Coordinated Hsp110 and Hsp104 Activities Power Protein Disaggregation in Saccharomyces cerevisiae

REFERENCES

• Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324–332. https://doi.org/10.1038/nature10317.
   PubMed Web of Science ®Google Scholar
• Morimoto RI. 2008. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427–1438. https://doi.org/10.1101/gad.1657108.
   PubMed Web of Science ®Google Scholar
• Alberti S. 2012. Molecular mechanisms of spatial protein quality control. Prion 6:437–442. https://doi.org/10.4161/pri.22470.
   PubMed Web of Science ®Google Scholar
• Chen B, Retzlaff M, Roos T, Frydman J. 2011. Cellular strategies of protein quality control. Cold Spring Harb Perspect Biol 3:a004374. https://doi.org/10.1101/cshperspect.a004374.
   PubMed Web of Science ®Google Scholar
• Miller SB, Mogk A, Bukau B. 2015. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J Mol Biol 427:1564–1574. https://doi.org/10.1016/j.jmb.2015.02.006.
   PubMed Web of Science ®Google Scholar
• Doyle SM, Genest O, Wickner S. 2013. Protein rescue from aggregates by powerful molecular chaperone machines. Nat Rev Mol Cell Biol 14:617–629. https://doi.org/10.1038/nrm3660.
   PubMedGoogle Scholar
• Mogk A, Kummer E, Bukau B. 2015. Cooperation of Hsp70 and Hsp100 chaperone machines in protein disaggregation. Front Mol Biosci 2:22. https://doi.org/10.3389/fmolb.2015.00022.
   PubMedGoogle Scholar
• Mattoo RU, Sharma SK, Priya S, Finka A, Goloubinoff P. 2013. Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates. J Biol Chem 288:21399–21411. https://doi.org/10.1074/jbc.M113.479253.
   PubMed Web of Science ®Google Scholar
• Nillegoda NB, Kirstein J, Szlachcic A, Berynskyy M, Stank A, Stengel F, Arnsburg K, Gao X, Scior A, Aebersold R, Guilbride DL, Wade RC, Morimoto RI, Mayer MP, Bukau B. 2015. Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation. Nature 524:247–251. https://doi.org/10.1038/nature14884.
   PubMedGoogle Scholar
• Rampelt H, Kirstein-Miles J, Nillegoda NB, Chi K, Scholz SR, Morimoto RI, Bukau B. 2012. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J 31:4221–4235. https://doi.org/10.1038/emboj.2012.264.
   PubMed Web of Science ®Google Scholar
• Shorter J. 2011. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 6:e26319. https://doi.org/10.1371/journal.pone.0026319.
   PubMed Web of Science ®Google Scholar
• Bracher A, Verghese J. 2015. The nucleotide exchange factors of Hsp70 molecular chaperones. Front Mol Biosci 2:10. https://doi.org/10.3389/fmolb.2015.00010.
   PubMed Web of Science ®Google Scholar
• Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU. 2006. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J 25:2519–2528. https://doi.org/10.1038/sj.emboj.7601138.
   PubMed Web of Science ®Google Scholar
• Shaner L, Sousa R, Morano KA. 2006. Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry 45:15075–15084. https://doi.org/10.1021/bi061279k.
   PubMedGoogle Scholar
• Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B. 2006. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J 25:2510–2518. https://doi.org/10.1038/sj.emboj.7601139.
   PubMed Web of Science ®Google Scholar
• Easton DP, Kaneko Y, Subjeck JR. 2000. The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5:276–290. https://doi.org/10.1379/1466-1268(2000)005<0276:THAGSP>2.0.CO;2.
   PubMed Web of Science ®Google Scholar
• Nagy M, Fenton WA, Li D, Furtak K, Horwich AL. 2016. Extended survival of misfolded G85R SOD1-linked ALS mice by transgenic expression of chaperone Hsp110. Proc Natl Acad Sci U S A 113:5424–5428. https://doi.org/10.1073/pnas.1604885113.
   PubMedGoogle Scholar
• Torrente MP, Shorter J. 2013. The metazoan protein disaggregase and amyloid depolymerase system: Hsp110, Hsp70, Hsp40, and small heat shock proteins. Prion 7:457–463. https://doi.org/10.4161/pri.27531.
   PubMed Web of Science ®Google Scholar
• Abrams JL, Verghese J, Gibney PA, Morano KA. 2014. Hierarchical functional specificity of cytosolic heat shock protein 70 (Hsp70) nucleotide exchange factors in yeast. J Biol Chem 289:13155–13167. https://doi.org/10.1074/jbc.M113.530014.
   PubMedGoogle Scholar
• Glover JR, Lindquist S. 1998. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73–82. https://doi.org/10.1016/S0092-8674(00)81223-4.
   PubMed Web of Science ®Google Scholar
• Lu Z, Cyr DM. 1998. Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 273:27824–27830. https://doi.org/10.1074/jbc.273.43.27824.
   PubMed Web of Science ®Google Scholar
• Polier S, Dragovic Z, Hartl FU, Bracher A. 2008. Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133:1068–1079. https://doi.org/10.1016/j.cell.2008.05.022.
   PubMed Web of Science ®Google Scholar
• Raviol H, Bukau B, Mayer MP. 2006. Human and yeast Hsp110 chaperones exhibit functional differences. FEBS Lett 580:168–174. https://doi.org/10.1016/j.febslet.2005.11.069.
   PubMedGoogle Scholar
• Acebron SP, Martin I, del Castillo U, Moro F, Muga A. 2009. DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett 583:2991–2996. https://doi.org/10.1016/j.febslet.2009.08.020.
   PubMedGoogle Scholar
• Winkler J, Tyedmers J, Bukau B, Mogk A. 2012. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 198:387–404. https://doi.org/10.1083/jcb.201201074.
   PubMed Web of Science ®Google Scholar
• Escusa-Toret S, Vonk WI, Frydman J. 2013. Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat Cell Biol 15:1231–1243. https://doi.org/10.1038/ncb2838.
   PubMed Web of Science ®Google Scholar
• Kaganovich D, Kopito R, Frydman J. 2008. Misfolded proteins partition between two distinct quality control compartments. Nature 454:1088–1095. https://doi.org/10.1038/nature07195.
   PubMed Web of Science ®Google Scholar
• Specht S, Miller SB, Mogk A, Bukau B. 2011. Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J Cell Biol 195:617–629. https://doi.org/10.1083/jcb.201106037.
   PubMed Web of Science ®Google Scholar
• Miller SB, Ho CT, Winkler J, Khokhrina M, Neuner A, Mohamed MY, Guilbride DL, Richter K, Lisby M, Schiebel E, Mogk A, Bukau B. 2015. Compartment-specific aggregases direct distinct nuclear and cytoplasmic aggregate deposition. EMBO J 34:778–797. https://doi.org/10.15252/embj.201489524.
   PubMed Web of Science ®Google Scholar
• Sadlish H, Rampelt H, Shorter J, Wegrzyn RD, Andréasson C, Lindquist S, Bukau B. 2008. Hsp110 chaperones regulate prion formation and propagation in S. cerevisiae by two discrete activities. PLoS One 3:e1763. https://doi.org/10.1371/journal.pone.0001763.
   PubMed Web of Science ®Google Scholar
• Moran C, Kinsella GK, Zhang ZR, Perrett S, Jones GW. 2013. Mutational analysis of Sse1 (Hsp110) suggests an integral role for this chaperone in yeast prion propagation in vivo. G3 (Bethesda) 3:1409–1418. https://doi.org/10.1534/g3.113.007112.
   PubMedGoogle Scholar
• Martineau CN, Beckerich JM, Kabani M. 2007. Flo11p-independent control of “mat” formation by hsp70 molecular chaperones and nucleotide exchange factors in yeast. Genetics 177:1679–1689. https://doi.org/10.1534/genetics.107.081141.
   PubMedGoogle Scholar
• Makhnevych T, Wong P, Pogoutse O, Vizeacoumar FJ, Greenblatt JF, Emili A, Houry WA. 2012. Hsp110 is required for spindle length control. J Cell Biol 198:623–636. https://doi.org/10.1083/jcb.201111105.
   PubMedGoogle Scholar
• Gowda NK, Kandasamy G, Froehlich MS, Dohmen RJ, Andréasson C. 2013. Hsp70 nucleotide exchange factor Fes1 is essential for ubiquitin-dependent degradation of misfolded cytosolic proteins. Proc Natl Acad Sci U S A 110:5975–5980. https://doi.org/10.1073/pnas.1216778110.
   PubMedGoogle Scholar
• Sondermann H, Ho AK, Listenberger LL, Siegers K, Moarefi I, Wente SR, Hartl FU, Young JC. 2002. Prediction of novel Bag-1 homologs based on structure/function analysis identifies Snl1p as an Hsp70 co-chaperone in Saccharomyces cerevisiae. J Biol Chem 277:33220–33227. https://doi.org/10.1074/jbc.M204624200.
   PubMedGoogle Scholar
• Kabani M, Beckerich JM, Brodsky JL. 2002. Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 22:4677–4689. https://doi.org/10.1128/MCB.22.13.4677-4689.2002.
   PubMed Web of Science ®Google Scholar
• O'Driscoll J, Clare D, Saibil H. 2015. Prion aggregate structure in yeast cells is determined by the Hsp104-Hsp110 disaggregase machinery. J Cell Biol 211:145–158. https://doi.org/10.1083/jcb.201505104.
   PubMed Web of Science ®Google Scholar
• Aguado A, Fernandez-Higuero JA, Cabrera Y, Moro F, Muga A. 2015. ClpB dynamics is driven by its ATPase cycle and regulated by the DnaK system and substrate proteins. Biochem J 466:561–570. https://doi.org/10.1042/BJ20141390.
   PubMedGoogle Scholar
• Yokom AL, Gates SN, Jackrel ME, Mack KL, Su M, Shorter J, Southworth DR. 2016. Spiral architecture of the Hsp104 disaggregase reveals the basis for polypeptide translocation. Nat Struct Mol Biol 23:830–837. https://doi.org/10.1038/nsmb.3277.
   PubMedGoogle Scholar
• Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B. 1999. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96:13732–13737. https://doi.org/10.1073/pnas.96.24.13732.
   PubMed Web of Science ®Google Scholar
• Abbas-Terki T, Donze O, Briand PA, Picard D. 2001. Hsp104 interacts with Hsp90 cochaperones in respiring yeast. Mol Cell Biol 21:7569–7575. https://doi.org/10.1128/MCB.21.22.7569-7575.2001.
   PubMedGoogle Scholar
• Andréasson C, Fiaux J, Rampelt H, Druffel-Augustin S, Bukau B. 2008. Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc Natl Acad Sci U S A 105:16519–16524. https://doi.org/10.1073/pnas.0804187105.
   PubMed Web of Science ®Google Scholar
• Fan Q, Park KW, Du Z, Morano KA, Li L. 2007. The role of Sse1 in the de novo formation and variant determination of the [PSI+] prion. Genetics 177:1583–1593. https://doi.org/10.1534/genetics.107.077982.
   PubMed Web of Science ®Google Scholar
• Kryndushkin D, Wickner RB. 2007. Nucleotide exchange factors for Hsp70s are required for [URE3] prion propagation in Saccharomyces cerevisiae. Mol Biol Cell 18:2149–2154. https://doi.org/10.1091/mbc.E07-02-0128.
   PubMed Web of Science ®Google Scholar
• Gao X, Carroni M, Nussbaum-Krammer C, Mogk A, Nillegoda NB, Szlachcic A, Guilbride DL, Saibil HR, Mayer MP, Bukau B. 2015. Human Hsp70 disaggregase reverses Parkinson's-linked alpha-synuclein amyloid fibrils. Mol Cell 59:781–793. https://doi.org/10.1016/j.molcel.2015.07.012.
   PubMed Web of Science ®Google Scholar
• Cushman-Nick M, Bonini NM, Shorter J. 2013. Hsp104 suppresses polyglutamine-induced degeneration post onset in a drosophila MJD/SCA3 model. PLoS Genet 9:e1003781. https://doi.org/10.1371/journal.pgen.1003781.
   PubMed Web of Science ®Google Scholar
• Jackrel ME, DeSantis ME, Martinez BA, Castellano LM, Stewart RM, Caldwell KA, Caldwell GA, Shorter J. 2014. Potentiated Hsp104 variants antagonize diverse proteotoxic misfolding events. Cell 156:170–182. https://doi.org/10.1016/j.cell.2013.11.047.
   PubMed Web of Science ®Google Scholar
• Jackrel ME, Shorter J. 2014. Potentiated Hsp104 variants suppress toxicity of diverse neurodegenerative disease-linked proteins. Dis Model Mech 7:1175–1184. https://doi.org/10.1242/dmm.016113.
   PubMed Web of Science ®Google Scholar
• Vacher C, Garcia-Oroz L, Rubinsztein DC. 2005. Overexpression of yeast hsp104 reduces polyglutamine aggregation and prolongs survival of a transgenic mouse model of Huntington's disease. Hum Mol Genet 14:3425–3433. https://doi.org/10.1093/hmg/ddi372.
   PubMed Web of Science ®Google Scholar
• Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. 1999. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23:425–428. https://doi.org/10.1038/70532.
   PubMed Web of Science ®Google Scholar
• Wilson DS, Keefe AD. 2001. Random mutagenesis by PCR. Curr Protoc Mol Biol Chapter 8: Unit 8.3. https://doi.org/10.1002/0471142727.mb0803s51.
   Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• Andréasson C, Fiaux J, Rampelt H, Mayer MP, Bukau B. 2008. Hsp110 is a nucleotide-activated exchange factor for Hsp70. J Biol Chem 283:8877–8884. https://doi.org/10.1074/jbc.M710063200.
   PubMedGoogle Scholar
• Silve S, Volland C, Garnier C, Jund R, Chevallier MR, Haguenauer-Tsapis R. 1991. Membrane insertion of uracil permease, a polytopic yeast plasma membrane protein. Mol Cell Biol 11:1114–1124. https://doi.org/10.1128/MCB.11.2.1114.
   PubMed Web of Science ®Google Scholar
• Gowda NK, Kaimal JM, Masser AE, Kang W, Friedlander MR, Andréasson C. 2016. Cytosolic splice isoform of Hsp70 nucleotide exchange factor Fes1 is required for the degradation of misfolded proteins in yeast. Mol Biol Cell 27:1210–1219. https://doi.org/10.1091/mbc.E15-10-0697.
   PubMedGoogle Scholar
• Abrams JL, Morano KA. 2013. Coupled assays for monitoring protein refolding in Saccharomyces cerevisiae. J Vis Exp 77:e50432. https://doi.org/10.3791/50432.
   Google Scholar