NMNAT2:HSP90 Complex Mediates Proteostasis in Proteinopathies

PLoS Biology

Volumn 14, Issue 6, 2016, Pages

  Ali, Yousuf O ^a,b,c   Allen, Hunter M ^a,b   Yu, Lei ^d   Li Kroeger, David ^b,c   Bakhshizadehmahmoudi, Dena ^a,b,c   Hatcher, Asante ^b,c   McCabe, Cristin ^e   Xu, Jishu ^f   Bjorklund, Nicole ^g   Taglialatela, Giulio ^g   Bennett, David A ^d   De Jager, Philip L ^e,f,h   Shulman, Joshua M ^b,c   Bellen, Hugo J ^b,c   Lu, Hui Chen ^a,b,c  

^a INDIANA UNIVERSITY   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d RUSH UNIVERSITY MEDICAL CENTER   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

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

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONE; HEAT SHOCK PROTEIN 90; MESSENGER RNA; NICOTINAMIDE MONONUCLEOTIDE ADENYLYLTRANSFERASE 2; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; TAU PROTEIN; UNCLASSIFIED DRUG; NMNAT2 PROTEIN, HUMAN; PROTEIN BINDING;

ALZHEIMER DISEASE; ARTICLE; BRAIN CELL; COGNITION; COMPLEX FORMATION; CONTROLLED STUDY; EXCITOTOXICITY; HUMAN; HUMAN TISSUE; NEUROFIBRILLARY TANGLE; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN REFOLDING; SENILE PLAQUE; SPINOCEREBELLAR DEGENERATION; SYNAPSE; AGED; ANIMAL; BRAIN; CELL CULTURE; CHLOROCEBUS AETHIOPS; COS CELL LINE; CYTOLOGY; FEMALE; FLUORESCENCE MICROSCOPY; GENETICS; MALE; METABOLISM; MIDDLE AGED; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; VERY ELDERLY; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; BLOTTING, WESTERN; BRAIN; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COGNITION; COS CELLS; FEMALE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; MOLECULAR CHAPERONES; MUTATION; NEURONS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STABILITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84979085126     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002472     Document Type: Article

References (114)

1. Zhai RG, Cao Y, Hiesinger PR, Zhou Y, Mehta SQ, Schulze KL, et al. Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biol. 2006;4(12):e416. 17132048
2. Zhai RG, Zhang F, Hiesinger PR, Cao Y, Haueter CM, Bellen HJ, NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature. 2008;452(7189):887–91. doi: 10.1038/nature0672118344983
3. Chiang PW, Wang J, Chen Y, Fu Q, Zhong J, Chen Y, et al. Exome sequencing identifies NMNAT1 mutations as a cause of Leber congenital amaurosis. Nat Genet. 2012;44(9):972–4. doi: 10.1038/ng.237022842231
4. Koenekoop RK, Wang H, Majewski J, Wang X, Lopez I, Ren H, et al. Mutations in NMNAT1 cause Leber congenital amaurosis and identify a new disease pathway for retinal degeneration. Nat Genet. 2012;44(9):1035–9. doi: 10.1038/ng.235622842230
5. Perrault I, Hanein S, Zanlonghi X, Serre V, Nicouleau M, Defoort-Delhemmes S, et al. Mutations in NMNAT1 cause Leber congenital amaurosis with early-onset severe macular and optic atrophy. Nat Genet. 2012;44(9):975–7. doi: 10.1038/ng.235722842229
6. Falk MJ, Zhang Q, Nakamaru-Ogiso E, Kannabiran C, Fonseca-Kelly Z, Chakarova C, et al. NMNAT1 mutations cause Leber congenital amaurosis. Nat Genet. 2012;44(9):1040–5. doi: 10.1038/ng.236122842227
7. Ali YO, Li-Kroeger D, Bellen HJ, Zhai RG, Lu HC, NMNATs, evolutionarily conserved neuronal maintenance factors. Trends Neurosci. 2013;36(11):632–40. doi: 10.1016/j.tins.2013.07.00223968695
8. Conforti L, Gilley J, Coleman MP, Wallerian degeneration: an emerging axon death pathway linking injury and disease. Nat Rev Neurosci. 2014;15(6):394–409. doi: 10.1038/nrn368024840802
9. Araki T, Sasaki Y, Milbrandt J, Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science. 2004;305(5686):1010–3. 15310905
10. Sasaki Y, Araki T, Milbrandt J, Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2006;26(33):8484–91.
11. Wang J, Zhai Q, Chen Y, Lin E, Gu W, McBurney MW, et al. A local mechanism mediates NAD-dependent protection of axon degeneration. The Journal of cell biology. 2005;170(3):349–55. 16043516
12. Sasaki Y, Vohra BP, Lund FE, Milbrandt J, Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009;29(17):5525–35.
13. Conforti L, Wilbrey A, Morreale G, Janeckova L, Beirowski B, Adalbert R, et al. Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. The Journal of cell biology. 2009;184(4):491–500. doi: 10.1083/jcb.20080717519237596
14. Yan T, Feng Y, Zheng J, Ge X, Zhang Y, Wu D, et al. Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem Int. 2010;56(1):101–6. doi: 10.1016/j.neuint.2009.09.00719778564
15. Gilley J, Coleman MP, Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010;8(1):e1000300. doi: 10.1371/journal.pbio.100030020126265
16. Milde S, Gilley J, Coleman MP, Subcellular localization determines the stability and axon protective capacity of axon survival factor Nmnat2. PLoS Biol. 2013;11(4):e1001539. doi: 10.1371/journal.pbio.100153923610559
17. Milde S, Fox AN, Freeman MR, Coleman MP, Deletions within its subcellular targeting domain enhance the axon protective capacity of Nmnat2 in vivo. Sci Rep. 2013;3:2567. doi: 10.1038/srep0256723995269
18. Hicks AN, Lorenzetti D, Gilley J, Lu B, Andersson KE, Miligan C, et al. Nicotinamide mononucleotide adenylyltransferase 2 (Nmnat2) regulates axon integrity in the mouse embryo. PLoS ONE. 2012;7(10):e47869. doi: 10.1371/journal.pone.004786923082226
19. Gilley J, Adalbert R, Yu G, Coleman MP, Rescue of peripheral and CNS axon defects in mice lacking NMNAT2. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2013;33(33):13410–24.
20. Wang JT, Barres BA, Axon degeneration: where the Wlds things are. Curr Biol. 2012;22(7):R221–3. doi: 10.1016/j.cub.2012.02.05622497934
21. Wang JT, Medress ZA, Barres BA, Axon degeneration: molecular mechanisms of a self-destruction pathway. The Journal of cell biology. 2012;196(1):7–18. doi: 10.1083/jcb.20110811122232700
22. Morfini GA, Burns M, Binder LI, Kanaan NM, LaPointe N, Bosco DA, et al. Axonal transport defects in neurodegenerative diseases. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009;29(41):12776–86.
23. Adalbert R, Coleman MP, Review: Axon pathology in age-related neurodegenerative disorders. Neuropathol Appl Neurobiol. 2013;39(2):90–108. doi: 10.1111/j.1365-2990.2012.01308.x23046254
24. Mayer PR, Huang N, Dewey CM, Dries DR, Zhang H, Yu G, Expression, localization, and biochemical characterization of nicotinamide mononucleotide adenylyltransferase 2. The Journal of biological chemistry. 2010;285(51):40387–96. doi: 10.1074/jbc.M110.17891320943658
25. Orsomando G, Cialabrini L, Amici A, Mazzola F, Ruggieri S, Conforti L, et al. Simultaneous single-sample determination of NMNAT isozyme activities in mouse tissues. PLoS ONE. 2012;7(12):e53271. doi: 10.1371/journal.pone.005327123300904
26. Liang WS, Dunckley T, Beach TG, Grover A, Mastroeni D, Walker DG, et al. Gene expression profiles in anatomically and functionally distinct regions of the normal aged human brain. Physiol Genomics. 2007;28(3):311–22. 17077275
27. Liang WS, Reiman EM, Valla J, Dunckley T, Beach TG, Grover A, et al. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc Natl Acad Sci U S A. 2008;105(11):4441–6. doi: 10.1073/pnas.070925910518332434
28. Van Deerlin VM, Sleiman PM, Martinez-Lage M, Chen-Plotkin A, Wang LS, Graff-Radford NR, et al. Common variants at 7p21 are associated with frontotemporal lobar degeneration with TDP-43 inclusions. Nat Genet. 2010;42(3):234–9. doi: 10.1038/ng.53620154673
29. Lesnick TG, Papapetropoulos S, Mash DC, Ffrench-Mullen J, Shehadeh L, de Andrade M, et al. A genomic pathway approach to a complex disease: axon guidance and Parkinson disease. PLoS Genet. 2007;3(6):e98. 17571925
30. Moran LB, Duke DC, Deprez M, Dexter DT, Pearce RK, Graeber MB, Whole genome expression profiling of the medial and lateral substantia nigra in Parkinson's disease. Neurogenetics. 2006;7(1):1–11. 16344956
31. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, Hughes G, et al. Regional and cellular gene expression changes in human Huntington's disease brain. Hum Mol Genet. 2006;15(6):965–77. 16467349
32. Ljungberg MC, Ali YO, Zhu J, Wu CS, Oka K, Zhai RG, et al. CREB-activity and nmnat2 transcription are down-regulated prior to neurodegeneration, while NMNAT2 over-expression is neuroprotective, in a mouse model of human tauopathy. Hum Mol Genet. 2012;21(2):251–67. doi: 10.1093/hmg/ddr49222027994
33. Ellis J, Proteins as molecular chaperones. Nature. 1987;328(6129):378–9. 3112578
34. Gestwicki JE, Garza D, Protein quality control in neurodegenerative disease. Prog Mol Biol Transl Sci. 2012;107:327–53. doi: 10.1016/B978-0-12-385883-2.00003-522482455
35. Hartl FU, Bracher A, Hayer-Hartl M, Molecular chaperones in protein folding and proteostasis. Nature. 2011;475(7356):324–32. doi: 10.1038/nature1031721776078
36. Sharma M, Burre J, Bronk P, Zhang Y, Xu W, Sudhof TC, CSPalpha knockout causes neurodegeneration by impairing SNAP-25 function. EMBO J. 2012;31(4):829–41. doi: 10.1038/emboj.2011.46722187053
37. Sharma M, Burre J, Sudhof TC, CSPalpha promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nature cell biology. 2011;13(1):30–9. doi: 10.1038/ncb213121151134
38. Tobaben S, Thakur P, Fernandez-Chacon R, Sudhof TC, Rettig J, Stahl B, A trimeric protein complex functions as a synaptic chaperone machine. Neuron. 2001;31(6):987–99. 11580898
39. Zinsmaier KE, Bronk P, Molecular chaperones and the regulation of neurotransmitter exocytosis. Biochem Pharmacol. 2001;62(1):1–11. 11377391
40. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S, Paralysis and early death in cysteine string protein mutants of Drosophila. Science. 1994;263(5149):977–80. 8310297
41. Benitez BA, Alvarado D, Cai Y, Mayo K, Chakraverty S, Norton J, et al. Exome-sequencing confirms DNAJC5 mutations as cause of adult neuronal ceroid-lipofuscinosis. PLoS ONE. 2011;6(11):e26741. doi: 10.1371/journal.pone.002674122073189
42. Noskova L, Stranecky V, Hartmannova H, Pristoupilova A, Baresova V, Ivanek R, et al. Mutations in DNAJC5, encoding cysteine-string protein alpha, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. American journal of human genetics. 2011;89(2):241–52. doi: 10.1016/j.ajhg.2011.07.00321820099
43. Selkoe DJ, Altered structural proteins in plaques and tangles: what do they tell us about the biology of Alzheimer's disease?Neurobiology of aging. 1986;7(6):425–32. 3104810
44. Soto C, Estrada LD, Protein misfolding and neurodegeneration. Arch Neurol. 2008;65(2):184–9. doi: 10.1001/archneurol.2007.5618268186
45. Calamini B, Morimoto RI, Protein homeostasis as a therapeutic target for diseases of protein conformation. Curr Top Med Chem. 2012;12(22):2623–40. 23339312
46. Petrucelli L, Dickson D, Kehoe K, Taylor J, Snyder H, Grover A, et al. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet. 2004;13(7):703–14. 14962978
47. Evans CG, Wisen S, Gestwicki JE, Heat shock proteins 70 and 90 inhibit early stages of amyloid beta-(1–42) aggregation in vitro. The Journal of biological chemistry. 2006;281(44):33182–91. 16973602
48. Baldwin AJ, Knowles TP, Tartaglia GG, Fitzpatrick AW, Devlin GL, Shammas SL, et al. Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc. 2011;133(36):14160–3. doi: 10.1021/ja201770321650202
49. Shammas SL, Waudby CA, Wang S, Buell AK, Knowles TP, Ecroyd H, et al. Binding of the molecular chaperone alphaB-crystallin to Abeta amyloid fibrils inhibits fibril elongation. Biophys J. 2011;101(7):1681–9. doi: 10.1016/j.bpj.2011.07.05621961594
50. Wilhelmus MM, Otte-Holler I, Wesseling P, de Waal RM, Boelens WC, Verbeek MM, Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropathology and applied neurobiology. 2006;32(2):119–30. 16599941
51. Wyttenbach A, Carmichael J, Swartz J, Furlong RA, Narain Y, Rankin J, et al. Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease. Proc Natl Acad Sci U S A. 2000;97(6):2898–903. 10717003
52. Bennett DA, Schneider JA, Arvanitakis Z, Wilson RS, Overview and findings from the religious orders study. Curr Alzheimer Res. 2012;9(6):628–45. 22471860
53. Bennett DA, Schneider JA, Buchman AS, Barnes LL, Boyle PA, Wilson RS, Overview and findings from the rush Memory and Aging Project. Curr Alzheimer Res. 2012;9(6):646–63. 22471867
54. Bennett DA, Wilson RS, Arvanitakis Z, Boyle PA, de Toledo-Morrell L, Schneider JA, Selected findings from the Religious Orders Study and Rush Memory and Aging Project. J Alzheimers Dis. 2013;33Suppl 1:S397–403. doi: 10.3233/JAD-2012-12900722647261
55. Bennett DA, Schneider JA, Arvanitakis Z, Kelly JF, Aggarwal NT, Shah RC, et al. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology. 2006;66(12):1837–44. 16801647
56. Bennett DA, Wilson RS, Schneider JA, Evans DA, Aggarwal NT, Arnold SE, et al. Apolipoprotein E epsilon4 allele, AD pathology, and the clinical expression of Alzheimer's disease. Neurology. 2003;60(2):246–52. 12552039
57. Wright S, Correlation and causation Part I. Method of path coefficients. J Agric Res. 1920;20:0557–85.
58. Lleras C, Path Analysis. Encyclopedia of Social Measurement. 2005;3.1.
59. Matsueda RL, Key advances in the history of structural equation modeling. Handbook of Structural Equation Modeling. 2012:17–42.
60. Yu L, Boyle PA, Leurgans S, Schneider JA, Bennett DA, Disentangling the effects of age and APOE on neuropathology and late life cognitive decline. Neurobiology of aging. 2014;35(4):819–26. doi: 10.1016/j.neurobiolaging.2013.10.07424199961
61. Youmans KL, Leung S, Zhang J, Maus E, Baysac K, Bu G, et al. Amyloid-beta42 alters apolipoprotein E solubility in brains of mice with five familial AD mutations. J Neurosci Methods. 2011;196(1):51–9. doi: 10.1016/j.jneumeth.2010.12.02521219931
62. Zerbinatti CV, Wozniak DF, Cirrito J, Cam JA, Osaka H, Bales KR, et al. Increased soluble amyloid-beta peptide and memory deficits in amyloid model mice overexpressing the low-density lipoprotein receptor-related protein. Proc Natl Acad Sci U S A. 2004;101(4):1075–80. 14732699
63. Hanger DP, Brion JP, Gallo JM, Cairns NJ, Luthert PJ, Anderton BH, Tau in Alzheimer's disease and Down's syndrome is insoluble and abnormally phosphorylated. Biochem J. 1991;275 (Pt 1):99–104. 1826835
64. Koren J, 3rdJinwal UK, Lee DC, Jones JR, Shults CL, Johnson AG, et al. Chaperone signalling complexes in Alzheimer's disease. J Cell Mol Med. 2009;13(4):619–30. 19449461
65. Parsell DA, Kowal AS, Lindquist S, Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. The Journal of biological chemistry. 1994;269(6):4480–7. 8308017
66. Parsell DA, Kowal AS, Singer MA, Lindquist S, Protein disaggregation mediated by heat-shock protein Hsp104. Nature. 1994;372(6505):475–8. 7984243
67. Chang Z, Primm TP, Jakana J, Lee IH, Serysheva I, Chiu W, et al. Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. The Journal of biological chemistry. 1996;271(12):7218–23. 8636160
68. Brunetti L, Di Stefano M, Ruggieri S, Cimadamore F, Magni G, Homology modeling and deletion mutants of human nicotinamide mononucleotide adenylyltransferase isozyme 2: new insights on structure and function relationship. Protein Sci. 2010;19(12):2440–50. doi: 10.1002/pro.52620954240
69. Berger F, Lau C, Dahlmann M, Ziegler M, Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. The Journal of biological chemistry. 2005;280(43):36334–41. 16118205
70. Yalowitz JA, Xiao S, Biju MP, Antony AC, Cummings OW, Deeg MA, et al. Characterization of human brain nicotinamide 5'-mononucleotide adenylyltransferase-2 and expression in human pancreas. Biochem J. 2004;377(Pt 2):317–26. 14516279
71. Gething MJ, Sambrook J, Protein folding in the cell. Nature. 1992;355(6355):33–45. 1731198
72. Hayer-Hartl MK, Weber F, Hartl FU, Mechanism of chaperonin action: GroES binding and release can drive GroEL-mediated protein folding in the absence of ATP hydrolysis. EMBO J. 1996;15(22):6111–21. 8947033
73. Kim HJ, Song EJ, Lee YS, Kim E, Lee KJ, Human Fas-associated factor 1 interacts with heat shock protein 70 and negatively regulates chaperone activity. The Journal of biological chemistry. 2005;280(9):8125–33. 15596450
74. Wickner S, Gottesman S, Skowyra D, Hoskins J, McKenney K, Maurizi MR, A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci U S A. 1994;91(25):12218–22. 7991609
75. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). The Journal of neuroscience: the official journal of the Society for Neuroscience. 2005;25(46):10637–47.
76. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science. 2005;309(5733):476–81. 16020737
77. Bandyopadhyay B, Li G, Yin H, Kuret J, Tau aggregation and toxicity in a cell culture model of tauopathy. The Journal of biological chemistry. 2007;282(22):16454–64. 17428800
78. Otvos L, Jr.Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM, Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res. 1994;39(6):669–73. 7534834
79. Jicha GA, Bowser R, Kazam IG, Davies P, Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res. 1997;48(2):128–32. 9130141
80. Tanemura K, Chui DH, Fukuda T, Murayama M, Park JM, Akagi T, et al. Formation of tau inclusions in knock-in mice with familial Alzheimer disease (FAD) mutation of presenilin 1 (PS1). The Journal of biological chemistry. 2006;281(8):5037–41. 16377636
81. Saibil H, Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol. 2013;14(10):630–42. doi: 10.1038/nrm365824026055
82. Schulte TW, Neckers LM, The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother Pharmacol. 1998;42(4):273–9. 9744771
83. Voellmy R, On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones. 2004;9(2):122–33. 15497499
84. Guo Y, Guettouche T, Fenna M, Boellmann F, Pratt WB, Toft DO, et al. Evidence for a mechanism of repression of heat shock factor 1 transcriptional activity by a multichaperone complex. The Journal of biological chemistry. 2001;276(49):45791–9. 11583998
85. Samarasinghe B, Wales CT, Taylor FR, Jacobs AT, Heat shock factor 1 confers resistance to Hsp90 inhibitors through p62/SQSTM1 expression and promotion of autophagic flux. Biochem Pharmacol. 2014;87(3):445–55. doi: 10.1016/j.bcp.2013.11.01424291777
86. Yoon YJ, Kim JA, Shin KD, Shin DS, Han YM, Lee YJ, et al. KRIBB11 inhibits HSP70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. The Journal of biological chemistry. 2011;286(3):1737–47. doi: 10.1074/jbc.M110.17944021078672
87. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, Zoghbi HY, Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat Genet. 1998;19(2):148–54. 9620770
88. Behl C, Widmann M, Trapp T, Holsboer F, 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun. 1995;216(2):473–82. 7488136
89. Wishart TM, Parson SH, Gillingwater TH, Synaptic vulnerability in neurodegenerative disease. J Neuropathol Exp Neurol. 2006;65(8):733–9. 16896307
90. Di Stefano M, Nascimento-Ferreira I, Orsomando G, Mori V, Gilley J, Brown R, et al. A rise in NAD precursor nicotinamide mononucleotide (NMN) after injury promotes axon degeneration. Cell death and differentiation. 2015;22(5):731–42. doi: 10.1038/cdd.2014.16425323584
91. Zang S, Ali YO, Ruan K, Zhai RG, Nicotinamide mononucleotide adenylyltransferase maintains active zone structure by stabilizing Bruchpilot. EMBO Rep. 2013;14(1):87–94. doi: 10.1038/embor.2012.18123154466
92. Caccamo A, Maldonado MA, Bokov AF, Majumder S, Oddo S, CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A. 2010;107(52):22687–92. doi: 10.1073/pnas.101285110821149712
93. Bennett DA, Schneider JA, Aggarwal NT, Arvanitakis Z, Shah RC, Kelly JF, et al. Decision rules guiding the clinical diagnosis of Alzheimer's disease in two community-based cohort studies compared to standard practice in a clinic-based cohort study. Neuroepidemiology. 2006;27(3):169–76. 17035694
94. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM, Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34(7):939–44. 6610841
95. Bennett DA, Wilson RS, Schneider JA, Evans DA, Beckett LA, Aggarwal NT, et al. Natural history of mild cognitive impairment in older persons. Neurology. 2002;59(2):198–205. 12136057
96. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, et al. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol. 2006;7:3. 16448564
97. Trapnell C, Pachter L, Salzberg SL, TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11. doi: 10.1093/bioinformatics/btp12019289445
98. Braak H, Braak E, Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82(4):239–59. 1759558
99. Livak KJ, Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. 11846609
100. Lee GJ, Assaying proteins for molecular chaperone activity. Methods Cell Biol. 1995;50:325–34. 8531805
101. Michels AA, Kanon B, Konings AW, Ohtsuka K, Bensaude O, Kampinga HH, Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. The Journal of biological chemistry. 1997;272(52):33283–9. 9407119
102. Rutherford SL, Lindquist S, Hsp90 as a capacitor for morphological evolution. Nature. 1998;396(6709):336–42. 9845070
103. Carroll JC, Iba M, Bangasser DA, Valentino RJ, James MJ, Brunden KR, et al. Chronic stress exacerbates tau pathology, neurodegeneration, and cognitive performance through a corticotropin-releasing factor receptor-dependent mechanism in a transgenic mouse model of tauopathy. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2011;31(40):14436–49.
104. Fischer I, Shea TB, Sapirstein VS, Kosik KS, Expression and distribution of microtubule-associated protein 2 (MAP2) in neuroblastoma and primary neuronal cells. Brain research. 1986;390(1):99–109. 3512042
105. Kosik KS, Finch EA, MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1987;7(10):3142–53.
106. Mosmann T, Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63. 6606682
107. Bjorklund NL, Sadagoparamanujam VM, Taglialatela G, Selective, quantitative measurement of releasable synaptic zinc in human autopsy hippocampal brain tissue from Alzheimer's disease patients. J Neurosci Methods. 2012;203(1):146–51. doi: 10.1016/j.jneumeth.2011.09.00821945000
108. Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol. 2012;123(1):1–11. doi: 10.1007/s00401-011-0910-322101365
109. Haglid KG, Stavrou D, Water-soluble and pentanol-extractable proteins in human brain normal tissue and human brain tumours, with special reference to S-100 protein. Journal of neurochemistry. 1973;20(6):1523–32. 4352513
110. Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, et al. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron. 2010;68(6):1067–81. doi: 10.1016/j.neuron.2010.11.03021172610
111. Spires TL, Orne JD, SantaCruz K, Pitstick R, Carlson GA, Ashe KH, et al. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. The American journal of pathology. 2006;168(5):1598–607. 16651626
112. Jin M, Shepardson N, Yang T, Chen G, Walsh D, Selkoe DJ, Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci U S A. 2011;108(14):5819–24. doi: 10.1073/pnas.101703310821421841
113. Resta V, Novelli E, Di Virgilio F, Galli-Resta L, Neuronal death induced by endogenous extracellular ATP in retinal cholinergic neuron density control. Development. 2005;132(12):2873–82. 15930116
114. Faddis BT, Hasbani MJ, Goldberg MP, Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1997;17(3):951–9.