4), 327-334.
[http://dx.doi.org/10.1097/JGP.0b013e31820119da] [PMID: 21427641]
[189]
Parent, J.H.; Ciampa, C.J.; Harrison, T.M.; Adams, J.N.; Zhuang, K.; Betts, M.J.; Maass, A.; Winer, J.R.; Jagust, W.J.; Berry, A.S. Locus coeruleus catecholamines link neuroticism and vulnerability to tau pathology in aging. Neuroimage, 2022, 263, 119658.
[http://dx.doi.org/10.1016/j.neuroimage.2022.119658] [PMID: 36191755]
[190]
McCall, J.G.; Al-Hasani, R.; Siuda, E.R.; Hong, D.Y.; Norris, A.J.; Ford, C.P.; Bruchas, M.R. CRH engagement of the locus coeruleus noradrenergic system mediates stress-induced anxiety. Neuron, 2015, 87(3), 605-620.
[http://dx.doi.org/10.1016/j.neuron.2015.07.002] [PMID: 26212712]
[191]
Zitnik, G.A.; Curtis, A.L.; Wood, S.K.; Arner, J.; Valentino, R.J. Adolescent social stress produces an enduring activation of the rat locus coeruleus and alters its coherence with the prefrontal cortex. Neuropsychopharmacology, 2016, 41(5), 1376-1385.
[http://dx.doi.org/10.1038/npp.2015.289] [PMID: 26361057]
[192]
Grueschow, M.; Stenz, N.; Thörn, H.; Ehlert, U.; Breckwoldt, J.; Brodmann Maeder, M.; Exadaktylos, A.K.; Bingisser, R.; Ruff, C.C.; Kleim, B. Real-world stress resilience is associated with the responsivity of the locus coeruleus. Nat. Commun., 2021, 12(1), 2275.
[http://dx.doi.org/10.1038/s41467-021-22509-1] [PMID: 33859187]
[193]
Southwick, S.M.; Krystal, J.H.; Bremner, J.D.; Morgan, C.A., III; Nicolaou, A.L.; Nagy, L.M.; Johnson, D.R.; Heninger, G.R.; Charney, D.S. Noradrenergic and serotonergic function in posttraumatic stress disorder. Arch. Gen. Psychiatry, 1997, 54(8), 749-758.
[http://dx.doi.org/10.1001/archpsyc.1997.01830200083012] [PMID: 9283511]
[194]
Wong, M.L.; Kling, M.A.; Munson, P.J.; Listwak, S.; Licinio, J.; Prolo, P.; Karp, B.; McCutcheon, I.E.; Geracioti, T.D., Jr; DeBellis, M.D.; Rice, K.C.; Goldstein, D.S.; Veldhuis, J.D.; Chrousos, G.P.; Oldfield, E.H.; McCann, S.M.; Gold, P.W. Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: Relation to hypercortisolism and corticotropin-releasing hormone. Proc. Natl. Acad. Sci. USA, 2000, 97(1), 325-330.
[http://dx.doi.org/10.1073/pnas.97.1.325] [PMID: 10618417]
[195]
Lucion, A.B.; Pereira, F.M.; Winkelman, E.C.; Sanvitto, G.L.; Anselmo-Franci, J.A. Neonatal handling reduces the number of cells in the locus coeruleus of rats. Behav. Neurosci., 2003, 117(5), 894-903.
[http://dx.doi.org/10.1037/0735-7044.117.5.894] [PMID: 14570540]
[196]
Mazure, C.M.; Swendsen, J. Sex differences in Alzheimer’s disease and other dementias. Lancet Neurol., 2016, 15(5), 451-452.
[http://dx.doi.org/10.1016/S1474-4422(16)00067-3] [PMID: 26987699]
[197]
Rubinow, D.R.; Schmidt, P.J. Sex differences and the neurobiology of affective disorders. Neuropsychopharmacology, 2019, 44(1), 111-128.
[http://dx.doi.org/10.1038/s41386-018-0148-z] [PMID: 30061743]
[198]
Yan, Y.; Dominguez, S.; Fisher, D.W.; Dong, H. Sex differences in chronic stress responses and Alzheimer’s disease. Neurobiol. Stress, 2018, 8, 120-126.
[http://dx.doi.org/10.1016/j.ynstr.2018.03.002] [PMID: 29888307]
[199]
Kudielka, B.M.; Kirschbaum, C. Sex differences in HPA axis responses to stress: A review. Biol. Psychol., 2005, 69(1), 113-132.
[http://dx.doi.org/10.1016/j.biopsycho.2004.11.009] [PMID: 15740829]
[200]
Bangasser, D.A.; Zhang, X.; Garachh, V.; Hanhauser, E.; Valentino, R.J. Sexual dimorphism in locus coeruleus dendritic morphology: A structural basis for sex differences in emotional arousal. Physiol. Behav., 2011, 103(3-4), 342-351.
[http://dx.doi.org/10.1016/j.physbeh.2011.02.037] [PMID: 21362438]
[201]
Bangasser, D.A.; Wiersielis, K.R.; Khantsis, S. Sex differences in the locus coeruleus-norepinephrine system and its regulation by stress. Brain Res., 2016, 1641(Pt B), 177-188.
[http://dx.doi.org/10.1016/j.brainres.2015.11.021] [PMID: 26607253]
[202]
Curtis, A.L.; Bethea, T.; Valentino, R.J. Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology, 2006, 31(3), 544-554.
[http://dx.doi.org/10.1038/sj.npp.1300875] [PMID: 16123744]
[203]
Fu, H.; Possenti, A.; Freer, R.; Nakano, Y.; Hernandez Villegas, N.C.; Tang, M.; Cauhy, P.V.M.; Lassus, B.A.; Chen, S.; Fowler, S.L.; Figueroa, H.Y.; Huey, E.D.; Johnson, G.V.W.; Vendruscolo, M.; Duff, K.E. A tau homeostasis signature is linked with the cellular and regional vulnerability of excitatory neurons to tau pathology. Nat. Neurosci., 2019, 22(1), 47-56.
[http://dx.doi.org/10.1038/s41593-018-0298-7] [PMID: 30559469]
[204]
Leroy, K.; Yilmaz, Z.; Brion, J.P. Increased level of active GSK-3? in Alzheimer’s disease and accumulation in argyrophilic grains and in neurones at different stages of neurofibrillary degeneration. Neuropathol. Appl. Neurobiol., 2007, 33(1), 43-55.
[http://dx.doi.org/10.1111/j.1365-2990.2006.00795.x] [PMID: 17239007]
[205]
Rissman, R.A.; Lee, K.F.; Vale, W.; Sawchenko, P.E. Corticotropin-releasing factor receptors differentially regulate stress-induced tau phosphorylation. J. Neurosci., 2007, 27(24), 6552-6562.
[http://dx.doi.org/10.1523/JNEUROSCI.5173-06.2007] [PMID: 17567816]
[206]
Kitazawa, M.; Oddo, S.; Yamasaki, T.R.; Green, K.N.; LaFerla, F.M. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer’s disease. J. Neurosci., 2005, 25(39), 8843-8853.
[http://dx.doi.org/10.1523/JNEUROSCI.2868-05.2005] [PMID: 16192374]
[207]
Pinheiro, S.; Silva, J.; Mota, C.; Vaz-Silva, J.; Veloso, A.; Pinto, V.; Sousa, N.; Cerqueira, J.; Sotiropoulos, I. Tau mislocation in glucocorticoid-triggered hippocampal pathology. Mol. Neurobiol., 2016, 53(7), 4745-4753.
[http://dx.doi.org/10.1007/s12035-015-9356-2] [PMID: 26328538]
[208]
Feng, Y.; Xia, Y.; Yu, G.; Shu, X.; Ge, H.; Zeng, K.; Wang, J.; Wang, X. Cleavage of GSK-3β by calpain counteracts the inhibitory effect of Ser9 phosphorylation on GSK-3β activity induced by H 2 O 2. J. Neurochem., 2013, 126(2), 234-242.
[http://dx.doi.org/10.1111/jnc.12285] [PMID: 23646926]
[209]
Cho, M.H.; Kim, D.H.; Choi, J.E.; Chang, E.J.; Seung-YongYoon Increased phosphorylation of dynamin-related protein 1 and mitochondrial fission in okadaic acid-treated neurons. Brain Res., 2012, 1454, 100-110.
[http://dx.doi.org/10.1016/j.brainres.2012.03.010] [PMID: 22459049]
[210]
Silva, J.M.; Rodrigues, S.; Sampaio-Marques, B.; Gomes, P.; Neves-Carvalho, A.; Dioli, C.; Soares-Cunha, C.; Mazuik, B.F.; Takashima, A.; Ludovico, P.; Wolozin, B.; Sousa, N.; Sotiropoulos, I. Dysregulation of autophagy and stress granule-related proteins in stress-driven Tau pathology. Cell Death Differ., 2019, 26(8), 1411-1427.
[http://dx.doi.org/10.1038/s41418-018-0217-1] [PMID: 30442948]
[211]
Brown, M.R.; Bondada, V.; Keller, J.N.; Thorpe, J.; Geddes, J.W. Proteasome or calpain inhibition does not alter cellular tau levels in neuroblastoma cells or primary neurons. J. Alzheimers Dis., 2005, 7(1), 15-24.
[http://dx.doi.org/10.3233/JAD-2005-7103] [PMID: 15750211]
[212]
Vanderweyde, T.; Youmans, K.; Liu-Yesucevitz, L.; Wolozin, B. Role of stress granules and RNA-binding proteins in neurodegeneration: A mini-review. Gerontology, 2013, 59(6), 524-533.
[http://dx.doi.org/10.1159/000354170] [PMID: 24008580]
[213]
Apicco, D.J.; Ash, P.E.A.; Maziuk, B.; LeBlang, C.; Medalla, M.; Al Abdullatif, A.; Ferragud, A.; Botelho, E.; Ballance, H.I.; Dhawan, U.; Boudeau, S.; Cruz, A.L.; Kashy, D.; Wong, A.; Goldberg, L.R.; Yazdani, N.; Zhang, C.; Ung, C.Y.; Tripodis, Y.; Kanaan, N.M.; Ikezu, T.; Cottone, P.; Leszyk, J.; Li, H.; Luebke, J.; Bryant, C.D.; Wolozin, B. Reducing the RNA binding protein TIA1 protects against tau-mediated neurodegeneration in vivo. Nat. Neurosci., 2018, 21(1), 72-80.
[http://dx.doi.org/10.1038/s41593-017-0022-z] [PMID: 29273772]
[214]
Vanderweyde, T.; Apicco, D.J.; Youmans-Kidder, K.; Ash, P.E.A.; Cook, C.; Lummertz da Rocha, E.; Jansen-West, K.; Frame, A.A.; Citro, A.; Leszyk, J.D.; Ivanov, P.; Abisambra, J.F.; Steffen, M.; Li, H.; Petrucelli, L.; Wolozin, B. Interaction of tau with the RNA-binding protein TIA1 regulates tau pathophysiology and toxicity. Cell Rep., 2016, 15(7), 1455-1466.
[http://dx.doi.org/10.1016/j.celrep.2016.04.045] [PMID: 27160897]
[215]
Maziuk, B.; Ballance, H.I.; Wolozin, B. Dysregulation of RNA binding protein aggregation in neurodegenerative disorders. Front. Mol. Neurosci., 2017, 10, 89.
[http://dx.doi.org/10.3389/fnmol.2017.00089] [PMID: 28420962]
[216]
Daskalakis, N.P.; Bagot, R.C.; Parker, K.J.; Vinkers, C.H.; de Kloet, E.R. The three-hit concept of vulnerability and resilience: Toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology, 2013, 38(9), 1858-1873.
[http://dx.doi.org/10.1016/j.psyneuen.2013.06.008] [PMID: 23838101]
[217]
Gauvrit, T.; Benderradji, H.; Buée, L.; Blum, D.; Vieau, D. Early-life environment influence on late-onset Alzheimer’s disease. Front. Cell Dev. Biol., 2022, 10, 834661.
[http://dx.doi.org/10.3389/fcell.2022.834661] [PMID: 35252195]
[218]
Hoeijmakers, L.; Lesuis, S.L.; Krugers, H.; Lucassen, P.J.; Korosi, A. A preclinical perspective on the enhanced vulnerability to Alzheimer's disease after early-life stress. Neurobiol. Stress, 2018, 8, 172-185.
[219]
Lemche, E. Early life stress and epigenetics in late-onset Alzheimer's dementia: A systematic review. Curr. Genomics, 2018, 19(7), 522-602.
[220]
Malik, M.; Parikh, I.; Vasquez, J.B.; Smith, C.; Tai, L.; Bu, G.; LaDu, M.J.; Fardo, D.W.; Rebeck, G.W.; Estus, S. Genetics ignite focus on microglial inflammation in Alzheimer’s disease. Mol. Neurodegener., 2015, 10(1), 52.
[http://dx.doi.org/10.1186/s13024-015-0048-1] [PMID: 26438529]
[221]
Koob, G.F. Corticotropin-releasing factor, norepinephrine, and stress. Biol. Psychiatry, 1999, 46(9), 1167-1180.
[http://dx.doi.org/10.1016/S0006-3223(99)00164-X] [PMID: 10560023]
[222]
Peters, A.; McEwen, B.S.; Friston, K. Uncertainty and stress: Why it causes diseases and how it is mastered by the brain. Prog. Neurobiol., 2017, 156, 164-188.
[http://dx.doi.org/10.1016/j.pneurobio.2017.05.004] [PMID: 28576664]
[223]
de Berker, A.O.; Rutledge, R.B.; Mathys, C.; Marshall, L.; Cross, G.F.; Dolan, R.J.; Bestmann, S. Computations of uncertainty mediate acute stress responses in humans. Nat. Commun., 2016, 7(1), 10996.
[http://dx.doi.org/10.1038/ncomms10996] [PMID: 27020312]
[224]
Grissom, N.; Bhatnagar, S. Habituation to repeated stress: Get used to it. Neurobiol. Learn. Mem., 2009, 92(2), 215-224.
[http://dx.doi.org/10.1016/j.nlm.2008.07.001] [PMID: 18667167]
[225]
Tops, M.; Buisman-Pijlman, F.T.; Carter, C.S. Oxytocin and attachment facilitate a shift from seeking novelty to recognizing and preferring familiarity: The key to increasing resilience? The Resilience Handbook: Approaches to Stress and Trauma; Routledge Publishers : England, 2013, pp. 115-130.
[226]
Atwool, N. Attachment and resilience: Implications for children in care. Child Care Pract., 2006, 12(4), 315-330.
[http://dx.doi.org/10.1080/13575270600863226]
[227]
Mikulincer, M. Attachment working models and the sense of trust: An exploration of interaction goals and affect regulation. J. Pers. Soc. Psychol., 1998, 74(5), 1209-1224.
[http://dx.doi.org/10.1037/0022-3514.74.5.1209]
[228]
Holwerda, T.J.; Deeg, D.J.H.; Beekman, A.T.F.; van Tilburg, T.G.; Stek, M.L.; Jonker, C.; Schoevers, R.A. Feelings of loneliness, but not social isolation, predict dementia onset: Results from the Amsterdam Study of the Elderly (AMSTEL). J. Neurol. Neurosurg. Psychiatry, 2014, 85(2), 135-142.
[http://dx.doi.org/10.1136/jnnp-2012-302755] [PMID: 23232034]
[229]
Drinkwater, E.; Davies, C.; Spires-Jones, T.L. Potential neurobiological links between social isolation and Alzheimer’s disease risk. Eur. J. Neurosci., 2022, 56(9), 5397-5412.
[http://dx.doi.org/10.1111/ejn.15373] [PMID: 34184343]
[230]
Bowlby, J. A Secure Base. Parent-Child Attachment and Healthy Human Development; Basic Books: New York, 1988.
[231]
Karreman, A.; Vingerhoets, A.J.J.M. Attachment and well-being: The mediating role of emotion regulation and resilience. Pers. Individ. Dif., 2012, 53(7), 821-826.
[http://dx.doi.org/10.1016/j.paid.2012.06.014]
[232]
Moriceau, S.; Shionoya, K.; Jakubs, K.; Sullivan, R.M. Early-life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. J. Neurosci., 2009, 29(50), 15745-15755.
[http://dx.doi.org/10.1523/JNEUROSCI.4106-09.2009] [PMID: 20016090]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy