Pathological tau promotes neuronal damage by impairing ribosomal function and decreasing protein synthesis

Journal of Neuroscience

Volumn 36, Issue 3, 2016, Pages 957-962

  Meier, Shelby ^a   Bell, Michelle ^a   Lyons, Danielle N ^a   Rodriguez Rivera, Jennifer ^a   Ingram, Alexandria ^a   Fontaine, Sarah N ^a   Mechas, Elizabeth ^a   Chen, Jing ^b   Wolozin, Benjamin ^c   Vine, Harry Le ^a,b   Zhu, Haining ^b   Abisambra, Jose F ^a,d  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Departments of Molecular and Cellular Biochemistry   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer; Ribosome; RNA; Tau; Tauopathies; Translation

Indexed keywords

ACTIN; ALPHA SYNUCLEIN; BOVINE SERUM ALBUMIN; HEAT SHOCK PROTEIN 70; INSULIN; POSTSYNAPTIC DENSITY PROTEIN 95; PUROMYCIN; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; CELL FRACTIONATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MALE; NERVE CELL LESION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RIBOSOME; RNA TRANSLATION; SURFACE PROPERTY; TANDEM MASS SPECTROMETRY; VERY ELDERLY; BIOSYNTHESIS; BRAIN; CELL CULTURE; METABOLISM; MICROSOME; NERVE CELL; PATHOLOGY; PHYSIOLOGY; TAUOPATHY;

AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; CELLS, CULTURED; FEMALE; HUMANS; MALE; MICROSOMES; NEURONS; PROTEIN BIOSYNTHESIS; RIBOSOMES; TAU PROTEINS; TAUOPATHIES;

EID: 84955056016     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3029-15.2016     Document Type: Article

References (33)

1. Abisambra JF, Fiorelli T, Padmanabhan J, Neame P, Wefes I, Potter H (2010) LDLR expression and localization are altered in mouse and human cell culture models of Alzheimer’s disease. PloS One 5:e8556. CrossRef Medline
2. Abisambra JF, Jinwal UK, Suntharalingam A, Arulselvam K, Brady S, Cock-man M, Jin Y, Zhang B, Dickey CA (2012) DnaJAl antagonizes constitutive Hsp70-mediated stabilization of tau. J Mol Biol 421:653-661. CrossRef Medline
3. Abisambra J, Jinwal UK, Miyata Y, Rogers J, Blair L, Li X, Seguin SP, Wang L, Jin Y, Bacon J, Brady S, Cockman M, Guidi C, Zhang J, Koren J, Young ZT, Atkins CA, Zhang B, Lawson LY, Weeber EJ, et al. (2013a) Allosteric heat shock protein 70 inhibitors rapidly rescue synaptic plasticity deficits by reducing aberrant tau. Biol Psychiatry 74:367-374. CrossRef Medline
4. Abisambra JF, Jinwal UK, Blair LJ, O’Leary JC 3rd, Li Q, Brady S, Wang L, Guidi CE, Zhang B, Nordhues BA, Cockman M, Suntharalingham A, Li P, Jin Y, Atkins CA, Dickey CA (2013b) Tau accumulation activates the unfolded protein response by impairing endoplasmic reticulum-associated degradation. J Neurosci 33:9498-9507. CrossRef Medline
5. Alzheimer’s Association (2014) 2014 Alzheimer’s disease facts and figures. Alzheimers Dement 10:e47-e92. CrossRef Medline
6. Ash PE, Vanderweyde TE, Youmans KL, Apicco DJ, Wolozin B (2014) Pathological stress granules in Alzheimer’s disease. Brain Res 1584:52-58. CrossRef Medline
7. Barghorn S, Zheng-Fischhofer Q, Ackmann M, Biernat J, von Bergen M, Mandelkow EM, Mandelkow E (2000) Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of fronto-temporal dementias. Biochemistry 39:11714-11721. CrossRef Medline
8. Clark LN, Poorkaj P, Wszolek Z, Geschwind DH, Nasreddine ZS, Miller B, Li D, Payami H, Awert F, Markopoulou K, Andreadis A, D’Souza I, Lee VM, Reed L, Trojanowski JQ, Zhukareva V, Bird T, Schellenberg G, Wilhelmsen KC (1998) Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci U S A95:13103-13107. CrossRef Medline
9. Ding Q, Markesbery WR, Chen Q, Li F, Keller JN (2005) Ribosomedysfunc-tion is an early event in Alzheimer’s disease. J Neurosci 25:9171-9175. CrossRef Medline
10. Duvarci S, Nader K, LeDoux JE (2008) De novo mRNA synthesis is required for both consolidation and reconsolidation of fear memories in the amygdala. Learn Mem 15:747-755. CrossRef Medline
11. Greenberg SG, Davies P, Schein JD, Binder LI (1992) Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 267:564-569. Medline
12. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A 83:4913-4917. CrossRef Medline
13. Guo JL, Lee VM (2011) Seeding ofnormal tau bypathological tau conform-ers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 286: 15317-15331. CrossRef Medline
14. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274. CrossRef Medline
15. Jinwal UK, Abisambra JF, Zhang J, Dharia S, O’Leary JC, Patel T, Braswell K, Jani T, Gestwicki JE, Dickey CA (2012) Cdc37/Hsp90 protein complex disruption triggers an autophagic clearance cascade for TDP-43 protein. J Biol Chem 287:24814-24820. CrossRef Medline
16. Jones JR, Lebar MD, Jinwal UK, Abisambra JF, Koren J 3rd, Blair L, O’Leary JC, Davey Z, Trotter J, Johnson AG, Weeber E, Eckman CB, Baker BJ, Dickey CA (2011) The diarylheptanoid (+) -aR,11S-myricanol and two flavones from bayberry (Myrica cerifera) destabilize the microtubule-associated protein tau. J Nat Prod 74:38-44. CrossRef Medline
17. Lasagna-Reeves CA, Castillo-Carranza DL, Sengupta U, Clos AL, Jackson GR, Kayed R (2011) Tau oligomers impair memoryand induce synaptic and mitochondrial dysfunction in wild-type mice. Mol Neurodegener 6:39. CrossRef Medline
18. Lopez D, Abisambra Socarrás JF, Bedi M, Ness GC (2007) Activation of the hepatic LDL receptor promoter by thyroid hormone. Biochim Biophys Acta 1771:1216-1225. CrossRef Medline
19. Marciniak SJ, Garcia-Bonilla L, Hu J, Harding HP, Ron D (2006) Activation-dependent substrate recruitmentbythe eukaryotic translation initiation factor 2 kinase PERK. J Cell Biol 172:201-209. CrossRef Medline
20. Meier S, Bell M, Lyons DN, Ingram A, Chen J, Gensel JC, Zhu H, Nelson PT, Abisambra JF (2015) Identification ofnovel tau interactions with endo-plasmic reticulum proteins in Alzheimer’s brain. J Alzheimers Dis 486:87-702. CrossRef Medline
21. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makh-inson M, He Y, Ramsay MF, Morris RG, Morrison JH, O’Dell TJ, Grant SG (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439. CrossRef Medline
22. Momeni P, Pittman A, Lashley T, Vandrovcova J, Malzer E, Luk C, Hulette C, Lees A, Revesz T, Hardy J, de Silva R (2009) Clinical and pathological features of an Alzheimer’s disease patient with the MAPT delta K280 mutation. Neurobiol Aging 30:388-393. CrossRef Medline
23. Moreno JA, Radford H, Peretti D, Steinert JR, Verity N, Martin MG, Halliday M, Morgan J, Dinsdale D, Ortori CA, Barrett DA, Tsaytler P, Bertolotti A, Willis AE, Bushell M, Mallucci GR (2012) Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 485: 507-511. CrossRef Medline
24. Nelson PT, Marton L, Saper CB (1993) Alz-50 immunohistochemistry in the normal sheep striatum: a light and electron microscope study. Brain Res 600:285-297. CrossRef Medline
25. Papasozomenos SC, Binder LI (1987) Phosphorylation determines two distinct species oftau in the central nervous system. Cell Motil Cytoskeleton 8:210-226. CrossRef Medline
26. Piao YS, Hayashi S, Wakabayashi K, Kakita A, Aida I, Yamada M, Takahashi H (2002) Cerebellar cortical tau pathology in progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol 103:469-474. CrossRef Medline
27. Rissman RA, Poon WW, Blurton-Jones M, Oddo S, Torp R, Vitek MP, LaFerla FM, Rohn TT, Cotman CW (2004) Caspase-cleavage oftau is an early event in Alzheimer disease tangle pathology. J Clin Invest 114: 121-130. CrossRef Medline
28. Rizzu P, Van Swieten JC, Joosse M, Hasegawa M, Stevens M, Tibben A, Niermeijer MF, Hillebrand M, Ravid R, Oostra BA, Goedert M, van Duijn CM, Heutink P (1999) High prevalence of mutations in the mic-rotubule-associated protein tau in a population study offrontotemporal dementia in The Netherlands. Am J Hum Genet 64:414-421. CrossRef Medline
29. Rosso SM, Donker Kaat L, Baks T, Joosse M, de Koning I, Pijnenburg Y, de Jong D, Dooijes D, Kamphorst W, Ravid R, Niermeijer MF, Verheij F, Kremer HP, Scheltens P, van Duijn CM, Heutink P, van Swieten JC (2003) Frontotemporal dementia in The Netherlands: patient characteristics and prevalence estimates from a population-based study. Brain 126: 2016-2022. CrossRef Medline
30. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, Forster C, Yue M, Orne J, Janus C, Mariash A, Kuskowski M, Hyman B, Hutton M, Ashe KH (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309:476-481. CrossRef Medline
31. Schmidt EK, Clavarino G, Ceppi M, Pierre P (2009) SUnSET, a nonradio-active method to monitor protein synthesis. Nat Methods 6:275-277. CrossRef Medline
32. Vanderweyde T, Yu H, Varnum M, Liu-Yesucevitz L, Citro A, Ikezu T, Duff K, Wolozin B (2012) Contrasting pathology of the stress granule proteins TIA-1 and G3BP intauopathies. J Neurosci 32:8270-8283. CrossRef Medline
33. Zhang CC, Xing A, Tan MS, Tan L, Yu JT (2015) The role of MAPT in neurodegenerative diseases: genetics, mechanisms and therapy. Mol Neu-robiol. Advance online publication. Retrieved Sep. 12, 2015. CrossRef Medline