Skip to main content

Stress and the Etiopathogenesis of Alzheimer’s Disease and Depression

  • Chapter
  • First Online:
Tau Biology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1184))

Abstract

Alzheimer’s disease (AD) is a multifactorial neurodegenerative disorder with a complex physiopathology whose initiators are poorly defined. Accumulating clinical and experimental evidence suggests a causal role of lifetime stress in AD. This chapter summarizes current knowledge about how chronic stress and its accompanying high levels of glucocorticoid (GC) secretion, trigger the two main pathomechanisms of AD: (i) misprocessing of amyloid precursor protein (APP) and the generation of amyloid beta (Aβ) and (ii) Tau hyperphosphorylation and aggregation. Given that depression is a well-known stress-related illness, and the evidence that depression may precede AD, this chapter also explores neurobiological mechanisms that may be common to depressive and AD pathologies. This review also discusses emerging insights into the role of Tau and its malfunction in disrupting neuronal cascades and neuroplasticity and, thus triggering brain pathology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Sousa N, Almeida OFX. Disconnection and reconnection: the morphological basis of (mal)adaptation to stress. Trends Neurosci. 2012;35:742–51. https://doi.org/10.1016/j.tins.2012.08.006.

    Article  CAS  PubMed  Google Scholar 

  2. Carroll BJ. Ageing, stress and the brain. Novartis Found Symp. 2002;242:26–36.. discussion 36–45

    CAS  PubMed  Google Scholar 

  3. McEwen BS. Mood disorders and allostatic load. Biol Psychiatry. 2003;54:200–7.

    Article  PubMed  Google Scholar 

  4. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87:873–904. https://doi.org/10.1152/physrev.00041.2006.

    Article  PubMed  Google Scholar 

  5. de Kloet ER, Joëls M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6:463–75. https://doi.org/10.1038/nrn1683.

    Article  CAS  PubMed  Google Scholar 

  6. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry. 2000;57:925–35.

    Article  CAS  PubMed  Google Scholar 

  7. Sorrells SF, Sapolsky RM. An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun. 2007;21:259–72. https://doi.org/10.1016/j.bbi.2006.11.006.

    Article  CAS  PubMed  Google Scholar 

  8. Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OFX. Stress and glucocorticoid footprints in the brain—the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev. 2008;32:1161–73. https://doi.org/10.1016/j.neubiorev.2008.05.007.

    Article  CAS  PubMed  Google Scholar 

  9. Vyas S, Rodrigues AJ, Silva JM, Tronche F, Almeida OFX, Sousa N, Sotiropoulos I. Chronic stress and glucocorticoids: from neuronal plasticity to neurodegeneration. Neural Plast. 2016;2016:1–15. https://doi.org/10.1155/2016/6391686.

    Article  CAS  Google Scholar 

  10. Reul JM, de Kloet ER. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 1985;117:2505–11. https://doi.org/10.1210/endo-117-6-2505.

    Article  CAS  PubMed  Google Scholar 

  11. de Kloet ER, Reul JM, Sutanto W. Corticosteroids and the brain. J Steroid Biochem Mol Biol. 1990;37:387–94.

    Article  PubMed  Google Scholar 

  12. Hassan AH, von Rosenstiel P, Patchev VK, Holsboer F, Almeida OF. Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp Neurol. 1996;140:43–52. https://doi.org/10.1006/exnr.1996.0113.

    Article  CAS  PubMed  Google Scholar 

  13. Almeida OF, Condé GL, Crochemore C, Demeneix BA, Fischer D, Hassan AH, Meyer M, Holsboer F, Michaelidis TM. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J. 2000;14(5):779–90.

    Article  CAS  PubMed  Google Scholar 

  14. ter Horst JP, van der Mark MH, Arp M, Berger S, de Kloet ER, Oitzl MS. Stress or no stress: mineralocorticoid receptors in the forebrain regulate behavioral adaptation. Neurobiol Learn Mem. 2012;98(1):33–40. https://doi.org/10.1016/j.nlm.2012.04.006.

    Article  CAS  PubMed  Google Scholar 

  15. van Eekelen JA, Rots NY, Sutanto W, de Kloet ER. The effect of aging on stress responsiveness and central corticosteroid receptors in the brown Norway rat. Neurobiol Aging. 1992;13:159–70.

    Article  PubMed  Google Scholar 

  16. Hassan AH, Patchev VK, von Rosenstiel P, Holsboer F, Almeida OF. Plasticity of hippocampal corticosteroid receptors during aging in the rat. FASEB J. 1999;13:115–22.

    Article  CAS  PubMed  Google Scholar 

  17. Riedemann T, Patchev AV, Cho K, Almeida OFX. Corticosteroids: way upstream. Mol Brain. 2010;3:2. https://doi.org/10.1186/1756-6606-3-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Groeneweg FL, Karst H, de Kloet ER, Joëls M. Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol Cell Endocrinol. 2012;350:299–309. https://doi.org/10.1016/j.mce.2011.06.020.

    Article  CAS  PubMed  Google Scholar 

  19. Yang S, Roselli F, Patchev AV, Yu S, Almeida OFX. Non-receptor-tyrosine kinases integrate fast glucocorticoid signaling in hippocampal neurons. J Biol Chem. 2013;288:23725–39. https://doi.org/10.1074/jbc.M113.470146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Trapp T, Rupprecht R, Castrén M, Reul JMHM, Holsboer F. Heterodimerization between mineralocorticoid and glucocorticoid receptor: a new principle of glucocorticoid action in the CNS. Neuron. 1994;13:1457–62. https://doi.org/10.1016/0896-6273(94)90431-6.

    Article  CAS  PubMed  Google Scholar 

  21. Nishi M, Ogawa H, Ito T, Matsuda K-I, Kawata M. Dynamic changes in subcellular localization of mineralocorticoid receptor in living cells: in comparison with glucocorticoid receptor using dual-color labeling with green fluorescent protein spectral variants. Mol Endocrinol. 2001;15:1077–92. https://doi.org/10.1210/mend.15.7.0659.

    Article  CAS  PubMed  Google Scholar 

  22. Gesing A, Bilang-Bleuel A, Droste SK, Linthorst AC, Holsboer F, Reul JM. Psychological stress increases hippocampal mineralocorticoid receptor levels: involvement of corticotropin-releasing hormone. J Neurosci. 2001;21:4822–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chen Y, Rex CS, Rice CJ, Dube CM, Gall CM, Lynch G, Baram TZ. Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling. Proc Natl Acad Sci. 2010;107:13123–8. https://doi.org/10.1073/pnas.1003825107.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rein T. FK506 binding protein 51 integrates pathways of adaptation: FKBP51 shapes the reactivity to environmental change. Bioessays. 2016;38:894–902. https://doi.org/10.1002/bies.201600050.

    Article  CAS  PubMed  Google Scholar 

  25. Grad I, Picard D. The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol. 2007;275:2–12. https://doi.org/10.1016/j.mce.2007.05.018.

    Article  CAS  PubMed  Google Scholar 

  26. Obradović D, Tirard M, Némethy Z, Hirsch O, Gronemeyer H, Almeida OFX. DAXX, FLASH, and FAF-1 modulate mineralocorticoid and glucocorticoid receptor-mediated transcription in hippocampal cells--toward a basis for the opposite actions elicited by two nuclear receptors? Mol Pharmacol. 2004;65:761–9. https://doi.org/10.1124/mol.65.3.761.

    Article  PubMed  Google Scholar 

  27. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin L-Y, Patterson C. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol. 1999;19:4535–45. https://doi.org/10.1128/MCB.19.6.4535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tirard M, Jasbinsek J, Almeida OFX, Michaelidis TM. The manifold actions of the protein inhibitor of activated STAT proteins on the transcriptional activity of mineralocorticoid and glucocorticoid receptors in neural cells. J Mol Endocrinol. 2004;32:825–41.

    Article  CAS  PubMed  Google Scholar 

  29. Tirard M, Almeida OFX, Hutzler P, Melchior F, Michaelidis TM. Sumoylation and proteasomal activity determine the transactivation properties of the mineralocorticoid receptor. Mol Cell Endocrinol. 2007;268:20–9. https://doi.org/10.1016/j.mce.2007.01.010.

    Article  CAS  PubMed  Google Scholar 

  30. Datson NA, Van Der Perk J, De Kloet ER, Vreugdenhil E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression: corticosteroid-responsive genes in hippocampus. Eur J Neurosci. 2001;14:675–89. https://doi.org/10.1046/j.0953-816x.2001.01685.x.

    Article  CAS  PubMed  Google Scholar 

  31. Schaaf MJM, de Jong J, de Kloet ER, Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res. 1998;813:112–20. https://doi.org/10.1016/S0006-8993(98)01010-5.

    Article  CAS  PubMed  Google Scholar 

  32. Hansson AC, Cintra A, Belluardo N, Sommer W, Bhatnagar M, Bader M, Ganten D, Fuxe K. Gluco- and mineralocorticoid receptor-mediated regulation of neurotrophic factor gene expression in the dorsal hippocampus and the neocortex of the rat: GR- and MR-mediated gene expression. Eur J Neurosci. 2000;12:2918–34. https://doi.org/10.1046/j.1460-9568.2000.00185.x.

    Article  CAS  PubMed  Google Scholar 

  33. Sandi C. Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci. 2004;5:917–30. https://doi.org/10.1038/nrn1555.

    Article  CAS  PubMed  Google Scholar 

  34. Sabban EL, Liu X, Serova L, Gueorguiev V, Kvetnansky R. Stress triggered changes in gene expression in adrenal medulla: transcriptional responses to acute and chronic stress. Cell Mol Neurobiol. 2006;26:843–54. https://doi.org/10.1007/s10571-006-9069-1.

    Article  CAS  Google Scholar 

  35. Lucassen PJ, Pruessner J, Sousa N, Almeida OFX, Van Dam AM, Rajkowska G, Swaab DF, Czéh B. Neuropathology of stress. Acta Neuropathol. 2014;127:109–35. https://doi.org/10.1007/s00401-013-1223-5.

    Article  CAS  PubMed  Google Scholar 

  36. Harris A, Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011;59:279–89. https://doi.org/10.1016/j.yhbeh.2010.06.007.

    Article  CAS  PubMed  Google Scholar 

  37. Seckl JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol. 2004;151(Suppl 3):U49–62.

    Article  CAS  PubMed  Google Scholar 

  38. Moisiadis VG, Matthews SG. Glucocorticoids and fetal programming part 2: mechanisms. Nat Rev Endocrinol. 2014;10:403–11. https://doi.org/10.1038/nrendo.2014.74.

    Article  CAS  PubMed  Google Scholar 

  39. Patchev AV, Rodrigues AJ, Sousa N, Spengler D, Almeida OFX. The future is now: early life events preset adult behaviour. Acta Physiol (Oxf). 2014;210:46–57. https://doi.org/10.1111/apha.12140.

    Article  CAS  Google Scholar 

  40. McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12:342–8. https://doi.org/10.1038/nn.2270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008;3:97–106.

    Article  PubMed  Google Scholar 

  42. Diamond DM, Bennett MC, Fleshner M, Rose GM. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 1992;2:421–30. https://doi.org/10.1002/hipo.450020409.

    Article  CAS  PubMed  Google Scholar 

  43. Martin SJ, Grimwood PD, Morris RGM. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci. 2000;23:649–711. https://doi.org/10.1146/annurev.neuro.23.1.649.

    Article  CAS  PubMed  Google Scholar 

  44. Kim JJ, Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci. 2002;3:453–62. https://doi.org/10.1038/nrn849.

    Article  CAS  PubMed  Google Scholar 

  45. Kim JJ, Foy MR, Thompson RF. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci U S A. 1996;93:4750–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Oitzl MS, de Kloet ER. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci. 1992;106:62–71.

    Article  CAS  PubMed  Google Scholar 

  47. Sandi C, Woodson JC, Haynes VF, Park CR, Touyarot K, Lopez-Fernandez MA, Venero C, Diamond DM. Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex. Biol Psychiatry. 2005;57:856–64. https://doi.org/10.1016/j.biopsych.2004.12.034.

    Article  PubMed  Google Scholar 

  48. Cacucci F, Wills TJ, Lever C, Giese KP, O’Keefe J. Experience-dependent increase in CA1 place cell spatial information, but not spatial reproducibility, is dependent on the autophosphorylation of the alpha-isoform of the calcium/calmodulin-dependent protein kinase II. J Neurosci. 2007;27(29):7854–9. https://doi.org/10.1523/JNEUROSCI.1704-07.2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cerqueira JJ, Taipa R, Uylings HBM, Almeida OFX, Sousa N. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex. 2007;17(9):1998–2006. https://doi.org/10.1093/cercor/bhl108.

    Article  PubMed  Google Scholar 

  50. Sousa N, Lukoyanov NV, Madeira MD, Almeida OFX, Paula-Barbosa MM. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience. 2000;97:253–66. https://doi.org/10.1016/S0306-4522(00)00050-6.

    Article  CAS  PubMed  Google Scholar 

  51. Woolley CS, Gould E, McEwen BS. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 1990;531:225–31.

    Article  CAS  PubMed  Google Scholar 

  52. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci. 2006;26(30):7870–4. https://doi.org/10.1523/JNEUROSCI.1184-06.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Schwabe L, Wolf OT. Stress prompts habit behavior in humans. J Neurosci. 2009;29:7191–8. https://doi.org/10.1523/JNEUROSCI.0979-09.2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sandi C, Davies HA, Cordero MI, Rodriguez JJ, Popov VI, Stewart MG. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur J Neurosci. 2003;17:2447–56.

    Article  PubMed  Google Scholar 

  55. Tasker JG, Herman JP. Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic–pituitary–adrenal axis. Stress. 2011;14:398–406. https://doi.org/10.3109/10253890.2011.586446.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Goldwater DS, Pavlides C, Hunter RG, Bloss EB, Hof PR, McEwen BS, Morrison JH. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience. 2009;164:798–808. https://doi.org/10.1016/j.neuroscience.2009.08.053.

    Article  CAS  PubMed  Google Scholar 

  57. Radley JJ, Morrison JH. Repeated stress and structural plasticity in the brain. Ageing Res Rev. 2005;4:271–87. https://doi.org/10.1016/j.arr.2005.03.004.

    Article  PubMed  Google Scholar 

  58. Shansky RM, Morrison JH. Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res. 2009;1293:108–13. https://doi.org/10.1016/j.brainres.2009.03.062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lopes S, Vaz-Silva J, Pinto V, Dalla C, Kokras N, Bedenk B, Mack N, Czisch M, Almeida OFX, Sousa N, Sotiropoulos I. Tau protein is essential for stress-induced brain pathology. Proc Natl Acad Sci. 2016;113:E3755–63. https://doi.org/10.1073/pnas.1600953113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lopes S, Teplytska L, Vaz-Silva J, Dioli C, Trindade R, Morais M, Webhofer C, Maccarrone G, Almeida OFX, Turck CW, Sousa N, Sotiropoulos I, Filiou MD. Tau deletion prevents stress-induced dendritic atrophy in prefrontal cortex: role of synaptic mitochondria. Cereb Cortex. 2016;27(4):2580–91. https://doi.org/10.1093/cercor/bhw057.

    Article  Google Scholar 

  61. Heine VM, Maslam S, Zareno J, Joëls M, Lucassen PJ. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci. 2004;19:131–44.

    Article  PubMed  Google Scholar 

  62. Dioli C, Patrício P, Trindade R, Pinto LG, Silva JM, Morais M, Ferreiro E, Borges S, Mateus-Pinheiro A, Rodrigues AJ, Sousa N, Bessa JM, Pinto L, Sotiropoulos I. Tau-dependent suppression of adult neurogenesis in the stressed hippocampus. Mol Psychiatry. 2017;22:1110–8. https://doi.org/10.1038/mp.2017.103.

    Article  CAS  PubMed  Google Scholar 

  63. Kempermann G, Krebs J, Fabel K. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry. 2008;21:290–5. https://doi.org/10.1097/YCO.0b013e3282fad375.

    Article  PubMed  Google Scholar 

  64. Mu Y, Gage FH. Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol Neurodegener. 2011;6:85. https://doi.org/10.1186/1750-1326-6-85.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Demars M, Hu Y-S, Gadadhar A, Lazarov O. Impaired neurogenesis is an early event in the etiology of familial Alzheimer’s disease in transgenic mice. J Neurosci Res. 2010;88:2103–17. https://doi.org/10.1002/jnr.22387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. O’Brien JT, Ames D, Schweitzer I, Mastwyk M, Colman P. Enhanced adrenal sensitivity to adrenocorticotrophic hormone (ACTH) is evidence of HPA axis hyperactivity in Alzheimer’s disease. Psychol Med. 1996;26:7–14.

    Article  PubMed  Google Scholar 

  67. Rasmuson S, Andrew R, Näsman B, Seckl JR, Walker BR, Olsson T. Increased glucocorticoid production and altered cortisol metabolism in women with mild to moderate Alzheimer’s disease. Biol Psychiatry. 2001;49:547–52. https://doi.org/10.1016/S0006-3223(00)01015-5.

    Article  CAS  PubMed  Google Scholar 

  68. Simard M, Hudon C, van Reekum R. Psychological distress and risk for dementia. Curr Psychiatry Rep. 2009;11:41–7.

    Article  PubMed  Google Scholar 

  69. Mejía S, Giraldo M, Pineda D, Ardila A, Lopera F. Nongenetic factors as modifiers of the age of onset of familial Alzheimer’s disease. Int Psychogeriatr. 2003;15:337–49.

    Article  PubMed  Google Scholar 

  70. Rothman SM, Mattson MP. Adverse stress, hippocampal networks, and Alzheimer’s disease. Neuromolecular Med. 2010;12:56–70. https://doi.org/10.1007/s12017-009-8107-9.

    Article  CAS  PubMed  Google Scholar 

  71. Hatzinger M, Z’Brun A, Hemmeter U, Seifritz E, Baumann F, Holsboer-Trachsler E, Heuser IJ. Hypothalamic-pituitary-adrenal system function in patients with Alzheimer’s disease. Neurobiol Aging. 1995;16:205–9.

    Article  CAS  PubMed  Google Scholar 

  72. Peskind ER, Wilkinson CW, Petrie EC, Schellenberg GD, Raskind MA. Increased CSF cortisol in AD is a function of APOE genotype. Neurology. 2001;56:1094–8.

    Article  CAS  PubMed  Google Scholar 

  73. Hoogendijk WJG, Meynen G, Endert E, Hofman MA, Swaab DF. Increased cerebrospinal fluid cortisol level in Alzheimer’s disease is not related to depression. Neurobiol Aging. 2006;27:780.e1–2. https://doi.org/10.1016/j.neurobiolaging.2005.07.017.

    Article  CAS  Google Scholar 

  74. Hartmann A, Veldhuis JD, Deuschle M, Standhardt H, Heuser I. Twenty-four hour cortisol release profiles in patients with Alzheimer’s and Parkinson’s disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol Aging. 1997;18:285–9.

    Article  CAS  PubMed  Google Scholar 

  75. Touma C, Ambrée O, Görtz N, Keyvani K, Lewejohann L, Palme R, Paulus W, Schwarze-Eicker K, Sachser N. Age- and sex-dependent development of adrenocortical hyperactivity in a transgenic mouse model of Alzheimer’s disease. Neurobiol Aging. 2004;25:893–904. https://doi.org/10.1016/j.neurobiolaging.2003.09.004.

    Article  CAS  PubMed  Google Scholar 

  76. Green KN. Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer’s disease. J Neurosci. 2006;26:9047–56. https://doi.org/10.1523/JNEUROSCI.2797-06.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NPV, Thakur M, McEwen BS, Hauger RL, Meaney MJ. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci. 1998;1:69–73. https://doi.org/10.1038/271.

    Article  CAS  PubMed  Google Scholar 

  78. Huang C-W, Lui C-C, Chang W-N, Lu C-H, Wang Y-L, Chang C-C. Elevated basal cortisol level predicts lower hippocampal volume and cognitive decline in Alzheimer’s disease. J Clin Neurosci. 2009;16:1283–6. https://doi.org/10.1016/j.jocn.2008.12.026.

    Article  CAS  PubMed  Google Scholar 

  79. Karran E, Mercken M, De Strooper B. The amyloid cascade hypothesis for Alzheimer’s disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov. 2011;10:698–712. https://doi.org/10.1038/nrd3505.

    Article  CAS  PubMed  Google Scholar 

  80. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E. Alzheimer’s disease. Lancet. 2011;377:1019–31. https://doi.org/10.1016/S0140-6736(10)61349-9.

    Article  PubMed  Google Scholar 

  81. Duyckaerts C, Delatour B, Potier M-C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol (Berl). 2009;118:5–36. https://doi.org/10.1007/s00401-009-0532-1.

    Article  CAS  Google Scholar 

  82. Dede AJO, Wixted JT, Hopkins RO, Squire LR. Hippocampal damage impairs recognition memory broadly, affecting both parameters in two prominent models of memory. Proc Natl Acad Sci. 2013;110:6577–82. https://doi.org/10.1073/pnas.1304739110.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Jeong YH, Park CH, Yoo J, Shin KY, Ahn S-M, Kim H-S, Lee SH, Emson PC, Suh Y-H. Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APP V717I-CT100 transgenic mice, an Alzheimer’s disease model. FASEB J. 2006;20:729–31. https://doi.org/10.1096/fj.05-4265fje.

    Article  CAS  PubMed  Google Scholar 

  84. Sotiropoulos I, Catania C, Riedemann T, Fry JP, Breen KC, Michaelidis TM, Almeida OFX. Glucocorticoids trigger Alzheimer disease-like pathobiochemistry in rat neuronal cells expressing human tau: glucocorticoids, human tau and Alzheimer’s disease. J Neurochem. 2008;107:385–97. https://doi.org/10.1111/j.1471-4159.2008.05613.x.

    Article  CAS  PubMed  Google Scholar 

  85. Catania C, Sotiropoulos I, Silva R, Onofri C, Breen KC, Sousa N, Almeida OFX. The amyloidogenic potential and behavioral correlates of stress. Mol Psychiatry. 2009;14:95–105. https://doi.org/10.1038/sj.mp.4002101.

    Article  CAS  PubMed  Google Scholar 

  86. Stein-Behrens BA, Elliott EM, Miller CA, Schilling JW, Newcombe R, Sapolsky RM. Glucocorticoids exacerbate kainic acid-induced extracellular accumulation of excitatory amino acids in the rat hippocampus. J Neurochem. 1992;58:1730–5.

    Article  CAS  PubMed  Google Scholar 

  87. Sotiropoulos I, Catania C, Pinto LG, Silva R, Pollerberg GE, Takashima A, Sousa N, Almeida OFX. Stress acts cumulatively to precipitate Alzheimer’s disease-like tau pathology and cognitive deficits. J Neurosci. 2011;31:7840–7. https://doi.org/10.1523/JNEUROSCI.0730-11.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Callahan LM, Vaules WA, Coleman PD. Progressive reduction of synaptophysin message in single neurons in Alzheimer disease. J Neuropathol Exp Neurol. 2002;61:384–95.

    Article  CAS  PubMed  Google Scholar 

  89. Lauckner J, Frey P, Geula C. Comparative distribution of tau phosphorylated at Ser262 in pre-tangles and tangles. Neurobiol Aging. 2003;24:767–76.

    Article  CAS  PubMed  Google Scholar 

  90. Hampel H, Bürger K, Pruessner JC, Zinkowski R, DeBernardis J, Kerkman D, Leinsinger G, Evans AC, Davies P, Möller H-J, Teipel SJ. Correlation of cerebrospinal fluid levels of tau protein phosphorylated at threonine 231 with rates of hippocampal atrophy in Alzheimer disease. Arch Neurol. 2005;62(5):770–3. https://doi.org/10.1001/archneur.62.5.770.

    Article  PubMed  Google Scholar 

  91. Augustinack JC, Schneider A, Mandelkow E-M, Hyman BT. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer’s disease. Acta Neuropathol (Berl). 2002;103:26–35.

    Article  CAS  Google Scholar 

  92. Ewers M, Buerger K, Teipel SJ, Scheltens P, Schroder J, Zinkowski RP, Bouwman FH, Schonknecht P, Schoonenboom NSM, Andreasen N, Wallin A, DeBernardis JF, Kerkman DJ, Heindl B, Blennow K, Hampel H. Multicenter assessment of CSF-phosphorylated tau for the prediction of conversion of MCI. Neurology. 2007;69:2205–12. https://doi.org/10.1212/01.wnl.0000286944.22262.ff.

    Article  CAS  PubMed  Google Scholar 

  93. van der Vlies AE, Verwey NA, Bouwman FH, Blankenstein MA, Klein M, Scheltens P, van der Flier WM. CSF biomarkers in relationship to cognitive profiles in Alzheimer disease. Neurology. 2009;72:1056–61. https://doi.org/10.1212/01.wnl.0000345014.48839.71.

    Article  CAS  PubMed  Google Scholar 

  94. Carroll JC, Iba M, Bangasser DA, Valentino RJ, James MJ, Brunden KR, Lee VM-Y, Trojanowski JQ. 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):14436–49. https://doi.org/10.1523/JNEUROSCI.3836-11.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Rissman RA, Lee K-F, Vale W, Sawchenko PE. Corticotropin-releasing factor receptors differentially regulate stress-induced tau phosphorylation. J Neurosci. 2007;27:6552–62. https://doi.org/10.1523/JNEUROSCI.5173-06.2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Sotiropoulos I, Silva J, Kimura T, Rodrigues AJ, Costa P, Almeida OFX, Sousa N, Takashima A. Female hippocampus vulnerability to environmental stress, a precipitating factor in Tau aggregation pathology. J Alzheimers Dis. 2015;43:763–74. https://doi.org/10.3233/JAD-140693.

    Article  CAS  PubMed  Google Scholar 

  97. de Calignon A, Polydoro M, Suárez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT. Propagation of tau pathology in a model of early Alzheimer’s disease. Neuron. 2012;73:685–97. https://doi.org/10.1016/j.neuron.2011.11.033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Wang YP, Biernat J, Pickhardt M, Mandelkow E, Mandelkow E-M. Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proc Natl Acad Sci. 2007;104:10252–7. https://doi.org/10.1073/pnas.0703676104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Rissman RA, Poon WW, Blurton-Jones M, Oddo S, Torp R, Vitek MP, LaFerla FM, Rohn TT, Cotman CW. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest. 2004;114:121–30. https://doi.org/10.1172/JCI20640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Weaver CL, Espinoza M, Kress Y, Davies P. Conformational change as one of the earliest alterations of tau in Alzheimer’s disease. Neurobiol Aging. 2000;21:719–27.

    Article  CAS  PubMed  Google Scholar 

  101. Kobayashi S, Tanaka T, Soeda Y, Almeida OFX, Takashima A. Local somatodendritic translation and hyperphosphorylation of tau protein triggered by AMPA and NMDA receptor stimulation. EBioMedicine. 2017;20:120–6. https://doi.org/10.1016/j.ebiom.2017.05.012.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wölfing H, Chieng BC, Christie MJ, Napier IA, Eckert A, Staufenbiel M, Hardeman E, Götz J. Dendritic function of tau mediates amyloid-β toxicity in Alzheimer’s disease mouse models. Cell. 2010;142:387–97. https://doi.org/10.1016/j.cell.2010.06.036.

    Article  CAS  PubMed  Google Scholar 

  103. Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, Pitstick R, Carlson GA, Lanier LM, Yuan L-L, Ashe KH, Liao D. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron. 2010;68:1067–81. https://doi.org/10.1016/j.neuron.2010.11.030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. McKinney RA. Excitatory amino acid involvement in dendritic spine formation, maintenance and remodelling: glutamate and dendritic spines. J Physiol. 2010;588:107–16. https://doi.org/10.1113/jphysiol.2009.178905.

    Article  CAS  PubMed  Google Scholar 

  105. Mondragon-Rodriguez 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;287:32040–53. https://doi.org/10.1074/jbc.M112.401240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Miller EC, Teravskis PJ, Dummer BW, Zhao X, Huganir RL, Liao D. Tau phosphorylation and tau mislocalization mediate soluble Aβ oligomer-induced AMPA glutamate receptor signaling deficits. Eur J Neurosci. 2014;39:1214–24. https://doi.org/10.1111/ejn.12507.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Nong Y, Huang Y-Q, Ju W, Kalia LV, Ahmadian G, Wang YT, Salter MW. Glycine binding primes NMDA receptor internalization. Nature. 2003;422:302–7. https://doi.org/10.1038/nature01497.

    Article  CAS  PubMed  Google Scholar 

  108. Yang C-H. Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J Neurosci. 2005;25:4288–93. https://doi.org/10.1523/JNEUROSCI.0406-05.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Magariños AM, McEwen BS, Flügge G, Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci. 1996;16:3534–40.

    Article  PubMed  PubMed Central  Google Scholar 

  110. 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;53:4745–53. https://doi.org/10.1007/s12035-015-9356-2.

    Article  CAS  PubMed  Google Scholar 

  111. Nixon RA. Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci. 2007;120:4081–91. https://doi.org/10.1242/jcs.019265.

    Article  CAS  PubMed  Google Scholar 

  112. Banerjee R, Beal MF, Thomas B. Autophagy in neurodegenerative disorders: pathogenic roles and therapeutic implications. Trends Neurosci. 2010;33:541–9. https://doi.org/10.1016/j.tins.2010.09.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005;169:425–34. https://doi.org/10.1083/jcb.200412022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Frake RA, Ricketts T, Menzies FM, Rubinsztein DC. Autophagy and neurodegeneration. J Clin Invest. 2015;125:65–74. https://doi.org/10.1172/JCI73944.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Silva JM, Rodrigues S, Sampaio-Marques B, Gomes P, Neves-Carvalho A, Dioli C, Soares-Cunha C, Mazuik BF, 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. 2018;26(8):1411–27. https://doi.org/10.1038/s41418-018-0217-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Hamano T, Gendron TF, Causevic E, Yen S-H, Lin W-L, Isidoro C, DeTure M, Ko L. Autophagic-lysosomal perturbation enhances tau aggregation in transfectants with induced wild-type tau expression. Eur J Neurosci. 2008;27:1119–30. https://doi.org/10.1111/j.1460-9568.2008.06084.x.

    Article  PubMed  Google Scholar 

  117. Wang Y, Martinez-Vicente M, Krüger U, Kaushik S, Wong E, Mandelkow E-M, Cuervo AM, Mandelkow E. Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet. 2009;18:4153–70. https://doi.org/10.1093/hmg/ddp367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Inoue K, Rispoli J, Kaphzan H, Klann E, Chen EI, Kim J, Komatsu M, Abeliovich A. Macroautophagy deficiency mediates age-dependent neurodegeneration through a phospho-tau pathway. Mol Neurodegener. 2012;7:48. https://doi.org/10.1186/1750-1326-7-48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Brown MR, Bondada V, Keller JN, Thorpe J, Geddes JW. Proteasome or calpain inhibition does not alter cellular tau levels in neuroblastoma cells or primary neurons. J Alzheimers Dis. 2005;7:15–24.

    Article  CAS  PubMed  Google Scholar 

  120. Feuillette S, Blard O, Lecourtois M, Frébourg T, Campion D, Dumanchin C. Tau is not normally degraded by the proteasome: tau not normally degraded by the proteasome. J Neurosci Res. 2005;80:400–5. https://doi.org/10.1002/jnr.20414.

    Article  CAS  PubMed  Google Scholar 

  121. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441:885–9. https://doi.org/10.1038/nature04724.

    Article  CAS  PubMed  Google Scholar 

  122. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer’s disease. J Neurosci. 2008;28:6926–37. https://doi.org/10.1523/JNEUROSCI.0800-08.2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Polman JAE, Hunter RG, Speksnijder N, van den Oever JME, Korobko OB, McEwen BS, de Kloet ER, Datson NA. Glucocorticoids modulate the mTOR pathway in the hippocampus: differential effects depending on stress history. Endocrinology. 2012;153:4317–27. https://doi.org/10.1210/en.2012-1255.

    Article  CAS  PubMed  Google Scholar 

  124. An W-L, Cowburn RF, Li L, Braak H, Alafuzoff I, Iqbal K, Iqbal I-G, Winblad B, Pei J-J. Up-regulation of phosphorylated/activated p70 S6 kinase and its relationship to neurofibrillary pathology in Alzheimer’s disease. Am J Pathol. 2003;163:591–607. https://doi.org/10.1016/S0002-9440(10)63687-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Pei J-J, Hugon J. mTOR-dependent signalling in Alzheimer’s disease. J Cell Mol Med. 2008;12:2525–32. https://doi.org/10.1111/j.1582-4934.2008.00509.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Menzies FM, Huebener J, Renna M, Bonin M, Riess O, Rubinsztein DC. Autophagy induction reduces mutant ataxin-3 levels and toxicity in a mouse model of spinocerebellar ataxia type 3. Brain. 2010;133:93–104. https://doi.org/10.1093/brain/awp292.

    Article  CAS  PubMed  Google Scholar 

  127. Jiang T, Yu J-T, Zhu X-C, Zhang Q-Q, Cao L, Wang H-F, Tan M-S, Gao Q, Qin H, Zhang Y-D, Tan L. Temsirolimus attenuates tauopathy in vitro and in vivo by targeting tau hyperphosphorylation and autophagic clearance. Neuropharmacology. 2014;85:121–30. https://doi.org/10.1016/j.neuropharm.2014.05.032.

    Article  CAS  PubMed  Google Scholar 

  128. Rivero-Ríos P, Gómez-Suaga P, Fernández B, Madero-Pérez J, Schwab AJ, Ebert AD, Hilfiker S. Alterations in late endocytic trafficking related to the pathobiology of LRRK2-linked Parkinson’s disease. Biochem Soc Trans. 2015;43:390–5. https://doi.org/10.1042/BST20140301.

    Article  CAS  PubMed  Google Scholar 

  129. Kett LR, Dauer WT. Endolysosomal dysfunction in Parkinson’s disease: recent developments and future challenges: Endolysosomal dysfunction in PD. Mov Disord. 2016;31:1433–43. https://doi.org/10.1002/mds.26797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Small SA, Simoes-Spassov S, Mayeux R, Petsko GA. Endosomal traffic jams represent a pathogenic hub and therapeutic target in Alzheimer’s disease. Trends Neurosci. 2017;40:592–602. https://doi.org/10.1016/j.tins.2017.08.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Vaz-Silva J, Gomes P, Jin Q, Zhu M, Zhuravleva V, Quintremil S, Meira T, Silva J, Dioli C, Soares-Cunha C, Daskalakis NP, Sousa N, Sotiropoulos I, Waites CL. Endolysosomal degradation of Tau and its role in glucocorticoid-driven hippocampal malfunction. EMBO J. 2018;37:e99084. https://doi.org/10.15252/embj.201899084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature. 2009;458:445–52. https://doi.org/10.1038/nature07961.

    Article  CAS  PubMed  Google Scholar 

  133. Sahu R, Kaushik S, Clement CC, Cannizzo ES, Scharf B, Follenzi A, Potolicchio I, Nieves E, Cuervo AM, Santambrogio L. Microautophagy of cytosolic proteins by late endosomes. Dev Cell. 2011;20:131–9. https://doi.org/10.1016/j.devcel.2010.12.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Pooler AM, Hanger DP. Functional implications of the association of tau with the plasma membrane. Biochem Soc Trans. 2010;38:1012–5. https://doi.org/10.1042/BST0381012.

    Article  CAS  PubMed  Google Scholar 

  135. Georgieva ER, Xiao S, Borbat PP, Freed JH, Eliezer D. Tau binds to lipid membrane surfaces via short amphipathic helices located in its microtubule-binding repeats. Biophys J. 2014;107:1441–52. https://doi.org/10.1016/j.bpj.2014.07.046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Wolozin B. Regulated protein aggregation: stress granules and neurodegeneration. Mol Neurodegener. 2012;7:56. https://doi.org/10.1186/1750-1326-7-56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol. 2008;10:1324–32. https://doi.org/10.1038/ncb1791.

    Article  CAS  PubMed  Google Scholar 

  138. Arimoto-Matsuzaki K, Saito H, Takekawa M. TIA1 oxidation inhibits stress granule assembly and sensitizes cells to stress-induced apoptosis. Nat Commun. 2016;7:10252. https://doi.org/10.1038/ncomms10252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Kampers T, Friedhoff P, Biernat J, Mandelkow E-M, Mandelkow E. RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett. 1996;399:344–9. https://doi.org/10.1016/S0014-5793(96)01386-5.

    Article  CAS  PubMed  Google Scholar 

  140. Liu-Yesucevitz L, Bilgutay A, Zhang Y-J, Vanderwyde T, Citro A, Mehta T, Zaarur N, McKee A, Bowser R, Sherman M, Petrucelli L, Wolozin B. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS One. 2010;5(10):e13250. https://doi.org/10.1371/journal.pone.0013250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Liu-Yesucevitz L, Lin AY, Ebata A, Boon JY, Reid W, Xu Y-F, Kobrin K, Murphy GJ, Petrucelli L, Wolozin B. ALS-linked mutations enlarge TDP-43-enriched neuronal RNA granules in the dendritic arbor. J Neurosci. 2014;34:4167–74. https://doi.org/10.1523/JNEUROSCI.2350-13.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Vanderweyde T, Yu H, Varnum M, Liu-Yesucevitz L, Citro A, Ikezu T, Duff K, Wolozin B. Contrasting pathology of the stress granule proteins TIA-1 and G3BP in tauopathies. J Neurosci. 2012;32:8270–83. https://doi.org/10.1523/JNEUROSCI.1592-12.2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Vanderweyde T, Apicco DJ, Youmans-Kidder K, Ash PEA, Cook C, Lummertz da Rocha E, Jansen-West K, Frame AA, Citro A, Leszyk JD, Ivanov P, Abisambra JF, 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;15:1455–66. https://doi.org/10.1016/j.celrep.2016.04.045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Apicco DJ, Ash PEA, Maziuk B, LeBlang C, Medalla M, Al Abdullatif A, Ferragud A, Botelho E, Ballance HI, Dhawan U, Boudeau S, Cruz AL, Kashy D, Wong A, Goldberg LR, Yazdani N, Zhang C, Ung CY, Tripodis Y, Kanaan NM, Ikezu T, Cottone P, Leszyk J, Li H, Luebke J, Bryant CD, Wolozin B. Reducing the RNA binding protein TIA1 protects against tau-mediated neurodegeneration in vivo. Nat Neurosci. 2018;21:72–80. https://doi.org/10.1038/s41593-017-0022-z.

    Article  CAS  PubMed  Google Scholar 

  145. Maziuk B, Ballance HI, Wolozin B. Dysregulation of RNA binding protein aggregation in neurodegenerative disorders. Front Mol Neurosci. 2017;10:89. https://doi.org/10.3389/fnmol.2017.00089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. McEwen BS, Gray JD, Nasca C. 60 years of neuroendocrinology: redefining neuroendocrinology: stress, sex and cognitive and emotional regulation. J Endocrinol. 2015;226:T67–83. https://doi.org/10.1530/JOE-15-0121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ownby RL, Crocco E, Acevedo A, John V, Loewenstein D. Depression and risk for Alzheimer disease: systematic review, meta-analysis, and metaregression analysis. Arch Gen Psychiatry. 2006;63:530. https://doi.org/10.1001/archpsyc.63.5.530.

    Article  PubMed  PubMed Central  Google Scholar 

  148. Heun R, Kockler M, Ptok U. Depression in Alzheimer’s disease: is there a temporal relationship between the onset of depression and the onset of dementia? Eur Psychiatry. 2002;17:254–8.

    Article  PubMed  Google Scholar 

  149. Kim HK, Nunes PV, Oliveira KC, Young LT, Lafer B. Neuropathological relationship between major depression and dementia: a hypothetical model and review. Prog Neuropsychopharmacol Biol Psychiatry. 2016;67:51–7. https://doi.org/10.1016/j.pnpbp.2016.01.008.

    Article  PubMed  Google Scholar 

  150. Rapp MA, Schnaider-Beeri M, Grossman HT, Sano M, Perl DP, Purohit DP, Gorman JM, Haroutunian V. Increased hippocampal plaques and tangles in patients with Alzheimer disease with a lifetime history of major depression. Arch Gen Psychiatry. 2006;63:161–7. https://doi.org/10.1001/archpsyc.63.2.161.

    Article  PubMed  Google Scholar 

  151. Mayeux R, Honig LS, Tang M-X, Manly J, Stern Y, Schupf N, Mehta PD. Plasma A[beta]40 and A[beta]42 and Alzheimer’s disease: relation to age, mortality, and risk. Neurology. 2003;61:1185–90.

    Article  CAS  PubMed  Google Scholar 

  152. Andreasen N, Blennow K. CSF biomarkers for mild cognitive impairment and early Alzheimer’s disease. Clin Neurol Neurosurg. 2005;107:165–73. https://doi.org/10.1016/j.clineuro.2004.10.011.

    Article  PubMed  Google Scholar 

  153. Evered L, Scott DA, Silbert B, Maruff P. Postoperative cognitive dysfunction is independent of type of surgery and anesthetic. Anesth Analg. 2011;112:1179–85. https://doi.org/10.1213/ANE.0b013e318215217e.

    Article  PubMed  Google Scholar 

  154. Sun X, Steffens DC, Au R, Folstein M, Summergrad P, Yee J, Rosenberg I, Mwamburi DM, Qiu WQ. Amyloid-associated depression: a prodromal depression of Alzheimer disease? Arch Gen Psychiatry. 2008;65:542. https://doi.org/10.1001/archpsyc.65.5.542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Mateus-Pinheiro A, Pinto L, Sousa N. Epigenetic (de)regulation of adult hippocampal neurogenesis: implications for depression. Clin Epigenetics. 2011;3:5. https://doi.org/10.1186/1868-7083-3-5.

    Article  PubMed  PubMed Central  Google Scholar 

  156. Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, Rábano A, Cafini F, Pallas-Bazarra N, Ávila J, Llorens-Martín M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med. 2019;25:554–60. https://doi.org/10.1038/s41591-019-0375-9.

    Article  CAS  PubMed  Google Scholar 

  157. Gu Y, Oyama F, Ihara Y. Tau is widely expressed in rat tissues. J Neurochem. 1996;67:1235–44.

    Article  CAS  PubMed  Google Scholar 

  158. Schoch KM, DeVos SL, Miller RL, Chun SJ, Norrbom M, Wozniak DF, Dawson HN, Bennett CF, Rigo F, Miller TM. Increased 4R-tau induces pathological changes in a human-tau mouse model. Neuron. 2016;90:941–7. https://doi.org/10.1016/j.neuron.2016.04.042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ioannis Sotiropoulos .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sotiropoulos, I., Silva, J.M., Gomes, P., Sousa, N., Almeida, O.F.X. (2019). Stress and the Etiopathogenesis of Alzheimer’s Disease and Depression. In: Takashima, A., Wolozin, B., Buee, L. (eds) Tau Biology. Advances in Experimental Medicine and Biology, vol 1184. Springer, Singapore. https://doi.org/10.1007/978-981-32-9358-8_20

Download citation

Publish with us

Policies and ethics