Accelerated neurodegeneration through chaperone-mediated oligomerization of tau

Journal of Clinical Investigation

Volumn 123, Issue 10, 2013, Pages 4158-4169

  Blair, Laura J ^a   Nordhues, Bryce A ^a   Hill, Shannon E ^b   Scaglione, K Matthew ^c   O'Leary III, John C ^a   Fontaine, Sarah N ^a   Breydo, Leonid ^a   Zhang, Bo ^a   Li, Pengfei ^a   Wang, Li ^a   Cotman, Carl ^d   Paulson, Henry L ^c   Muschol, Martin ^b   Uversky, Vladimir N ^a,e   Klengel, Torsten ^f   Binder, Elisabeth B ^f   Kayed, Rakez ^g   Golde, Todd E ^h   Berchtold, Nicole ^d   Dickey, Chad A ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^f MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^g University of Texas Medical Branch School of Medicine   (United States)

^h UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; FK 506 BINDING PROTEIN; HEAT SHOCK PROTEIN 90; MESSENGER RNA; PROTEASOME; TAU PROTEIN; TACROLIMUS BINDING PROTEIN 5;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DEMETHYLATION; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TAUOPATHY; TRANSGENIC MOUSE; ADULT; AGED; ANIMAL; CASE CONTROL STUDY; CHEMISTRY; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HIPPOCAMPAL CA3 REGION; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID; ANIMALS; CA3 REGION, HIPPOCAMPAL; CASE-CONTROL STUDIES; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEK293 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEOLYSIS; TACROLIMUS BINDING PROTEINS; TAU PROTEINS; YOUNG ADULT;

EID: 84885054226     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69003     Document Type: Article

References (71)

1. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl). 1991;82(4):239-259.
2. Gomez-Isla T, et al. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol. 1997;41(1):17-24.
3. Lasagna-Reeves CA, et al. Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J. 2012;26(5):1946-1959.
4. de Calignon A, et al. Caspase activation precedes and leads to tangles. Nature. 2010;464(7292):1201-1204.
5. Santacruz K, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science. 2005;309(5733):476-481.
6. de Calignon A, et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron. 2012;73(4):685-697.
7. Clavaguera F, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol. 2009;11(7):909-913.
8. Liu L, et al. Trans-synaptic spread of tau pathology in vivo. PLoS One. 2012;7(2):e31302.
9. Hutton M, et al. Association of missense and 5'-splicesite mutations in tau with the inherited dementia FTDP-17. Nature. 1998;393(6686):702-705.
10. Ros R, et al. A new mutation of the tau gene, G303V, in early-onset familial progressive supranuclear palsy. Arch Neurol. 2005;62(9):1444-1450.
11. Dumanchin C, et al. Segregation of a missense mutation in the microtubule-associated protein tau gene with familial frontotemporal dementia and parkinsonism. Hum Mol Genet. 1998;7(11):1825-1829.
12. Gresham D, Dunham MJ, Botstein D. Comparing whole genomes using DNA microarrays. Nat Rev Genet. 2008;9(4):291-302.
13. Colantuoni C, et al. Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature. 2011;478(7370):519-523.
14. Thompson AD, et al. Analysis of the tau-associated proteome reveals that exchange of Hsp70 for Hsp90 is involved in tau degradation. ACS Chem Biol. 2012;7(10):1677-1686.
15. Sherman MY, Goldberg AL. Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron. 2001;29(1):15-32.
16. Dickey CA, et al. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J Clin Invest. 2007;117(3):648-658.
17. Jinwal UK, et al. The Hsp90 cochaperone, FKBP51, increases Tau stability and polymerizes microtubules. J Neurosci. 2010;30(2):591-599.
18. Luo W, et al. Roles of heat-shock protein 90 in maintaining and facilitating the neurodegenerative phenotype in tauopathies. Proc Natl Acad Sci U S A. 2007;104(22):9511-9516.
19. Dickey CA, et al. HSP induction mediates selective clearance of tau phosphorylated at proline-directed Ser/Thr sites but not KXGS (MARK) sites. FASEB J. 2006;20(6):753-755.
20. Tortosa E, Santa-Maria I, Moreno F, Lim F, Perez M, Avila J. Binding of Hsp90 to tau promotes a conformational change and aggregation of tau protein. J Alzheimers Dis. 2009;17(2):319-325.
21. Liou YC, et al. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature. 2003;424(6948):556-561.
22. Pastorino L, et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature. 2006;440(7083):528-534.
23. Koberle M, et al. Yersinia enterocolitica YopT and Clostridium difficile toxin B induce expression of GILZ in epithelial cells. PLoS One. 2012;7(7):e40730.
24. Binder EB, et al. Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat Genet. 2004;36(12):1319-1325.
25. Smith DF, Baggenstoss BA, Marion TN, Rimerman RA. Two FKBP-related proteins are associated with progesterone receptor complexes. J Biol Chem. 1993;268(24):18365-18371.
26. Radanyi C, Chambraud B, Baulieu EE. The ability of the immunophilin FKBP59-HBI to interact with the 90-kDa heat shock protein is encoded by its tetratricopeptide repeat domain. Proc Natl Acad Sci U S A. 1994;91(23):11197- 11201.
27. Blatch GL, Lassle M. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays. 1999;21(11):932-939.
28. Pirkl F, Buchner J. Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J Mol Biol. 2001;308(4):795-806.
29. Schulke JP, et al. Differential impact of tetratricopeptide repeat proteins on the steroid hormone receptors. PLoS One. 2010;5(7):e11717.
30. O'Leary JC, et al. A new anti-depressive strategy for the elderly: ablation of FKBP5/FKBP51. PLoS One. 2011;6(9):e24840.
31. Tranguch S, et al. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc Natl Acad Sci U S A. 2005;102(40):14326-14331.
32. David DC, Layfield R, Serpell L, Narain Y, Goedert M, Spillantini MG. Proteasomal degradation of tau protein. J Neurochem. 2002;83:176-185.
33. Grune T, et al. Tau protein degradation is catalyzed by the ATP/ubiquitin-independent 20S proteasome under normal cell conditions. Arch Biochem Biophys. 2010;500(2):181-188.
34. Shringarpure R, Grune T, Davies KJ. Protein oxidation and 20S proteasome-dependent proteolysis in mammalian cells. Cell Mol Life Sci. 2001;58(10):1442-1450.
35. Coux O, Tanaka K, Goldberg AL. Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem. 1996;65:801-847.
36. Schweers O, Schonbrunn-Hanebeck E, Marx A, Mandelkow E. Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure. J Biol Chem. 1994;269(39):24290-24297.
37. Prodromou C, et al. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 1999;18(3):754-762.
38. Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN. PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta. 2010;1804(4):996-1010.
39. Whitmore L, Wallace BA. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers. 2008;89(5):392-400.
40. Uversky VN, Li J, Fink AL. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J Biol Chem. 2001;276(14):10737-10744.
41. Munishkina LA, Fink AL, Uversky VN. Conformational prerequisites for formation of amyloid fibrils from histones. J Mol Biol. 2004;342(4):1305-1324.
42. Uversky VN, Fink AL. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta. 2004;1698(2):131-153.
43. Chirita CN, Congdon EE, Yin H, Kuret J. Triggers of full-length tau aggregation: a role for partially folded intermediates. Biochemistry. 2005;44(15):5862-5872.
44. Abisambra JF, et al. Phosphorylation dynamics regulate Hsp27-mediated rescue of neuronal plasticity deficits in tau transgenic mice. J Neurosci. 2010;30(46):15374-15382.
45. Berger Z, et al. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J Neurosci. 2007;27(14):3650-3662.
46. O'Leary JC, et al. Phenothiazine-mediated rescue of cognition in tau transgenic mice requires neuroprotection and reduced soluble tau burden. Mol Neurodegener. 2010;5:45.
47. Dickey C, et al. Aging analysis reveals slowed tau turnover and enhanced stress response in a mouse model of tauopathy. Am J Pathol. 2009;174(1):228-238.
48. Ramsden M, et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci. 2005;25(46):10637-10647.
49. Spires TL, et al. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am J Pathol. 2006;168(5):1598-1607.
50. Sun A, Nguyen XV, Bing G. Comparative analysis of an improved thioflavin-s stain, Gallyas silver stain, and immunohistochemistry for neurofibrillary tangle demonstration on the same sections. J Histochem Cytochem. 2002;50(4):463-472.
51. Cribbs DH, et al. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J Neuroinflammation. 2012;9:179.
52. Dickey CA, et al. Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species. J Neurosci. 2006;26(26):6985-6996.
53. Petrucelli L, et al. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet. 2004;13(7):703-714.
54. Klengel T, et al. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci. 2013;16(1):33-41.
55. Spires-Jones TL, Kopeikina KJ, Koffie RM, de Calignon A, Hyman BT. Are tangles as toxic as they look? J Mol Neurosci. 2011;45(3):438-444.
56. Wittmann CW, et al. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science. 2001;293(5530):711-714.
57. Lee RS, et al. Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinology. 2010;151(9):4332-4343.
58. Yang X, et al. Glucocorticoid-induced loss of DNA methylation in non-neuronal cells and potential involvement of DNMT1 in epigenetic regulation of Fkbp5. Biochem Biophys Res Commun. 2012;420(3):570-575.
59. Davis KL, et al. Cortisol and Alzheimer's disease, I: Basal studies. Am J Psychiatry. 1986;143(3):300-305.
60. Lichtenberg B, Mandelkow EM, Hagestedt T, Mandelkow E. Structure and elasticity of microtubule-associated protein tau. Nature. 1988;334(6180):359- 362.
61. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science. 2008;319(5865):916-919.
62. Bennett EJ, Bence NF, Jayakumar R, Kopito RR. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell. 2005;17(3):351-365.
63. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 2001;292(5521):1552-1555.
64. Gillardon F, et al. The 20S proteasome isolated from Alzheimer's disease brain shows post-translational modifications but unchanged proteolytic activity. J Neurochem. 2007;101(6):1483-1490.
65. Gregori L, Hainfeld JF, Simon MN, Goldgaber D. Binding of amyloid beta protein to the 20 S proteasome. J Biol Chem. 1997;272(1):58-62.
66. Eisenberg D, Jucker M. The amyloid state of proteins in human diseases. Cell. 2012;148(6):1188-1203.
67. Spires-Jones TL, et al. In vivo imaging reveals dissociation between caspase activation and acute neuronal death in tangle-bearing neurons. J Neurosci. 2008;28(4):862-867.
68. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron. 2004;43(3):321-332.
69. O'Leary JC, Koren J, Dickey CA. Neuronal life span versus health span: principles of natural selection at work in the degenerating brain. J Mol Neurosci. 2011;45(3):467-472.
70. Brunden KR, Trojanowski JQ, Lee VM. Evidence that non-fibrillar tau causes pathology linked to neurodegeneration and behavioral impairments. J Alzheimers Dis. 2008;14(4):393-399.
71. Marx J. Alzheimer's disease. A new t ake on tau. Science. 2007;316(5830):1416-1417.