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Research Paper

Low activity of select Hsp104 mutants is sufficient to propagate unstable prion variants

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Pages 394-403 | Received 08 Aug 2013, Accepted 19 Sep 2013, Published online: 24 Sep 2013

References

  • Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 2001; 24:519 - 50; http://dx.doi.org/10.1146/annurev.neuro.24.1.519; PMID: 11283320
  • Prusiner SB, Scott MR, DeArmond SJ, Cohen FE. Prion protein biology. Cell 1998; 93:337 - 48; http://dx.doi.org/10.1016/S0092-8674(00)81163-0; PMID: 9590169
  • Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. In vitro propagation of the prion-like state of yeast Sup35 protein. Science 1997; 277:381 - 3; http://dx.doi.org/10.1126/science.277.5324.381; PMID: 9219697
  • Tuite MF, Cox BS. Propagation of yeast prions. Nat Rev Mol Cell Biol 2003; 4:878 - 90; http://dx.doi.org/10.1038/nrm1247; PMID: 14625537
  • Bousset L, Melki R. Similar and divergent features in mammalian and yeast prions. Microbes Infect 2002; 4:461 - 9; http://dx.doi.org/10.1016/S1286-4579(02)01561-7; PMID: 11932197
  • Patino MM, Liu JJ, Glover JR, Lindquist S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 1996; 273:622 - 6; http://dx.doi.org/10.1126/science.273.5275.622; PMID: 8662547
  • Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J 1996; 15:3127 - 34; PMID: 8670813
  • Liebman SW, Derkatch IL. The yeast [PSI+] prion: making sense of nonsense. J Biol Chem 1999; 274:1181 - 4; http://dx.doi.org/10.1074/jbc.274.3.1181; PMID: 9880481
  • True HL, Berlin I, Lindquist SL. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 2004; 431:184 - 7; http://dx.doi.org/10.1038/nature02885; PMID: 15311209
  • True HL, Lindquist SL. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000; 407:477 - 83; http://dx.doi.org/10.1038/35035005; PMID: 11028992
  • Derkatch IL, Bradley ME, Zhou P, Chernoff YO, Liebman SW. Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 1997; 147:507 - 19; PMID: 9335589
  • Sondheimer N, Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 2000; 5:163 - 72; http://dx.doi.org/10.1016/S1097-2765(00)80412-8; PMID: 10678178
  • Derkatch IL, Bradley ME, Masse SV, Zadorsky SP, Polozkov GV, Inge-Vechtomov SG, Liebman SW. Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast?. EMBO J 2000; 19:1942 - 52; http://dx.doi.org/10.1093/emboj/19.9.1942; PMID: 10790361
  • Osherovich LZ, Weissman JS. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 2001; 106:183 - 94; http://dx.doi.org/10.1016/S0092-8674(01)00440-8; PMID: 11511346
  • Derkatch IL, Bradley ME, Hong JY, Liebman SW. Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 2001; 106:171 - 82; http://dx.doi.org/10.1016/S0092-8674(01)00427-5; PMID: 11511345
  • Stein KC, True HL. The [RNQ+] prion: a model of both functional and pathological amyloid. Prion 2011; 5:291 - 8; PMID: 22052347
  • Chernoff YO, Lindquist SL, Ono B, Inge-Vechtomov SG, Liebman SW. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. [psi+] Science 1995; 268:880 - 4; http://dx.doi.org/10.1126/science.7754373; PMID: 7754373
  • Alberti S, Halfmann R, King O, Kapila A, Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009; 137:146 - 58; http://dx.doi.org/10.1016/j.cell.2009.02.044; PMID: 19345193
  • Tuite MF, Marchante R, Kushnirov V. Fungal prions: structure, function and propagation. Top Curr Chem 2011; 305:257 - 98; http://dx.doi.org/10.1007/128_2011_172; PMID: 21717344
  • Glover JR, Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 1998; 94:73 - 82; http://dx.doi.org/10.1016/S0092-8674(00)81223-4; PMID: 9674429
  • Sanchez Y, Lindquist SL. HSP104 required for induced thermotolerance. Science 1990; 248:1112 - 5; http://dx.doi.org/10.1126/science.2188365; PMID: 2188365
  • Lum R, Niggemann M, Glover JR. Peptide and protein binding in the axial channel of Hsp104. Insights into the mechanism of protein unfolding. J Biol Chem 2008; 283:30139 - 50; http://dx.doi.org/10.1074/jbc.M804849200; PMID: 18755692
  • Lum R, Tkach JM, Vierling E, Glover JR. Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J Biol Chem 2004; 279:29139 - 46; http://dx.doi.org/10.1074/jbc.M403777200; PMID: 15128736
  • Tessarz P, Mogk A, Bukau B. Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol Microbiol 2008; 68:87 - 97; http://dx.doi.org/10.1111/j.1365-2958.2008.06135.x; PMID: 18312264
  • Hung GC, Masison DC. N-terminal domain of yeast Hsp104 chaperone is dispensable for thermotolerance and prion propagation but necessary for curing prions by Hsp104 overexpression. Genetics 2006; 173:611 - 20; http://dx.doi.org/10.1534/genetics.106.056820; PMID: 16582428
  • Grimminger-Marquardt V, Lashuel HA. Structure and function of the molecular chaperone Hsp104 from yeast. Biopolymers 2010; 93:252 - 76; http://dx.doi.org/10.1002/bip.21301; PMID: 19768774
  • Winkler J, Tyedmers J, Bukau B, Mogk A. Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 2012; 179:152 - 60; http://dx.doi.org/10.1016/j.jsb.2012.05.002; PMID: 22580344
  • Cashikar AG, Schirmer EC, Hattendorf DA, Glover JR, Ramakrishnan MS, Ware DM, Lindquist SL. Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol Cell 2002; 9:751 - 60; http://dx.doi.org/10.1016/S1097-2765(02)00499-9; PMID: 11983167
  • Tkach JM, Glover JR. Amino acid substitutions in the C-terminal AAA+ module of Hsp104 prevent substrate recognition by disrupting oligomerization and cause high temperature inactivation. J Biol Chem 2004; 279:35692 - 701; http://dx.doi.org/10.1074/jbc.M400782200; PMID: 15178690
  • Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov VV. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 2003; 278:49636 - 43; http://dx.doi.org/10.1074/jbc.M307996200; PMID: 14507919
  • Wegrzyn RD, Bapat K, Newnam GP, Zink AD, Chernoff YO. Mechanism of prion loss after Hsp104 inactivation in yeast. Mol Cell Biol 2001; 21:4656 - 69; http://dx.doi.org/10.1128/MCB.21.14.4656-4669.2001; PMID: 11416143
  • Satpute-Krishnan P, Langseth SX, Serio TR. Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol 2007; 5:e24; http://dx.doi.org/10.1371/journal.pbio.0050024; PMID: 17253904
  • Takahashi A, Hara H, Kurahashi H, Nakamura Y. A systematic evaluation of the function of the protein-remodeling factor Hsp104 in [PSI+] prion propagation in S. cerevisiae by comprehensive chromosomal mutations. Prion 2007; 1:69 - 77; http://dx.doi.org/10.4161/pri.1.1.4060; PMID: 19164920
  • Bardill JP, Dulle JE, Fisher JR, True HL. Requirements of Hsp104p activity and Sis1p binding for propagation of the [RNQ(+)] prion. Prion 2009; 3:151 - 60; http://dx.doi.org/10.4161/pri.3.3.9662; PMID: 19770577
  • Hattendorf DA, Lindquist SL. Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J 2002; 21:12 - 21; http://dx.doi.org/10.1093/emboj/21.1.12; PMID: 11782421
  • Hattendorf DA, Lindquist SL. Analysis of the AAA sensor-2 motif in the C-terminal ATPase domain of Hsp104 with a site-specific fluorescent probe of nucleotide binding. Proc Natl Acad Sci U S A 2002; 99:2732 - 7; http://dx.doi.org/10.1073/pnas.261693199; PMID: 11867765
  • Helsen CW, Glover JR. Insight into molecular basis of curing of [PSI+] prion by overexpression of 104-kDa heat shock protein (Hsp104). J Biol Chem 2012; 287:542 - 56; http://dx.doi.org/10.1074/jbc.M111.302869; PMID: 22081611
  • True HL. The battle of the fold: chaperones take on prions. Trends Genet 2006; 22:110 - 7; http://dx.doi.org/10.1016/j.tig.2005.12.004; PMID: 16378656
  • Inoue Y, Taguchi H, Kishimoto A, Yoshida M. Hsp104 binds to yeast Sup35 prion fiber but needs other factor(s) to sever it. J Biol Chem 2004; 279:52319 - 23; http://dx.doi.org/10.1074/jbc.M408159200; PMID: 15448141
  • Shorter J, Lindquist S. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 2004; 304:1793 - 7; http://dx.doi.org/10.1126/science.1098007; PMID: 15155912
  • Sweeny EA, Shorter J. Prion proteostasis: Hsp104 meets its supporting cast. Prion 2008; 2:135 - 40; http://dx.doi.org/10.4161/pri.2.4.7952; PMID: 19242125
  • Newnam GP, Wegrzyn RD, Lindquist SL, Chernoff YO. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol Cell Biol 1999; 19:1325 - 33; PMID: 9891066
  • Sharma D, Masison DC. Functionally redundant isoforms of a yeast Hsp70 chaperone subfamily have different antiprion effects. Genetics 2008; 179:1301 - 11; http://dx.doi.org/10.1534/genetics.108.089458; PMID: 18562668
  • Aron R, Higurashi T, Sahi C, Craig EA. J-protein co-chaperone Sis1 required for generation of [RNQ+] seeds necessary for prion propagation. EMBO J 2007; 26:3794 - 803; http://dx.doi.org/10.1038/sj.emboj.7601811; PMID: 17673909
  • Higurashi T, Hines JK, Sahi C, Aron R, Craig EA. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci U S A 2008; 105:16596 - 601; http://dx.doi.org/10.1073/pnas.0808934105; PMID: 18955697
  • Jones GW, Masison DC. Saccharomyces cerevisiae Hsp70 mutations affect [PSI+] prion propagation and cell growth differently and implicate Hsp40 and tetratricopeptide repeat cochaperones in impairment of [PSI+]. [PSI+] Genetics 2003; 163:495 - 506; PMID: 12618389
  • Mathur V, Hong JY, Liebman SW. Ssa1 overexpression and [PIN(+)] variants cure [PSI(+)] by dilution of aggregates. J Mol Biol 2009; 390:155 - 67; http://dx.doi.org/10.1016/j.jmb.2009.04.063; PMID: 19422835
  • Krishnan R, Lindquist SL. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 2005; 435:765 - 72; http://dx.doi.org/10.1038/nature03679; PMID: 15944694
  • Tanaka M, Chien P, Naber N, Cooke R, Weissman JS. Conformational variations in an infectious protein determine prion strain differences. Nature 2004; 428:323 - 8; http://dx.doi.org/10.1038/nature02392; PMID: 15029196
  • Toyama BH, Kelly MJ, Gross JD, Weissman JS. The structural basis of yeast prion strain variants. Nature 2007; 449:233 - 7; http://dx.doi.org/10.1038/nature06108; PMID: 17767153
  • Collinge J, Clarke AR. A general model of prion strains and their pathogenicity. Science 2007; 318:930 - 6; http://dx.doi.org/10.1126/science.1138718; PMID: 17991853
  • Tanaka M, Chien P, Yonekura K, Weissman JS. Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 2005; 121:49 - 62; http://dx.doi.org/10.1016/j.cell.2005.03.008; PMID: 15820678
  • Derkatch IL, Chernoff YO, Kushnirov VV, Inge-Vechtomov SG, Liebman SW. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 1996; 144:1375 - 86; PMID: 8978027
  • Zhou P, Derkatch IL, Uptain SM, Patino MM, Lindquist S, Liebman SW. The yeast non-Mendelian factor [ETA+] is a variant of [PSI+], a prion-like form of release factor eRF3. EMBO J 1999; 18:1182 - 91; http://dx.doi.org/10.1093/emboj/18.5.1182; PMID: 10064585
  • Tanaka M, Collins SR, Toyama BH, Weissman JS. The physical basis of how prion conformations determine strain phenotypes. Nature 2006; 442:585 - 9; http://dx.doi.org/10.1038/nature04922; PMID: 16810177
  • Tessier PM, Lindquist S. Prion recognition elements govern nucleation, strain specificity and species barriers. Nature 2007; 447:556 - 61; http://dx.doi.org/10.1038/nature05848; PMID: 17495929
  • DeSantis ME, Shorter J. Hsp104 drives “protein-only” positive selection of Sup35 prion strains encoding strong [PSI(+)]. Chem Biol 2012; 19:1400 - 10; http://dx.doi.org/10.1016/j.chembiol.2012.09.013; PMID: 23177195
  • Tipton KA, Verges KJ, Weissman JS. In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol Cell 2008; 32:584 - 91; http://dx.doi.org/10.1016/j.molcel.2008.11.003; PMID: 19026788
  • Bradley ME, Edskes HK, Hong JY, Wickner RB, Liebman SW. Interactions among prions and prion “strains” in yeast. Proc Natl Acad Sci U S A 2002; 99:Suppl 4 16392 - 9; http://dx.doi.org/10.1073/pnas.152330699; PMID: 12149514
  • Bradley ME, Liebman SW. Destabilizing interactions among [PSI(+)] and [PIN(+)] yeast prion variants. Genetics 2003; 165:1675 - 85; PMID: 14704158
  • Bardill JP, True HL. Heterologous prion interactions are altered by mutations in the prion protein Rnq1p. J Mol Biol 2009; 388:583 - 96; http://dx.doi.org/10.1016/j.jmb.2009.03.036; PMID: 19324054
  • Kalastavadi T, True HL. Analysis of the [RNQ+] prion reveals stability of amyloid fibers as the key determinant of yeast prion variant propagation. J Biol Chem 2010; 285:20748 - 55; http://dx.doi.org/10.1074/jbc.M110.115303; PMID: 20442412
  • Bagriantsev SN, Kushnirov VV, Liebman SW. Analysis of amyloid aggregates using agarose gel electrophoresis. Methods Enzymol 2006; 412:33 - 48; http://dx.doi.org/10.1016/S0076-6879(06)12003-0; PMID: 17046650
  • Schirmer EC, Queitsch C, Kowal AS, Parsell DA, Lindquist S. The ATPase activity of Hsp104, effects of environmental conditions and mutations. J Biol Chem 1998; 273:15546 - 52; http://dx.doi.org/10.1074/jbc.273.25.15546; PMID: 9624144
  • Parsell DA, Kowal AS, Lindquist S. Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J Biol Chem 1994; 269:4480 - 7; PMID: 8308017
  • DeSantis ME, Leung EH, Sweeny EA, Jackrel ME, Cushman-Nick M, Neuhaus-Follini A, Vashist S, Sochor MA, Knight MN, Shorter J. Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 2012; 151:778 - 93; http://dx.doi.org/10.1016/j.cell.2012.09.038; PMID: 23141537
  • Krzewska J, Melki R. Molecular chaperones and the assembly of the prion Sup35p, an in vitro study. EMBO J 2006; 25:822 - 33; http://dx.doi.org/10.1038/sj.emboj.7600985; PMID: 16467849
  • Romanova NV, Chernoff YO. Hsp104 and prion propagation. Protein Pept Lett 2009; 16:598 - 605; http://dx.doi.org/10.2174/092986609788490078; PMID: 19519517
  • Glover JR, Lum R. Remodeling of protein aggregates by Hsp104. Protein Pept Lett 2009; 16:587 - 97; http://dx.doi.org/10.2174/092986609788490087; PMID: 19519516
  • Du Z, Park KW, Yu H, Fan Q, Li L. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat Genet 2008; 40:460 - 5; http://dx.doi.org/10.1038/ng.112; PMID: 18362884
  • Patel BK, Gavin-Smyth J, Liebman SW. The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat Cell Biol 2009; 11:344 - 9; http://dx.doi.org/10.1038/ncb1843; PMID: 19219034
  • Wickner RB, Taylor KL, Edskes HK, Maddelein ML, Moriyama H, Roberts BT. Prions of yeast as heritable amyloidoses. J Struct Biol 2000; 130:310 - 22; http://dx.doi.org/10.1006/jsbi.2000.4250; PMID: 10940235
  • Doyle SM, Shorter J, Zolkiewski M, Hoskins JR, Lindquist S, Wickner S. Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity. Nat Struct Mol Biol 2007; 14:114 - 22; http://dx.doi.org/10.1038/nsmb1198; PMID: 17259993
  • Schaupp A, Marcinowski M, Grimminger V, Bösl B, Walter S. Processing of proteins by the molecular chaperone Hsp104. J Mol Biol 2007; 370:674 - 86; http://dx.doi.org/10.1016/j.jmb.2007.04.070; PMID: 17543332
  • Mackay RG, Helsen CW, Tkach JM, Glover JR. The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry 2008; 47:1918 - 27; http://dx.doi.org/10.1021/bi701714s; PMID: 18197703
  • Kryndushkin DS, Engel A, Edskes H, Wickner RB. Molecular chaperone Hsp104 can promote yeast prion generation. Genetics 2011; 188:339 - 48; http://dx.doi.org/10.1534/genetics.111.127779; PMID: 21467567
  • Borchsenius AS, Müller S, Newnam GP, Inge-Vechtomov SG, Chernoff YO. Prion variant maintained only at high levels of the Hsp104 disaggregase. Curr Genet 2006; 49:21 - 9; http://dx.doi.org/10.1007/s00294-005-0035-0; PMID: 16307272

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