CoChat
Sign Up
Cited by 810

The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.

Stress granules and neurodegeneration

Wolozin, Benjamin, Ivanov, Pavel·2019·Nature Reviews Neuroscience
DOI 10.1038/s41583-019-0222-5PMC PMC6986315
Open this paper in CoChat — free account

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41583-019-0222-5

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 165

  1. Nott, T. J. et al. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 57, 936–947 (2015). · DOI · Paper page
  2. Boeynaems, S. et al. Protein phase separation: a new phase in cell biology. Trends Cell Biol. 28, 420–435 (2018). · DOI
  3. Taylor, J. P., Brown, R. H., Jr. & Cleveland, D. W. Decoding ALS: from genes to mechanism. Nature 539, 197–206 (2016). · DOI
  4. Irwin, D. J. et al. Frontotemporal lobar degeneration: defining phenotypic diversity through personalized medicine. Acta Neuropathol. 129, 469–491 (2015). · DOI
  5. Kim, H. J. et al. Therapeutic modulation of eIF2α phosphorylation rescues TDP-43 toxicity in amyotrophic lateral sclerosis disease models. Nat. Genet. 46, 152–160 (2014). · DOI
  6. Radford, H., Moreno, J. A., Verity, N., Halliday, M. & Mallucci, G. R. PERK inhibition prevents tau-mediated neurodegeneration in a mouse model of frontotemporal dementia. Acta Neuropathol. 130, 633–642 (2015). · DOI
  7. Chia, R., Chio, A. & Traynor, B. J. Novel genes associated with amyotrophic lateral sclerosis: diagnostic and clinical implications. Lancet Neurol. 17, 94–102 (2018). · DOI
  8. Jin, M. et al. Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl Acad. Sci. USA 108, 5819–5824 (2011). · DOI · Paper page
  9. Bang, J., Spina, S. & Miller, B. L. Frontotemporal dementia. Lancet 386, 1672–1682 (2015). · DOI · Paper page
  10. Lin, Y., Protter, D. S., Rosen, M. K. & Parker, R. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol. Cell 60, 208–219 (2015). · DOI
  11. Liu-Yesucevitz, L. et al. Local RNA translation at the synapse and in disease. J. Neurosci. 31, 16086–16093 (2011). · DOI
  12. Parker, R. & Sheth, U. P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635–646 (2007). · DOI · Paper page
  13. Mao, Y. S., Zhang, B. & Spector, D. L. Biogenesis and function of nuclear bodies. Trends Genet. 27, 295–306 (2011). · DOI
  14. Shpargel, K. B. & Matera, A. G. Gemin proteins are required for efficient assembly of Sm-class ribonucleoproteins. Proc. Natl Acad. Sci. USA 102, 17372–17377 (2005). · DOI
  15. Zhang, H. et al. Multiprotein complexes of the survival of motor neuron protein SMN with Gemins traffic to neuronal processes and growth cones of motor neurons. J. Neurosci. 26, 8622–8632 (2006). · DOI
  16. Jain, A. & Vale, R. D. RNA phase transitions in repeat expansion disorders. Nature 546, 243–247 (2017). · DOI
  17. Fay, M. M., Anderson, P. J. & Ivanov, P. ALS/FTD-associated C9ORF72 repeat RNA promotes phase transitions in vitro and in cells. Cell Rep. 21, 3573–3584 (2017). · DOI
  18. Van Treeck, B. et al. RNA self-assembly contributes to stress granule formation and defining the stress granule transcriptome. Proc. Natl Acad. Sci. USA 115, 2734–2739 (2018). · DOI
  19. Maharana, S. et al. RNA buffers the phase separation behavior of prion-like RNA binding proteins. Science 360, 918–921 (2018). This study elegantly shows the important role that RNA plays in regulating the phase separation dynamics of membraneless organelles. · DOI
  20. Guo, L. et al. Nuclear-import receptors reverse aberrant phase transitions of RNA-binding proteins with prion-like domains. Cell 173, 677–692.e620 (2018). This paper demonstrates that nuclear import receptors can act as disaggregates, thereby providing a novel mechanism for regulating SGs and identifying a functional link between the nuclear transport machinery and disease pathology. · DOI
  21. Hofweber, M. et al. Phase separation of FUS is suppressed by its nuclear import receptor and arginine methylation. Cell 173, 706–719.e713 (2018). · DOI
  22. Qamar, S. et al. FUS phase separation is modulated by a molecular chaperone and methylation of arginine cation–pi interactions. Cell 173, 720–734.e715 (2018). · DOI
  23. Liu-Yesucevitz, L. et al. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLOS ONE 5, e13250 (2010). This report shows that TDP43 associates with SGs and also provides immunohistochemical evidence that TDP43 pathology associates with SG markers in ALS brain tissue. · DOI
  24. Gupta, N. et al. Stress granule-associated protein G3BP2 regulates breast tumor initiation. Proc. Natl Acad. Sci. USA 114, 1033–1038 (2017). · DOI
  25. Valentin-Vega, Y. A. et al. Cancer-associated DDX3X mutations drive stress granule assembly and impair global translation. Sci. Rep. 6, 25996 (2016).
  26. Anderson, P., Kedersha, N. & Ivanov, P. Stress granules, P-bodies and cancer. Biochim. Biophys. Acta 1849, 861–870 (2015). · DOI
  27. Kedersha, N. et al. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257–1268 (2000). · DOI
  28. Kedersha, N. L., Gupta, M., Li, W., Miller, I. & Anderson, P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2α to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431–1442 (1999). · DOI
  29. Anderson, P. & Kedersha, N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141–150 (2008). · DOI
  30. Kedersha, N. et al. Evidence that ternary complex (eIF2–GTP–tRNAi Met)-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13, 195–210 (2002). · DOI
  31. Markmiller, S. et al. Context-dependent and disease-specific diversity in protein interactions within stress granules. Cell 172, 590–604.e513 (2018). This paper provides a comprehensive characterization of SG proteomes in cells and also highlights the compositional differences among different types of SGs. · DOI
  32. Lastres-Becker, I. et al. Mammalian ataxin-2 modulates translation control at the pre-initiation complex via PI3K/mTOR and is induced by starvation. Biochim. Biophys. Acta 1862, 1558–1569 (2016). · DOI
  33. Kedersha, N. et al. G3BP–caprin1–USP10 complexes mediate stress granule condensation and associate with 40S subunits. J. Cell Biol. 212, 845–860 (2016). · DOI
  34. Ohn, T., Kedersha, N., Hickman, T., Tisdale, S. & Anderson, P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10, 1224–1231 (2008). · DOI
  35. Jain, S. et al. ATPase-modulated stress granules contain a diverse proteome and substructure. Cell 164, 487–498 (2016). · DOI
  36. Wheeler, J. R., Jain, S., Khong, A. & Parker, R. Isolation of yeast and mammalian stress granule cores. Methods 126, 12–17 (2017). · DOI
  37. Wheeler, J. R., Matheny, T., Jain, S., Abrisch, R. & Parker, R. Distinct stages in stress granule assembly and disassembly. eLife 5, e18413 (2016).
  38. Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C. & Bassell, G. J. Metabotropic glutamate receptor activation regulates fragile X mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 24, 2648–2655 (2004). · DOI · Paper page
  39. Jackson, R. J., Hellen, C. U. & Pestova, T. V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113–127 (2010). This review provides an outstanding and detailed overview of the machinery carrying out translational initiation and the pathways of translational regulation. · DOI · Paper page
  40. Fujimura, K., Sasaki, A. T. & Anderson, P. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of non-canonical stress granules. Nucleic Acids Res. 40, 8099–8110 (2012). · DOI
  41. Emara, M. M. et al. Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem. Biophys. Res. Commun. 423, 763–769 (2012). · DOI
  42. Szaflarski, W. et al. Vinca alkaloid drugs promote stress-induced translational repression and stress granule formation. Oncotarget 7, 30307–30322 (2016). · DOI
  43. Frydryskova, K. et al. Distinct recruitment of human eIF4E isoforms to processing bodies and stress granules. BMC Mol. Biol. 17, 21 (2016). · DOI
  44. Wek, R. C. Role of eif2α kinases in translational control and adaptation to cellular stress. Cold Spring Harb. Perspect. Biol. 10, a032870 (2018). · DOI
  45. Wek, S. A., Zhu, S. & Wek, R. C. The histidyl-tRNA synthetase-related sequence in the eIF-2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell Biol. 15, 4497–4506 (1995). · DOI
  46. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. & Ron, D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897–904 (2000). · DOI · Paper page
  47. Srivastava, S. P., Kumar, K. U. & Kaufman, R. J. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273, 2416–2423 (1998). · DOI · Paper page
  48. McEwen, E. et al. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J. Biol. Chem. 280, 16925–16933 (2005). · DOI
  49. Sudhakar, A. et al. Phosphorylation of serine 51 in initiation factor 2α (eIF2α) promotes complex formation between eIF2α(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39, 12929–12938 (2000). · DOI
  50. Kedersha, N. & Anderson, P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963–969 (2002). · DOI
  51. Li, Y. et al. Immunoprecipitation and mass spectrometry defines an extensive RBM45 protein-protein interaction network. Brain Res. 1647, 79–93 (2016). · DOI
  52. Umoh, M. E. et al. A proteomic network approach across the ALS–FTD disease spectrum resolves clinical phenotypes and genetic vulnerability in human brain. EMBO Mol. Med. 10, 48–62 (2018). · DOI
  53. Gunawardana, C. G. et al. The human tau interactome: binding to the ribonucleoproteome, and impaired binding of the proline-to-leucine mutant at position 301 (p301l) to chaperones and the proteasome. Mol. Cell Proteom. 14, 3000–3014 (2015). · DOI
  54. Dhungel, N. et al. Parkinson’s disease genes VPS35 and EIF4G1 interact genetically and converge on α-synuclein. Neuron 85, 76–87 (2015). · DOI
  55. Nichols, N. et al. EIF4G1 mutations do not cause Parkinson’s disease. Neurobiol. Aging 36, 2444.e1–4 (2015). · DOI
  56. Kim, W. J., Kim, J. H. & Jang, S. K. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO J. 26, 5020–5032 (2007). · DOI
  57. Bordeleau, M. E. et al. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat. Chem. Biol. 2, 213–220 (2006). · DOI
  58. Ivanov, P., Emara, M. M., Villen, J., Gygi, S. P. & Anderson, P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 43, 613–623 (2011). · DOI
  59. Lyons, S. M., Achorn, C., Kedersha, N. L., Anderson, P. J. & Ivanov, P. YB-1 regulates tiRNA-induced stress granule formation but not translational repression. Nucleic Acids Res. 44, 6949–6960 (2016). · DOI
  60. Armstrong, R. A., Carter, D. & Cairns, N. J. A quantitative study of the neuropathology of 32 sporadic and familial cases of frontotemporal lobar degeneration with TDP-43 proteinopathy (FTLD–TDP). Neuropathol. Appl. Neurobiol. 38, 25–38 (2012). · DOI
  61. Janssens, J. et al. Overexpression of ALS-associated p.M337V human TDP-43 in mice worsens disease features compared to wild-type human TDP-43 mice. Mol. Neurobiol. 48, 22–35 (2013). · DOI
  62. Figley, M. D., Bieri, G., Kolaitis, R. M., Taylor, J. P. & Gitler, A. D. Profilin 1 associates with stress granules and als-linked mutations alter stress granule dynamics. J. Neurosci. 34, 8083–8097 (2014). · DOI
  63. Gilks, N. et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15, 5383–5398 (2004). · DOI
  64. Bounedjah, O. et al. Free mRNA in excess upon polysome dissociation is a scaffold for protein multimerization to form stress granules. Nucleic Acids Res. 42, 8678–8691 (2014). · DOI
  65. Bley, N. et al. Stress granules are dispensable for mRNA stabilization during cellular stress. Nucleic Acids Res. 43, e26 (2015). · DOI
  66. Vogler, T. O. et al. TDP-43 and RNA form amyloid-like myo-granules in regenerating muscle. Nature 563, 508–513 (2018). · DOI
  67. Lefebvre, S. et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80, 155–165 (1995). · DOI
  68. Bassell, G. J. & Warren, S. T. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60, 201–214 (2008). · DOI · Paper page
  69. Kenneson, A., Zhang, F., Hagedorn, C. H. & Warren, S. T. Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers. Hum. Mol. Genet. 10, 1449–1454 (2001). · DOI
  70. Hagerman, P. J. & Hagerman, R. J. Fragile X-associated tremor/ataxia syndrome (FXTAS). Ment. Retard. Dev. Disabil. Res. Rev. 10, 25–30 (2004). · DOI
  71. Neumann, M. et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130–133 (2006). · DOI · Paper page
  72. Vance, C. et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208–1211 (2009). · DOI
  73. Van Deerlin, V. M. et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol. 7, 409–416 (2008). · DOI · Paper page
  74. Mackenzie, I. R. et al. TIA1 mutations in amyotrophic lateral sclerosis and frontotemporal dementia promote phase separation and alter stress granule dynamics. Neuron 95, 808–816 e809 (2017). · DOI
  75. Kim, H. J. et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495, 467–473 (2013). · DOI
  76. Kwiatkowski, T. J., Jr. et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205–1208 (2009). · DOI
  77. Elden, A. C. et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 466, 1069–1075 (2010). · DOI
  78. Emara, M. M. et al. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J. Biol. Chem. 285, 10959–10968 (2010). · DOI · Paper page
  79. Greenway, M. J. et al. ANG mutations segregate with familial and ‘sporadic’ amyotrophic lateral sclerosis. Nat. Genet. 38, 411–413 (2006). · DOI
  80. Dormann, D. & Haass, C. TDP-43 and FUS: a nuclear affair. Trends Neurosci. 34, 339–348 (2011). · DOI
  81. Bosco, D. A. et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet. 19, 4160–4175 (2011). · DOI
  82. Phillips, K., Kedersha, N., Shen, L., Blackshear, P. J. & Anderson, P. Arthritis suppressor genes TIA-1 and TTP dampen the expression of tumor necrosis factor α, cyclooxygenase 2, and inflammatory arthritis. Proc. Natl Acad. Sci. USA 101, 2011–2016 (2004). · DOI
  83. Garaigorta, U., Heim, M. H., Boyd, B., Wieland, S. & Chisari, F. V. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J. Virol. 86, 11043–11056 (2012). · DOI
  84. Wolozin, B. Regulated protein aggregation: stress granules and neurodegeneration. Mol. Neurodegener. 7, 56 (2012). · DOI
  85. Scheltens, P. et al. Alzheimer’s disease. Lancet 388, 505–517 (2016). · DOI · Paper page
  86. Banani, S. F. et al. Compositional control of phase-separated cellular bodies. Cell 166, 651–663 (2016). This article outlines the different cellular factors controlling the formation of membraneless organelles, such as stress granules and P-bodies. · DOI
  87. Lee, Y. et al. TIA1 variant drives myodegeneration in multisystem proteinopathy with SQSTM1 mutations. J. Clin. Invest. 128, 1164–1177 (2018). · DOI
  88. Patel, A. et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 162, 1066–1077 (2015). · DOI
  89. Molliex, A. et al. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163, 123–133 (2015). · DOI
  90. Hughes, M. P. et al. Atomic structures of low-complexity protein segments reveal kinked beta sheets that assemble networks. Science 359, 698–701 (2018). This study shows how different types of amino acid interactions, such as π–π and π–cation binding, control the formation of membraneless organelles and insoluble amyloids. · DOI
  91. Ash, P. E. A. et al. Heavy metal neurotoxicants induce ALS-linked TDP-43 pathology. Toxicol. Sci. 167, 105–115, https://doi.org/10.1093/toxsci/kfy267 (2019). · DOI
  92. Vanderweyde, T. et al. Interaction of tau with the RNA-binding protein TIA1 regulates tau pathophysiology and toxicity. Cell Rep. 15, 1–12 (2016). · DOI
  93. Vanderweyde, T. et al. Contrasting pathology of stress granule proteins TIA-1 and G3BP in tauopathies. J. Neurosci. 32, 8270–8283 (2012). This article demonstrates how tau and TIA1 interact to regulate SG biology and demonstrates that reducing TIA1 inhibits tau-mediated neurodegeneration in cultured neurons. · DOI
  94. Zhang, Y. J. et al. Poly(GR) impairs protein translation and stress granule dynamics in C9orf72-associated frontotemporal dementia and amyotrophic lateral sclerosis. Nat. Med. 24, 1136–1142 (2018). · DOI
  95. Ash, P. E. et al. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 77, 639–646 (2013). · DOI
  96. Green, K. M. et al. RAN translation at C9orf72-associated repeat expansions is selectively enhanced by the integrated stress response. Nat. Commun. 8, 2005 (2017).
  97. Boeynaems, S. et al. Phase separation of c9orf72 dipeptide repeats perturbs stress granule dynamics. Mol. Cell 65, 1044–1055.e1045 (2017). · DOI
  98. Lee, K. H. et al. C9orf72 dipeptide repeats impair the assembly, dynamics, and function of membrane-less organelles. Cell 167, 774–788.e717 (2016). This study shows how an extended dipeptide repeat can disrupt SG biology. · DOI
  99. Gasset-Rosa, F. et al. Cytoplasmic TDP-43 de-mixing independent of stress granules drives inhibition of nuclear import, loss of nuclear TDP-43, and cell death. Neuron 102, 339–357.e7 (2019). This article demonstrates that, in cells, TDP43 aggregates pass through a SG phase transiently before evolving into pathological aggregates. · DOI
  100. Mann, J. R. et al. RNA binding antagonizes neurotoxic phase transitions of TDP-43. Neuron 102, 321–338.e8 (2019). · DOI
  101. McGurk, L. et al. Poly(ADP–ribose) prevents pathological phase separation of TDP-43 by promoting liquid demixing and stress granule localization. Mol. Cell 71, 703–717 e709 (2018). · DOI
  102. Brettschneider, J. et al. TDP-43 pathology and neuronal loss in amyotrophic lateral sclerosis spinal cord. Acta Neuropathol. 128, 423–437 (2014). · DOI
  103. Zhang, K. et al. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 525, 56–61 (2015). · DOI · Paper page
  104. Chou, C. C. et al. TDP-43 pathology disrupts nuclear pore complexes and nucleocytoplasmic transport in ALS/FTD. Nat. Neurosci. 21, 228–239 (2018). · DOI
  105. Afroz, T. et al. Functional and dynamic polymerization of the ALS-linked protein TDP-43 antagonizes its pathologic aggregation. Nat. Commun. 8, 45 (2017). · DOI
  106. Hanger, D. P., Hughes, K., Woodgett, J. R., Brion, J. P. & Anderton, B. H. Glycogen synthase kinase-3 induces Alzheimer’s disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147, 58–62 (1992). · DOI · Paper page
  107. Baumann, K., Mandelkow, E., Biernat, J., Piwnica-Worms, H. & Mandelkow, E. Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 336, 417–424 (1993). · DOI
  108. Timm, T., Marx, A., Panneerselvam, S., Mandelkow, E. & Mandelkow, E. M. Structure and regulation of MARK, a kinase involved in abnormal phosphorylation of Tau protein. BMC Neurosci. 9, S9 (2008). · DOI
  109. Trinczek, B., Biernat, J., Baumann, K., Mandelkow, E. M. & Mandelkow, E. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Biol. Cell 6, 1887–1902 (1995). · DOI · Paper page
  110. 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. 399, 344–349 (1996). · DOI · Paper page
  111. Friedhoff, P., Schneider, A., Mandelkow, E. M. & Mandelkow, E. Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution. Biochemistry 37, 10223–10230 (1998). · DOI
  112. Wilson, D. M. & Binder, L. I. Free fatty acids stimulate the polymerization of tau and amyloid beta peptides: in vitro evidence for a common effector of pathogenesis in Alzheimer’s disease. Am. J. Pathol. 150, 2181–2195 (1997).
  113. Zhang, X. et al. RNA stores tau reversibly in complex coacervates. PLOS Biol. 15, e2002183 (2017).
  114. Wegmann, S. et al. Tau protein liquid–liquid phase separation can initiate tau aggregation. EMBO J. 37, e98049 (2018). This article provides a detailed characterization of the biophysical factors controlling tau phase separation. · DOI · Paper page
  115. Wang, P. et al. Tau interactome mapping based identification of Otub1 as Tau deubiquitinase involved in accumulation of pathological Tau forms in vitro and in vivo. Acta Neuropathol. 133, 731–749 (2017). · DOI
  116. Eftekharzadeh, B. et al. Tau protein disrupts nucleocytoplasmic transport in Alzheimer’s disease. Neuron 99, 925–940 e927 (2018). · DOI · Paper page
  117. Silva, J. M. et al. Dysregulation of autophagy and stress granule-related proteins in stress-driven Tau pathology. Cell Death Differ. 171, 1411–1427 (2019). This paper demonstrates that behaviourally stressful experiences can elicit the biochemical changes associated with the translational stress response in the brain. · DOI
  118. Cairns, N. J. et al. TDP-43 in familial and sporadic frontotemporal lobar degeneration with ubiquitin inclusions. Am. J. Pathol. 171, 227–240 (2007). · DOI
  119. Moujalled, D. et al. Phosphorylation of hnRNP K by cyclin-dependent kinase 2 controls cytosolic accumulation of TDP-43. Hum. Mol. Genet. 24, 1655–1669 (2015). · DOI
  120. Jiang, L. et al. TIA1 regulates the generation and response to toxic tau oligomers. Acta Neuropathol. 137, 259–277 (2019). This article demonstrates that tau oligomers and fibrils both propagate pathology in vivo, but that only tau oligomers stimulate the accumulation of tau-associated SGs and cause neurodegeneration. · DOI
  121. Sanders, D. W. et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82, 1271–1288 (2014). · DOI · Paper page
  122. Liu, L. et al. Trans-synaptic spread of tau pathology in vivo. PLOS ONE 7, e31302 (2012).
  123. Smethurst, P. et al. In vitro prion-like behaviour of TDP-43 in ALS. Neurobiol Dis. 96, 236–247 (2016). · DOI
  124. Asai, H. et al. Depletion of microglia and inhibition of exosome synthesis halt tau propagation. Nat. Neurosci. 18, 1584–1593 (2015). · DOI · Paper page
  125. Ghosh, S. & Geahlen, R. L. Stress granules modulate SYK to cause microglial cell dysfunction in Alzheimer’s disease. EBioMedicine 2, 1785–1798 (2015). · DOI
  126. Pimenova, A. A., Raj, T. & Goate, A. M. Untangling genetic risk for Alzheimer’s disease. Biol. Psychiatry 83, 300–310 (2018). · DOI · Paper page
  127. Roberson, E. D. et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science 316, 750–754 (2007). · DOI · Paper page
  128. Vossel, K. A. et al. Tau reduction prevents Aβ-induced defects in axonal transport. Science 330, 198 (2010). · DOI · Paper page
  129. Cruts, M. et al. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442, 920–924 (2006). · DOI · Paper page
  130. Klim, J. R. et al. ALS-implicated protein TDP-43 sustains levels of STMN2, a mediator of motor neuron growth and repair. Nat. Neurosci. 22, 167–179 (2019). · DOI · Paper page
  131. Nguyen, H. P., Van Broeckhoven, C. & van der Zee, J. ALS genes in the genomic era and their implications for FTD. Trends Genet. 34, 404–423 (2018). · DOI
  132. Fecto, F. et al. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 68, 1440–1446 (2011). · DOI · Paper page
  133. Weidberg, H. & Elazar, Z. TBK1 mediates crosstalk between the innate immune response and autophagy. Sci. Signal. 4, pe39 (2011). · DOI
  134. Gilpin, K. M., Chang, L. & Monteiro, M. J. ALS-linked mutations in ubiquilin-2 or hnRNPA1 reduce interaction between ubiquilin-2 and hnRNPA1. Hum. Mol. Genet. 24, 2565–2577 (2015). · DOI
  135. Cassel, J. A. & Reitz, A. B. Ubiquilin-2 (UBQLN2) binds with high affinity to the C-terminal region of TDP-43 and modulates TDP-43 levels in H4 cells: characterization of inhibition by nucleic acids and 4-aminoquinolines. Biochim. Biophys. Acta 1834, 964–971 (2013). · DOI
  136. Buchan, J. R., Kolaitis, R. M., Taylor, J. P. & Parker, R. Eukaryotic stress granules are cleared by autophagy and CDC48/VCP function. Cell 153, 1461–1474 (2013). · DOI · Paper page
  137. Nicolas, A. et al. Genome-wide analyses identify KIF5A as a novel ALS gene. Neuron 97, 1268–1283.e1266 (2018). · DOI
  138. Wu, C. H. et al. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488, 499–503 (2012). · DOI
  139. Puls, I. et al. Mutant dynactin in motor neuron disease. Nat. Genet. 33, 455–456 (2003). · DOI
  140. Smith, B. N. et al. Exome-wide rare variant analysis identifies TUBA4A mutations associated with familial ALS. Neuron 84, 324–331 (2014). · DOI
  141. Munch, C. et al. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology 63, 724–726 (2004). · DOI
  142. Landers, J. E. et al. Reduced expression of the kinesin-associated protein 3 (KIFAP3) gene increases survival in sporadic amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 106, 9004–9009 (2009). · DOI
  143. Magnani, E. et al. Interaction of tau protein with the dynactin complex. EMBO J. 26, 4546–4554 (2007). · DOI
  144. Bemiller, S. M. et al. TREM2 deficiency exacerbates tau pathology through dysregulated kinase signaling in a mouse model of tauopathy. Mol. Neurodegener. 12, 74 (2017). · DOI · Paper page
  145. Broce, I. et al. Immune-related genetic enrichment in frontotemporal dementia: an analysis of genome-wide association studies. PLOS Med. 15, e1002487 (2018).
  146. Becker, L. A. et al. Therapeutic reduction of ataxin-2 extends lifespan and reduces pathology in TDP-43 mice. Nature 544, 367–371 (2017). This study demonstrates that therapeutic reduction of ATXN2 delays the progression of TDP43-induced neurodegeneration in vivo. · DOI · Paper page
  147. Zhang, K. et al. Stress granule assembly disrupts nucleocytoplasmic transport. Cell 173, 958–971.e917 (2018). This article demonstrates a closely linked relationship between the accumulation of SGs and disruption of nuclear pore biology. · DOI
  148. Smith, H. L. & Mallucci, G. R. The unfolded protein response: mechanisms and therapy of neurodegeneration. Brain 139, 2113–2121 (2016). · DOI
  149. Moreno, J. A. et al. Sustained translational repression by eIF2α-P mediates prion neurodegeneration. Nature 485, 507–511 (2012). This study demonstrates that reducing eIF2α phosphorylation in vivo decreases neurodegeneration mediated by prions. · DOI
  150. Ma, T. et al. Suppression of eIF2α kinases alleviates Alzheimer’s disease-related plasticity and memory deficits. Nat. Neurosci. 16, 1299–1305 (2013). · DOI
  151. Wang, I. F. et al. Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43. Proc. Natl Acad. Sci. USA 109, 15024–15029 (2012). · DOI · Paper page
  152. Martinez, F. J. et al. Protein–RNA networks regulated by normal and ALS-associated mutant HnRNPA2B1 in the nervous system. Neuron 92, 780–795 (2016). · DOI
  153. Walter, H. & Brooks, D. E. Phase separation in cytoplasm, due to macromolecular crowding, is the basis for microcompartmentation. FEBS Lett. 361, 135–139 (1995). · DOI
  154. Toombs, J. A. et al. De novo design of synthetic prion domains. Proc. Natl Acad. Sci. USA 109, 6519–6524 (2012). · DOI
  155. Prilusky, J. et al. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21, 3435–3438 (2005). · DOI
  156. Wei, M. T. et al. Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles. Nat. Chem. 9, 1118–1125 (2017). · DOI
  157. Wang, J. et al. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174, 688–699.e616 (2018). · DOI
  158. Bergeron-Sandoval, L. P., Safaee, N. & Michnick, S. W. Mechanisms and consequences of macromolecular phase separation. Cell 165, 1067–1079 (2016). · DOI
  159. Feric, M. et al. Coexisting liquid phases underlie nucleolar subcompartments. Cell 165, 1686–1697 (2016). This article elegantly demonstrates that the nucleolus exists as a phase-separated structure, as well as demonstrating many key methods used in the field. · DOI
  160. Prum, R. O., Dufresne, E. R., Quinn, T. & Waters, K. Development of colour-producing β-keratin nanostructures in avian feather barbs. J. R. Soc. Interface 6 (Suppl. 2), S253–S265 (2009).
  161. Milovanovic, D., Wu, Y., Bian, X. & De Camilli, P. A liquid phase of synapsin and lipid vesicles. Science 361, 604–607 (2018). · DOI
  162. Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340 (2012). · DOI
  163. Hnisz, D., Shrinivas, K., Young, R. A., Chakraborty, A. K. & Sharp, P. A. A phase separation model for transcriptional control. Cell 169, 13–23 (2017). · DOI · Paper page
  164. Youn, J. Y. et al. High-density proximity mapping reveals the subcellular organization of mRNA-associated granules and bodies. Mol. Cell 69, 517–532.e511 (2018). · DOI
  165. Wolozin, B. The evolution of phase-separated TDP-43 in stress. Neuron 102, 265–267 (2019). · DOI

Cited by

Sorted by citations

Metadata

Authors
Wolozin, B., & Ivanov, P.
ORCID
Venue
Nature Reviews Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2019-10-03
Volume
20
Issue
11
Pages
649-666
ISSN
  • 1471-003X
  • 1471-0048
DOI
10.1038/s41583-019-0222-5
PMC
PMC6986315
Cited by
810
References
28
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review