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

Prion

Volumn 7, Issue 5, 2013, Pages 394-403

  Dulle, Jennifer E ^a   True, Heather L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

PSI+ ; RNQ+ ; Chaperone biology; Hsp104; Prion variants; Yeast prions

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 104; PROTEIN VARIANT;

AMINO ACID SEQUENCE; ARTICLE; CONFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HEAT; HYDROLYSIS; MUTAGENESIS; NONHUMAN; POINT MUTATION; PRION; PROTEIN AGGREGATION; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

CHAPERONE BIOLOGY; HSP104; PRION VARIANTS; YEAST PRIONS; [PSI+]; [RNQ+];

ADENOSINE TRIPHOSPHATE; HEAT-SHOCK PROTEINS; HYDROLYSIS; MUTATION, MISSENSE; PEPTIDE TERMINATION FACTORS; POINT MUTATION; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84887837907     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.26547     Document Type: Article

References (77)

1. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 2001;24:519-50; PMID:11283320; http://dx.doi.org/10.1146/annurev. neuro.24.1.519
2. Prusiner SB, Scott MR, De Armond SJ, Cohen FE. Prion protein biology. Cell 1998;93:337-48; PMID:9590169; http://dx.doi.org/10.1016/S0092-8674 (00) 81163-0
3. Paushkin SV, Kushnirov V V, Smirnov VN, Ter-Avanesyan MD. In vitro propagation of the prion-like state of yeast Sup35 protein. Science 1997;277:381-3; PM ID:9219697; http://dx.doi.org/10.1126/science.277.5324.381
4. Tuite MF, Cox BS. Propagation of yeast prions. Nat Rev Mol Cell Biol 2003;4:878-90; PMID:14625537; http://dx.doi.org/10.1038/nrm1247
5. Bousset L, Melki R. Similar and divergent features in mammalian and yeast prions. Microbes Infect 2002;4:461-9; PMID:11932197; http://dx.doi.org/10.1016/ S1286-4579 (02) 01561-7
6. 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; PMID:8662547; http://dx.doi.org/10.1126/science.273.5275.622
7. 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
8. Liebman SW, Derkatch IL. The yeast [PSI+] prion: making sense of nonsense. J Biol Chem 1999;274:1181-4; PMID:9880481; http://dx.doi. o r g/10.1074/j b c. 274. 3.1181
9. True HL, Berlin I, Lindquist SL. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 2004;431:184-7; PMID:15311209; http://dx.doi.org/10.1038/nature02885
10. True HL, Lindquist SL. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000;407:477-83; PMID:11028992; http://dx.doi.org/10.1038/35035005
11. 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
12. Sondheimer N, Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 2000;5:163-72; PMID:10678178; http://dx.doi.org/10. 1016/S1097-2765 (00) 80412-8
13. 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; PMID:10790361; http://dx.doi.org/10.1093/emboj/19.9.1942
14. Osherovich LZ, Weissman JS. Multiple Gln/Asnrich prion domains confer susceptibility to induction of the yeast [PSI (+)] prion. Cell 2001;106:183-94; PM ID:11511346; http://dx.doi.org/10.1016/S0092-8674 (01) 00440-8
15. Derkatch IL, Bradley ME, Hong JY, Liebman SW. Prions affect the appearance of other prions: the story of [PIN (+)]. Cell 2001;106:171-82; PMID:11511345; http://dx.doi.org/10.1016/S0092-8674 (01) 00427-5
16. Stein KC, True HL. The [RNQ+] prion: a model of both functional and pathological amyloid. Prion 2011;5:291-8; PMID:22052347
17. 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; PMID:7754373; http://dx.doi.org/10.1126/ science.7754373
18. 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; PMID:19345193; http://dx.doi.org/10.1016/j.cell.2009.02. 044
19. Tuite MF, Marchante R, Kushnirov V. Fungal prions: structure, function and propagation. Top Curr Chem 2011;305:257-98; PMID:21717344; http://dx.doi.org/10.1007/128-2011-172
20. Glover JR, Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 1998;94:73-82; PMID:9674429; http://dx.doi.org/10.1016/S0092-8674 (00) 81223-4
21. Sanchez Y, Lindquist SL. HSP104 required for induced thermotolerance. Science 1990;248:1112-5; PMID:2188365; http://dx.doi.org/10.1126/science.2188365
22. 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; PMID:18755692; http://dx.doi.org/10.1074/jbc. M804849200
23. 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; PMID:15128736; http://dx.doi.org/10.1074/jbc. M403777200
24. 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; PMID:18312264; http://dx.doi. o r g/10.1111/j.1365-2958. 2008. 06135. x
25. 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; PMID:16582428; http://dx.doi.org/10.1534/genetics.106.056820
26. Grimminger-Marquardt V, Lashuel HA. Structure and function of the molecular chaperone Hsp104 from yeast. Biopolymers 2010;93:252-76; PMID:19768774; http://dx.doi.org/10.1002/bip. 21301
27. Winkler J, Tyedmers J, Bukau B, Mogk A. Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 2012;179:152-60; PMID:22580344; http://dx.doi.org/10.1016/j. jsb.2012.05.002
28. 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; PM ID:11983167; http://dx.doi.org/10.1016/S1097-2765 (02) 00499-9
29. 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; PMID:15178690; http://dx.doi.org/10.1074/jbc. M400782200
30. Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov V V. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 2003;278:49636-43; PMID:14507919; http://dx.doi.org/10.1074/jbc. M307996200
31. 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; PMID:11416143; http://dx.doi.org/10.1128/MCB.21.14.4656-4669.2001
32. Satpute-Krishnan P, Langseth SX, Serio TR. Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol 2007;5:e24; PMID:17253904; http://dx.doi.org/10.1371/journal.pbio.0050024
33. Takahashi A, Hara H, Kurahashi H, Nakamura Y. A systematic evaluation of the function of the proteinremodeling factor Hsp104 in [PSI+] prion propagation in S. cerevisiae by comprehensive chromosomal mutations. Prion 2007;1:69-77; PMID:19164920; http://dx.doi.org/10.4161/pri.1.1.4060
34. 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; PMID:19770577; http://dx.doi.org/10.4161/pri.3.3.9662
35. 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; PMID:11782421; http://dx.doi.org/10.1093/emboj/21.1.12
36. 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; PMID:11867765; http://dx.doi.org/10.1073/pnas.261693199
37. 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; PMID:22081611; http://dx.doi. or g/10.1074/jbc. M111.302869
38. True HL. The battle of the fold: chaperones take on prions. Trends Genet 2006;22:110-7; PMID:16378656; http://dx.doi.org/10.1016/j. tig.2005.12.004
39. 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; PMID:15448141; http://dx.doi.org/10.1074/jbc. M408159200
40. Shorter J, Lindquist S. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 2004;304:1793-7; PMID:15155912; http://dx.doi.org/10.1126/science.1098007
41. Sweeny EA, Shorter J. Prion proteostasis: Hsp104 meets its supporting cast. Prion 2008;2:135-40; PMID:19242125; http://dx.doi.org/10.4161/pri.2.4.7952
42. 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
43. Sharma D, Masison DC. Functionally redundant isoforms of a yeast Hsp70 chaperone subfamily have different antiprion effects. Genetics 2008;179:1301-11; PMID:18562668; http://dx.doi.org/10.1534/genetics.108.089458
44. 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; PMID:17673909; http://dx.doi.org/10.1038/sj.emboj.7601811
45. 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; PMID:18955697; http://dx.doi.org/10.1073/pnas.0808934105
46. 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
47. Mathur V, Hong JY, Liebman SW. Ssa1 overexpression and [PIN (+)] variants cure [PSI (+)] by dilution of aggregates. J Mol Biol 2009;390:155-67; PMID:19422835; http://dx.doi.org/10.1016/j. jmb.2009.04.063
48. Krishnan R, Lindquist SL. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 2005;435:765-72; PMID:15944694; http://dx.doi.org/10.1038/nature03679
49. 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; PMID:15029196; http://dx.doi.org/10.1038/nature02392
50. Toyama BH, Kelly MJ, Gross JD, Weissman JS. The structural basis of yeast prion strain variants. Nature 2007;449:233-7; PMID:17767153; http://dx.doi.org/10.1038/nature06108
51. Collinge J, Clarke AR. A general model of prion strains and their pathogenicity. Science 2007;318:930-6; PM ID:17991853; http://dx.doi.org/10. 1126/science.1138718
52. 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; PMID:15820678; http://dx.doi.org/10.1016/j. cell.2005.03.008
53. Derkatch IL, Chernoff YO, Kushnirov V V, Inge-Vechtomov SG, Liebman SW. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 1996;144:1375-86; PMID:8978027
54. 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; PMID:10064585; http://dx.doi.org/ 10.1093/emboj/18.5.1182
55. Tanaka M, Collins SR, Toyama BH, Weissman JS. The physical basis of how prion conformations determine strain phenotypes. Nature 2006;442:585-9; PMID:16810177; http://dx.doi.org/10.1038/nature04922
56. Tessier PM, Lindquist S. Prion recognition elements govern nucleation, strain specificity and species barriers. Nature 2007;447:556-61; PMID:17495929; http://dx.doi.org/10.1038/nature05848
57. De Santis ME, Shorter J. Hsp104 drives "proteinonly" positive selection of Sup35 prion strains encoding strong [PSI (+)]. Chem Biol 2012;19:1400-10; PMID:23177195; http://dx.doi.org/10.1016/j. chembiol. 2012.09.013
58. 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; PMID:19026788; http://dx.doi.org/10.1016/j. molcel.2008.11.003
59. 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; PMID:12149514; http://dx.doi.org/10.1073/pnas. 152330699
60. Bradley ME, Liebman SW. Destabilizing interactions among [PSI (+)] and [PIN (+)] yeast prion variants. Genetics 2003;165:1675-85; PMID:14704158
61. Bardill JP, True HL. Heterologous prion interactions are altered by mutations in the prion protein Rnq1p. J Mol Biol 2009;388:583-96; PMID:19324054; http://dx.doi.org/10.1016/j.jmb.2009.03.036
62. 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; PMID:20442412; http://dx.doi.org/10.1074/jbc. M110.115303
63. Bagriantsev SN, Kushnirov V V, Liebman SW. Analysis of amyloid aggregates using agarose gel electrophoresis. Methods Enzymol 2006;412:33-48; PMID:17046650; http://dx.doi.org/10.1016/S0076-6879 (06) 12003-0
64. 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; PMID:9624144; http://dx.doi.org/10.1074/jbc.273.25.15546
65. 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
66. De Santis 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; PMID:23141537; http://dx.doi.org/10.1016/j. cell.2012.09.038
67. Krzewska J, Melki R. Molecular chaperones and the assembly of the prion Sup35p, an in vitro study. EMBO J 2006;25:822-33; PMID:16467849; http://dx.doi.org/10.1038/sj.emboj.7600985
68. Romanova NV, Chernoff YO. Hsp104 and prion propagation. Protein Pept Lett 2009;16:598-605; PMID:19519517; http://dx.doi.org/10.2174/092986609788490078
69. Glover JR, Lum R. Remodeling of protein aggregates by Hsp104. Protein Pept Lett 2009;16:587-97; PMID:19519516; http://dx.doi.org/10.2174/ 092986609788490087
70. 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; PMID:18362884; http://dx.doi.org/10.1038/ng.112
71. 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; PMID:19219034; http://dx.doi.org/10.1038/ncb1843
72. 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; PMID:10940235; http://dx.doi.org/10.1006/jsbi.2000.4250
73. 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; PMID:17259993; http://dx.doi.org/10.1038/nsmb1198
74. 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; PMID:17543332; http://dx.doi.org/10.1016/j. jmb.2007.04.070
75. 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; PM ID:18197703; http://dx.doi.org/10.1021/bi701714s
76. Kryndushkin DS, Engel A, Edskes H, Wickner RB. Molecular chaperone Hsp104 can promote yeast prion generation. Genetics 2011;188:339-48; PMID:21467567; http://dx.doi.org/10.1534/g enetics.111.127779
77. 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; PMID:16307272; http://dx.doi.org/10.1007/s00294-005-0035-0