Longitudinal measures of proteostasis in live neurons: Features that determine fate in models of neurodegenerative disease

FEBS Letters

Volumn 587, Issue 8, 2013, Pages 1139-1146

  Skibinski, Gaia ^a,b   Finkbeiner, Steven ^a,b,c,d,e  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b Hellman Family Foundation Program in Alzheimer's Disease Research   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Depts of Neurology and Neurosurgery   (United States)

^e Department of Molecular Biochemistry and Biophysics W M Keck Foundation Yale School of Medicine   (United States)

Author keywords

Longitudinal; Primary neuron; Proteostasis; Survival

Indexed keywords

ADAPTATION; AUTOMATED ROBOTIC MICROSCOPE; CELL DEATH; DEGENERATIVE DISEASE; DISEASE MODEL; FLUORESCENCE MICROSCOPY; HUMAN; LONGITUDINAL SURVIVAL ANALYSIS; MICROSCOPE; NERVE CELL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; REVIEW; STATISTICAL ANALYSIS; SURVIVAL;

ADAPTATION, PHYSIOLOGICAL; CELL SURVIVAL; HOMEOSTASIS; HUMANS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; NEURONS; PROTEIN FOLDING; PROTEINS; PROTEOSTASIS DEFICIENCIES;

EID: 84876058100     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.02.043     Document Type: Review

References (122)

1. W.E. Balch Adapting proteostasis for disease intervention Science 319 5865 2008 916 919
2. P.M. Douglas, and A. Dillin Protein homeostasis and aging in neurodegeneration J. Cell Biol. 190 5 2010 719 729
3. R.W. Carrell, and D.A. Lomas Conformational disease Lancet 350 9071 1997 134 138
4. R.R. Kopito Aggresomes, inclusion bodies and protein aggregation Trends Cell Biol. 10 12 2000 524 530
5. C.G. Glabe Common mechanisms of amyloid oligomer pathogenesis in degenerative disease Neurobiol. Aging 27 4 2006 570 575
6. A. del Sol Diseases as network perturbations Curr. Opin. Biotechnol. 21 4 2010 566 571
7. M. Arrasate, and S. Finkbeiner Automated microscope system for determining factors that predict neuronal fate Proc. Natl. Acad. Sci. USA 102 10 2005 3840 3845
8. K. Lou, and M. de Rond The 'not invented here' myth Nat. Rev. Drug Discovery 5 6 2006 451 452
9. A.K. Gardino Transient non-native hydrogen bonds promote activation of a signaling protein Cell 139 6 2009 1109 1118
10. D.A. Drummond, and C.O. Wilke Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution Cell 134 2 2008 341 352
11. K.A. Dill, K. Ghosh, and J.D. Schmit Physical limits of cells and proteomes Proc. Natl. Acad. Sci. USA 108 44 2011 17876 17882
12. T. Gidalevitz Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity PLoS Genet. 5 3 2009 e1000399
13. K. Ghosh, and K. Dill Cellular proteomes have broad distributions of protein stability Biophys. J. 99 12 2010 3996 4002
14. H.A. Scheraga, M. Khalili, and A. Liwo Protein-folding dynamics: overview of molecular simulation techniques Annu. Rev. Phys. Chem. 58 2007 57 83
15. A.I. Bartlett, and S.E. Radford An expanding arsenal of experimental methods yields an explosion of insights into protein folding mechanisms Nat. Struct. Mol. Biol. 16 6 2009 582 588
16. D.J. Brockwell, and S.E. Radford Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17 1 2007 30 37
17. J.D. Bryngelson Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins 21 3 1995 167 195
18. J.N. Onuchic, and P.G. Wolynes Theory of protein folding Curr. Opin. Struct. Biol. 14 1 2004 70 75
19. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
20. S. Raychaudhuri The role of intrinsically unstructured proteins in neurodegenerative diseases PLoS One 4 5 2009 e5566
21. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 10 2001 597 604
22. F.U. Hartl Molecular chaperones in cellular protein folding Nature 381 6583 1996 571 579
23. R. Engel Macromolecular crowding compacts unfolded apoflavodoxin and causes severe aggregation of the off-pathway intermediate during apoflavodoxin folding J. Biol. Chem. 283 41 2008 27383 27394
24. L.M. Charlton Residue-level interrogation of macromolecular crowding effects on protein stability J. Am. Chem. Soc. 130 21 2008 6826 6830
25. D. Homouz Crowded, cell-like environment induces shape changes in aspherical protein Proc. Natl. Acad. Sci. USA 105 33 2008 11754 11759
26. D.C. Walker, and J. Southgate The virtual cell-a candidate co-ordinator for 'middle-out' modelling of biological systems Brief. Bioinf. 10 4 2009 450 461
27. Y.M. Ramdzan Conformation sensors that distinguish monomeric proteins from oligomers in live cells Chem. Biol. 17 4 2010 371 379
28. R. Gupta Firefly luciferase mutants as sensors of proteome stress Nat. Methods 8 10 2011 879 884
29. A.L. Hsu, C.T. Murphy, and C. Kenyon Regulation of aging and age-related disease by DAF-16 and heat-shock factor Science 300 5622 2003 1142 1145
30. S. Wickner, M.R. Maurizi, and S. Gottesman Posttranslational quality control: folding, refolding, and degrading proteins Science 286 5446 1999 1888 1893
31. J. Klucken Hsp70 reduces alpha-synuclein aggregation and toxicity J. Biol. Chem. 279 24 2004 25497 25502
32. A.S. Tsvetkov A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model Proc. Natl. Acad. Sci. USA 107 39 2010 16982 16987
33. I.F. Wang, K.J. Tsai, and C.K. Shen Autophagy activation ameliorates neuronal pathogenesis of FTLD-U mice: a new light for treatment of TARDBP/TDP-43 proteinopathies Autophagy 9 2 2013 239 240
34. D.J. Gifondorwa Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis J. Neurosci. 27 48 2007 13173 13180
35. C.G. Glabe, and R. Kayed Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis Neurology 66 2 Suppl 1 2006 S74 S78
36. S. Finkbeiner Disease-modifying pathways in neurodegeneration J. Neurosci. 26 41 2006 10349 10357
37. D.M. Fowler Functional amyloid formation within mammalian tissue PLoS Biol. 4 1 2006 e6
38. T. Cohen Inhibition of amyloid fibril formation and cytotoxicity by hydroxyindole derivatives Biochemistry 45 15 2006 4727 4735
39. C. Behrends Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers Mol. Cell 23 6 2006 887 897
40. P.M. Douglas Chaperone-dependent amyloid assembly protects cells from prion toxicity Proc. Natl. Acad. Sci. USA 105 20 2008 7206 7211
41. R.A. Bodner Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases Proc. Natl. Acad. Sci. USA 103 11 2006 4246 4251
42. P.T. Kotzbauer Pathologic accumulation of alpha-synuclein and abeta in Parkinson disease patients with dementia Arch. Neurol. 2012 1 6
43. J.J. Hoozemans The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus Am. J. Pathol. 174 4 2009 1241 1251
44. J.J. Hoozemans Activation of the unfolded protein response in Parkinson's disease Biochem. Biophys. Res. Commun. 354 3 2007 707 711
45. S.C. Hand, and I. Hardewig Downregulation of cellular metabolism during environmental stress: mechanisms and implications Annu. Rev. Physiol. 58 1996 539 563
46. V. Albanese Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells Cell 124 1 2006 75 88
47. H.P. Harding Regulated translation initiation controls stress-induced gene expression in mammalian cells Mol. Cell 6 5 2000 1099 1108
48. J.A. Moreno Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration Nature 485 7399 2012 507 511
49. E.M. Ozbudak Regulation of noise in the expression of a single gene Nat. Genet. 31 1 2002 69 73
50. M.B. Elowitz Stochastic gene expression in a single cell Science 297 5584 2002 1183 1186
51. A. Bar-Even Noise in protein expression scales with natural protein abundance Nat. Genet. 38 6 2006 636 643
52. A. Raj Stochastic mRNA synthesis in mammalian cells PLoS Biol. 4 10 2006 e309
53. N. Friedman, L. Cai, and X.S. Xie Linking stochastic dynamics to population distribution: an analytical framework of gene expression Phys. Rev. Lett. 97 16 2006 168302
54. J.M. Raser, and E.K. O'Shea Control of stochasticity in eukaryotic gene expression Science 304 5678 2004 1811 1814
55. M.L. Kilfoil, P. Lasko, and E. Abouheif Stochastic variation: from single cells to superorganisms HFSP J. 3 6 2009 379 385
56. W.J. Blake Noise in eukaryotic gene expression Nature 422 6932 2003 633 637
57. A. Colman-Lerner Regulated cell-to-cell variation in a cell-fate decision system Nature 437 7059 2005 699 706
58. R. Bahar Increased cell-to-cell variation in gene expression in ageing mouse heart Nature 441 7096 2006 1011 1014
59. R.I. Morimoto The heat shock response: systems biology of proteotoxic stress in aging and disease Cold Spring Harb. Symp. Quant. Biol. 76 2011 91 99
60. A.S. Tsvetkov, S. Mitra, and S. Finkbeiner Protein turnover differences between neurons and other cells Autophagy 5 2009 5
61. C.J. Marcuccilli Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock J. Neurosci. 16 2 1996 478 485
62. S.K. Mathur Deficient induction of human hsp70 heat shock gene transcription in Y79 retinoblastoma cells despite activation of heat shock factor 1 Proc. Natl. Acad. Sci. USA 91 18 1994 8695 8699
63. T.V. Strong Widespread expression of the human and rat Huntington's disease gene in brain and nonneural tissues Nat. Genet. 5 3 1993 259 265
64. S. Sharma LRRK2 expression in idiopathic and G2019S positive Parkinson's disease subjects: a morphological and quantitative study Neuropathol. Appl. Neurobiol. 37 7 2011 777 790
65. I.J. Cajigas, T. Will, and E.M. Schuman Protein homeostasis and synaptic plasticity EMBO J. 29 16 2010 2746 2752
66. V. Prahlad, T. Cornelius, and R.I. Morimoto Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons Science 320 5877 2008 811 814
67. V. Prahlad, and R.I. Morimoto Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins Proc. Natl. Acad. Sci. USA 108 34 2011 14204 14209
68. S.M. Garcia Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells Genes Dev. 21 22 2007 3006 3016
69. A. Ben-Zvi, E.A. Miller, and R.I. Morimoto Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging Proc. Natl. Acad. Sci. USA 106 35 2009 14914 14919
70. J.F. Morley The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 99 16 2002 10417 10422
71. J.V. Hindle Ageing, neurodegeneration and Parkinson's disease Age Ageing 39 2 2010 156 161
72. L. Hood, and R.M. Perlmutter The impact of systems approaches on biological problems in drug discovery Nat. Biotechnol. 22 10 2004 1215 1217
73. L. Hood Systems biology and new technologies enable predictive and preventative medicine Science 306 5696 2004 640 643
74. P.M. Antony, R. Balling, and N. Vlassis From systems biology to systems biomedicine Curr. Opin. Biotechnol. 23 4 2012 604 608
75. Z. Spiro, I.A. Kovacs, and P. Csermely Drug-therapy networks and the prediction of novel drug targets J. Biol. 7 6 2008 20
76. D. Hwang A systems approach to prion disease Mol. Syst. Biol. 5 2009 252
77. G.I. Simko Network strategies to understand the aging process and help age-related drug design Genome Med. 1 9 2009 90
78. J. Kotz Phenotypic screeing, take two SciBx 5 15 2012 1 3
79. M. Arrasate Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431 7010 2004 805 810
80. A. Daub, P. Sharma, and S. Finkbeiner High-content screening of primary neurons: ready for prime time Curr. Opin. Neurobiol. 19 5 2009 537 543
81. P. Sharma High-throughput screening in primary neurons Methods Enzymol. 506 2012 331 360
82. C. Pan Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions Mol. Cell. Proteomics 8 3 2009 443 450
83. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 4 2006 663 676
84. K. Okita, T. Ichisaka, and S. Yamanaka Generation of germline-competent induced pluripotent stem cells Nature 448 7151 2007 313 317
85. A. Swistowski Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions Stem Cells 28 10 2010 1893 1904
86. F. Soldner Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors Cell 136 5 2009 964 977
87. M. Wernig Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease Proc. Natl. Acad. Sci. USA 105 15 2008 5856 5861
88. B. Bilican Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability Proc. Natl. Acad. Sci. USA 109 15 2012 5803 5808
89. A. Sanchez-Danes Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease EMBO Mol. Med 4 5 2012 380 395
90. The Hd Ipsc C Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes Cell Stem Cell 11 2 2012 264 278
91. H.N. Nguyen LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress Cell Stem Cell 8 3 2011 267 280
92. T.L. Spires-Jones Monitoring protein aggregation and toxicity in Alzheimer's disease mouse models using in vivo imaging Methods 53 3 2011 201 207
93. V.K. Unni Studying protein degradation pathways in vivo using a cranial window-based approach Methods 53 3 2011 194 200
94. V.K. Unni In vivo imaging of alpha-synuclein in mouse cortex demonstrates stable expression and differential subcellular compartment mobility PLoS One 5 5 2010 e10589
95. E. Pastrana A handle on neurodegenerative disease complexity Nat. Methods 9 1 2012 21
96. F. Sambataro, and M. Pennuto Cell-autonomous and non-cell-autonomous toxicity in polyglutamine diseases Prog. Neurobiol. 97 2 2012 152 172
97. C. Cunningham Microglia and neurodegeneration: the role of systemic inflammation Glia 61 1 2013 71 90
98. P. Brundin, R. Melki, and R. Kopito Prion-like transmission of protein aggregates in neurodegenerative diseases Nat. Rev. Mol. Cell Biol. 11 4 2010 301 307
99. Y.C. Lin, and A.J. Koleske Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders Annu. Rev. Neurosci. 33 2010 349 378
100. B. Alvarez-Castelao, C. Ruiz-Rivas, and J.G. Castano A critical appraisal of quantitative studies of protein degradation in the framework of cellular proteostasis Biochem. Res. Int. 2012 2012 823597
101. S.J. Barmada Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis J. Neurosci. 30 2 2010 639 649
102. M. Halter Automated live cell imaging of green fluorescent protein degradation in individual fibroblasts Cytometry A 71 10 2007 827 834
103. B.Y. Gueuvoghlanian-Silva Profile of inflammatory mediators in gestational diabetes mellitus: phenotype and genotype Am. J. Reprod. Immunol. 67 3 2012 241 250
104. K. Itoh Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1 1999 76 86
105. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
106. S.B. Cullinan Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival Mol. Cell. Biol. 23 20 2003 7198 7209
107. B.N. Giepmans The fluorescent toolbox for assessing protein location and function Science 312 5771 2006 217 224
108. P.C. van Dijk The analysis of survival data in nephrology: basic concepts and methods of Cox regression Kidney Int. 74 6 2008 705 709
109. K.J. Jager The analysis of survival data: the Kaplan-Meier method Kidney Int. 74 5 2008 560 565
110. K. Nakamura Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein J. Biol. Chem. 286 23 2011 20710 20726
111. M.W. Becher Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length Neurobiol. Dis. 4 6 1998 387 397
112. S.J. Cherra 3rd, R.K. Dagda, and C.T. Chu Review: autophagy and neurodegeneration: survival at a cost? Neuropathol. Appl. Neurobiol. 36 2 2010 125 132
113. Y. Tong Loss of leucine-rich repeat kinase 2 causes age-dependent bi-phasic alterations of the autophagy pathway Mol. Neurodegener. 7 2012 2
114. F.W. Dekker Survival analysis: time-dependent effects and time-varying risk factors Kidney Int. 74 8 2008 994 997
115. H.E. Mulcahy, and D.P. O'Donoghue Duration of colorectal cancer symptoms and survival: the effect of confounding clinical and pathological variables Eur. J. Cancer 33 9 1997 1461 1467
116. J. Miller Quantitative relationships between huntingtin levels, polyglutamine length, inclusion body formation, and neuronal death provide novel insight into huntington's disease molecular pathogenesis J. Neurosci. 30 31 2010 10541 10550
117. E. Wong, and A.M. Cuervo Autophagy gone awry in neurodegenerative diseases Nat. Neurosci. 13 7 2010 805 811
118. L. Scrucca, A. Santucci, and F. Aversa Regression modeling of competing risk using R: an in depth guide for clinicians Bone Marrow Transplant. 45 9 2010 1388 1395
119. L. Scrucca, A. Santucci, and F. Aversa Competing risk analysis using R: an easy guide for clinicians Bone Marrow Transplant. 40 4 2007 381 387
120. A.M. Strasak Use of penalized splines in extended Cox-type additive hazard regression to flexibly estimate the effect of time-varying serum uric acid on risk of cancer incidence: a prospective, population-based study in 78,850 men Ann. Epidemiol. 19 1 2009 15 24
121. M.E. Glickman, and D.A. van Dyk Basic Bayesian methods Methods Mol. Biol. 404 2007 319 338
122. J. Miller Identifying polyglutamine protein species in situ that best predict neurodegeneration Nat. Chem. Biol. 7 12 2011 925 934