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Molecular dissection of amyloid disaggregation by human HSP70

  • 1.

    Wentink, A., Nussbaum-Krammer, C. & Bukau, B. Modulation of amyloid states by molecular chaperones. Cold Spring Harb. Perspect. Biol. 11, a033969 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Kampinga, H. H. & Bergink, S. Heat shock proteins as potential targets for protective strategies in neurodegeneration. Lancet Neurol. 15, 748–759 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Duennwald, M. L., Echeverria, A. & Shorter, J. Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans. PLoS Biol. 10, e1001346 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 4.

    Gao, X. et al. Human Hsp70 disaggregase reverses Parkinson’s-linked α-synuclein amyloid fibrils. Mol. Cell 59, 781–793 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 5.

    Rosenzweig, R., Nillegoda, N. B., Mayer, M. P. & Bukau, B. The Hsp70 chaperone network. Nat. Rev. Mol. Cell Biol. 20, 665–680 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 6.

    Mayer, M. P. & Gierasch, L. M. Recent advances in the structural and mechanistic aspects of Hsp70 molecular chaperones. J. Biol. Chem. 294, 2085–2097 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 7.

    Bracher, A. & Verghese, J. The nucleotide exchange factors of Hsp70 molecular chaperones. Front. Mol. Biosci. 2, 10 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 8.

    Nachman, E. et al. Disassembly of Tau fibrils by the human Hsp70 disaggregation machinery generates small seeding-competent species. J. Biol. Chem. 295, 9676–9690 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 9.

    Scior, A. et al. Complete suppression of Htt fibrilization and disaggregation of Htt fibrils by a trimeric chaperone complex. EMBO J. 37, 282–299 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 10.

    Burmann, B. M. et al. Regulation of α-synuclein by chaperones in mammalian cells. Nature 577, 127–132 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 11.

    Redeker, V., Pemberton, S., Bienvenut, W., Bousset, L. & Melki, R. Identification of protein interfaces between α-synuclein, the principal component of Lewy bodies in Parkinson disease, and the molecular chaperones human Hsc70 and the yeast Ssa1p. J. Biol. Chem. 287, 32630–32639 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 12.

    Uéda, K. et al. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA 90, 11282–11286 (1993).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 13.

    Guerrero-Ferreira, R., Kovacik, L., Ni, D. & Stahlberg, H. New insights on the structure of alpha-synuclein fibrils using cryo-electron microscopy. Curr. Opin. Neurobiol. 61, 89–95 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Vilar, M. et al. The fold of alpha-synuclein fibrils. Proc. Natl Acad. Sci. USA 105, 8637–8642 (2008).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 15.

    Sha, B., Lee, S. & Cyr, D. M. The crystal structure of the peptide-binding fragment from the yeast Hsp40 protein Sis1. Structure 8, 799–807 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 16.

    Jiang, Y., Rossi, P. & Kalodimos, C. G. Structural basis for client recognition and activity of Hsp40 chaperones. Science 365, 1313–1319 (2019).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    De Los Rios, P. & Barducci, A. Hsp70 chaperones are non-equilibrium machines that achieve ultra-affinity by energy consumption. eLife 3, e02218 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 18.

    Lu, Z. & Cyr, D. M. Protein folding activity of Hsp70 is modified differentially by the Hsp40 co-chaperones Sis1 and Ydj1. J. Biol. Chem. 273, 27824–27830 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 19.

    De Los Rios, P., Ben-Zvi, A., Slutsky, O., Azem, A. & Goloubinoff, P. Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling. Proc. Natl Acad. Sci. USA 103, 6166–6171 (2006).

    ADS  PubMed  Article  CAS  Google Scholar 

  • 20.

    Goloubinoff, P. & De Los Rios, P. The mechanism of Hsp70 chaperones: (entropic) pulling the models together. Trends Biochem. Sci. 32, 372–380 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 21.

    Sousa, R. & Lafer, E. M. The physics of entropic pulling: a novel model for the Hsp70 motor mechanism. Int. J. Mol. Sci. 20, E2334 (2019).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 22.

    Sousa, R. et al. Clathrin-coat disassembly illuminates the mechanisms of Hsp70 force generation. Nat. Struct. Mol. Biol. 23, 821–829 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 23.

    Rampelt, H. et al. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J. 31, 4221–4235 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 24.

    Easton, D. P., Kaneko, Y. & Subjeck, J. R. The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5, 276–290 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Faust, A. O. et al. HSP40s use class-specific regulation to drive HSP70 functional diversity. Nature https://doi.org/10.1038/s41586-020-2906-4 (2020).

  • 26.

    Assenza, S. et al. Efficient conversion of chemical energy into mechanical work by Hsp70 chaperones. eLife 8, e48491 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 27.

    Imamoglu, R., Balchin, D., Hayer-Hartl, M. & Hartl, F. U. Bacterial Hsp70 resolves misfolded states and accelerates productive folding of a multi-domain protein. Nat. Commun. 11, 365 (2020).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Kellner, R. et al. Single-molecule spectroscopy reveals chaperone-mediated expansion of substrate protein. Proc. Natl Acad. Sci. USA 111, 13355–13360 (2014).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 29.

    Sharma, S. K., De los Rios, P., Christen, P., Lustig, A. & Goloubinoff, P. The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat. Chem. Biol. 6, 914–920 (2010).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 30.

    Kmiecik, S. W., Le Breton, L. & Mayer, M. P. Feedback regulation of heat shock factor 1 (Hsf1) activity by Hsp70-mediated trimer unzipping and dissociation from DNA. EMBO J. 39, e104096 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Pieri, L., Madiona, K., Bousset, L. & Melki, R. Fibrillar α-synuclein and huntingtin exon 1 assemblies are toxic to the cells. Biophys. J. 102, 2894–2905 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 32.

    Taguchi, Y. V. et al. Hsp110 mitigates α-synuclein pathology in vivo. Proc. Natl Acad. Sci. USA 116, 24310–24316 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Tittelmeier, J. et al. The HSP110/HSP70 disaggregation system generates spreading-competent toxic α-synuclein species. EMBO J. 39, e103954 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Nillegoda, N. B. et al. Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation. Nature 524, 247–251 (2015).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 35.

    Paleologou, K. E. et al. Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of alpha-synuclein. J. Biol. Chem. 283, 16895–16905 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    Hoyer, W. et al. Dependence of α-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322, 383–393 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277–293 (1995).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 38.

    Lee, W., Tonelli, M. & Markley, J. L. NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy. Bioinformatics 31, 1325–1327 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 39.

    Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 46, W296–W303 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Bertelsen, E. B., Chang, L., Gestwicki, J. E. & Zuiderweg, E. R. Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl Acad. Sci. USA 106, 8471–8476 (2009).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 41.

    Liu, Q. & Hendrickson, W. A. Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131, 106–120 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Tuttle, M. D. et al. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. Nat. Struct. Mol. Biol. 23, 409–415 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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