Prion propagation can occur in a prokaryote and requires the ClpB chaperone

eLife

Volumn 3, Issue August2014, 2014, Pages 1-19

  Yuan, Andy H ^a,b   Garrity, Sean J ^a   Nako, Entela ^a   Hochschild, Ann ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PROTEIN CLPB; CHAPERONE; CLPB PROTEIN, E COLI; DODECYL SULFATE SODIUM; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN; HSP104 PROTEIN, S CEREVISIAE; NEW1 PROTEIN, S CEREVISIAE; PRION; SACCHAROMYCES CEREVISIAE PROTEIN; SUP35 PROTEIN, S CEREVISIAE; TRANSLATION TERMINATION FACTOR;

ANIMAL CELL; ARTICLE; BREEDING; CELL GROWTH; CELL LINEAGE; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; NONHUMAN; PLASMID; PRION PROPAGATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; TEMPERATURE SENSITIVE MUTANT; WESTERN BLOTTING; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PRION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; FUNGI; MAMMALIA; PROKARYOTA;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; MOLECULAR CHAPERONES; MUTATION; PEPTIDE TERMINATION FACTORS; PRIONS; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SODIUM DODECYL SULFATE;

EID: 84934290549     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02949     Document Type: Article

References (67)

1. Aigle M, Lacroute F. 1975. Genetical aspects of [URE3], a non-mitochondrial, cytoplasmically inherited mutation in yeast. Molecular & General Genetics 136:327-335. doi: 10.1007/BF00341717.
2. Alberti S, Halfmann R, King O, Kapila A, Lindquist S. 2009. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137:146-158. doi: 10.1016/j.cell.2009.02.044.
3. Allen KD, Chernova TA, Tennant EP, Wilkinson KD, Chernoff YO. 2007. Effects of ubiquitin system alterations on the formation and loss of a yeast prion. The Journal of Biological Chemistry 282:3004-3013. doi: 10.1074/jbc.M609597200.
4. Carroni M, Kummer E, Oguchi Y, Wendler P, Clare DK, Sinning I, Kopp J, Mogk A, Bukau B, Saibil H. 2014. Head-to-tail interactions of the coiled-coil domains regulate ClpB cooperation with Hsp70 in protein disaggregation. eLife doi: 10.7554/eLife.02481.
5. Caughey B, Baron GS, Chesebro B, Jeffrey M. 2009. Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annual Review of Biochemistry 78:177-204. doi: 10.1146/annurev.biochem.78.082907.145410.
6. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851-855. doi: 10.1126/science.1067484.
7. Chernoff YO, Lindquist SL, Ono B, Inge-Vechtomov SG, Liebman SW. 1995. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268:880-884. doi: 10.1126/science.7754373.
8. Coustou V, Deleu C, Saupe S, Begueret J. 1997. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proceedings of the National Academy of Sciences of USA 94:9773-9778. doi: 10.1073/pnas.94.18.9773.
9. Cox BS. 1965. ψ, a cytoplasmic suppressor of super-suppressor in yeast. Heredity 20:505-521. doi: 10.1038/hdy.1965.65.
10. Cox B, Ness F, Tuite M. 2003. Analysis of the generation and segregation of propagons: entities that propagate the [PSI+] prion in yeast. Genetics 165:23-33.
11. Derkatch IL, Bradley ME, Hong JY, Liebman SW. 2001. Prions affect the appearance of other prions: the story of [PIN+]. Cell 106:171-182. doi: 10.1016/S0092-8674(01)00427-5.
12. Derkatch IL, Bradley ME, Masse SV, Zadorsky SP, Polozkov GV, Inge-Vechtomov SG, Liebman SW. 2000. Dependence and independence of [PSI+] and [PIN+]: a two-prion system in yeast? The EMBO Journal 19:1942-1952. doi: 10.1093/emboj/19.9.1942.
13. Derkatch IL, Bradley ME, Zhou P, Chernoff YO, Liebman SW. 1997. Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147:507-519.
14. DeSantis ME, Leung EH, Sweeny EA, Jackrel ME, Cushman-Nick M, Neuhaus-Follini A, Vashist S, Sochor MA, Knight MN, Shorter J. 2012. Operational plasticity enables Hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151:778-793. doi: 10.1016/j.cell.2012.09.038.
15. Diaz-Espinoza R, Soto C. 2012. High-resolution structure of infectious prion protein: the final frontier. Nature Structural & Molecular Biology 19:370-377. doi: 10.1038/nsmb.2266.
16. DiSalvo S, Derdowski A, Pezza JA, Serio TR. 2011. Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nature Structural & Molecular Biology 18:486-492. doi: 10.1038/nsmb.2031.
17. Doyle SM, Wickner S. 2009. Hsp104 and ClpB: protein disaggregating machines. Trends in Biochemical Sciences 34:40-48. doi: 10.1016/j.tibs.2008.09.010.
18. Espargaró A, Villar-Piqué A, Sabaté R, Ventura S. 2012. Yeast prions form infectious amyloid inclusion bodies in bacteria. Microbial Cell Factories 11:89. doi: 10.1186/1475-2859-11-89.
19. Espinosa Angarica V, Ventura S, Sancho J. 2013. Discovering putative prion sequences in complete proteomes using probabilistic representations of Q/N-rich domains. BMC Genomics 14:316. doi: 10.1186/1471-2164-14-316.
20. Fernándes-Tresguerres ME, Moreno-Díaz de la Espina S, Gasset-Rosa F, Giraldo R. 2010. A DNA-promoted amyloid proteinopathy in Escherichia coli. Molecular Microbiology 77:1456-1469. doi: 10.1111/j.1365-2958.2010.07299.x.
21. Frederick KK, Debelouchina GT, Kayatekin C, Dorminy T, Jacavone AC, Griffin RG, Lindquist S. 2014. Distinct prion strains are defined by amyloid core structure and chaperone binding site dynamics. Chemistry & Biology 21:295-305. doi: 10.1016/j.chembiol.2013.12.013.
22. Garrity SJ, Sivanathan V, Dong J, Lindquist S, Hochschild A. 2010. Conversion of a yeast prion protein to an infectious form in bacteria. Proceedings of the National Academy of Sciences of USA 107:10596-10601. doi: 10.1073/pnas.0913280107.
23. Gasset-Rosa F, Coquel AS, Moreno-Del Álamo M, Chen P, Song X, Serrano AM, Fernández-Tresguerres ME, Moreno-Díaz de la Espina S, Lindner AB, Giraldo R. 2014. Direct assessment in bacteria of prionoid propagation and phenotype selection by Hsp70 chaperone. Molecular Microbiology 91:1070-1087. doi: 10.1111/mmi.12518.
24. Goldschmidt L, Teng PK, Riek R, Eisenberg D. 2010. Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proceedings of the National Academy of Sciences of USA 107:3487-3492. doi: 10.1073/pnas.0915166107.
25. Haldimann A, Wanner BL. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. Journal of Bacteriology 183:6384-6393. doi: 10.1128/JB.183.21.6384-6393.2001.
26. Higurashi T, Hines JK, Sahi C, Aron R, Craig EA. 2008. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proceedings of the National Academy of Sciences of USA 105:16596-16601. doi: 10.1073/pnas.0808934105.
27. Holmes DL, Lancaster AK, Lindquist S, Halfmann R. 2013. Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153:153-165. doi: 10.1016/j.cell.2013.02.026.
28. King C, Diaz-Avalos R. 2004. Protein-only transmission of three yeast prion strains. Nature 428:319-323. doi: 10.1038/nature02391.
29. Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov VV. 2003. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. The Journal of Biological Chemistry 278:49636-49643. doi: 10.1074/jbc.M307996200.
30. Lancaster AK, Bardill JP, True HL, Masel J. 2010. The spontaneous appearance rate of the yeast prion [PSI+] and its implications for the evolution of the evolvability properties of the [PSI+] system. Genetics 184:393-400. doi: 10.1534/genetics.109.110213.
31. Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M, Tsai FT. 2003. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115:229-240. doi: 10.1016/S0092-8674(03)00807-9.
32. Li L, Lindquist S. 2000. Creating a protein-based element of inheritance. Science 287:661-676. doi: 10.1126/science.287.5453.661.
33. Liebman SW, Chernoff YO. 2012. Prions in yeast. Genetics 191:1041-1072. doi: 10.1534/genetics.111.137760.
34. Liu JJ, Sondheimer N, Lindquist SL. 2002. Changes in the middle region of Sup35 profoundly alter the nature of epigenetic inheritance for the yeast prion [PSI+]. Proceedings of the National Academy of Sciences of USA 99:16446-16453. doi: 10.1073/pnas.252652099.
35. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Research 25:1203-1210. doi: 10.1093/nar/25.6.1203.
36. Maddelein ML, Reis SD, Duvezin-Caubet S, Coulary-Salin B, Saupe SJ. 2002. Amyloid aggregates of the HET-s prion protein are infectious. Proceedings of the National Academy of Sciences of USA 99:7402-7407. doi: 10.1073/pnas.072199199.
37. Mogk A, Schlieker C, Strub C, Rist W, Weibezahn J, Bukau B. 2003. Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. The Journal of Biological Chemistry 278:17615-17624. doi: 10.1074/jbc.M209686200.
38. Ness F, Ferreira P, Cox BS, Tuite MF. 2002. Guanidine hydrochloride inhibits the generation of prion "seeds" but not prion protein aggregation in yeast. Molecular and Cellular Biology 22:5593-5605. doi: 10.1128/MCB.22.15.5593-5605.2002.
39. Newby GA, Lindquist S. 2013. Blessings in disguise: biological benefits of prion-like mechanisms. Trends in Cell Biology 23:251-259. doi: 10.1016/j.tcb.2013.01.007.
40. Oguchi Y, Kummer E, Seyffer F, Berynskyy M, Anstett B, Zahn R, Wade RC, Mogk A, Bukau B. 2012. A tightly regulated molecular toggle controls AAA+ disaggregase. Nature Structural & Molecular Biology 19:1338-1346. doi: 10.1038/nsmb.2441.
41. Osherovich LZ, Weissman JS. 2001. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106:183-194. doi: 10.1016/S0092-8674(01)00440-8.
42. Patino MM, Liu JJ, Glover JR, Lindquist S. 1996. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273:622-626. doi: 10.1126/science.273.5275.622.
43. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. 1996. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. The EMBO Journal 15:3127-3134.
44. Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144. doi: 10.1126/science.6801762.
45. Reidy M, Miot M, Masison DC. 2012. Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics 192:185-193. doi: 10.1534/genetics.112.142307.
46. Romero D, Aguilar C, Losick R, Kolter R. 2010. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proceedings of the National Academy of Sciences of USA 107:2230-2234. doi: 10.1073/pnas.0910560107.
47. Sabaté R, Espargaró A, Saupe SJ, Ventura S. 2009. Characterization of the amyloid bacterial inclusion bodies of the HET-s fungal prion. Microbial Cell Factories 8:56. doi: 10.1186/1475-2859-8-56.
48. Satpute-Krishnan P, Langseth SX, Serio TR. 2007. Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLOS Biology 5:e24. doi: 10.1371/journal.pbio.0050024.
49. Seyffer F, Kummer E, Oguchi Y, Winkler J, Kumar M, Zahn R, Sourjik V, Bukau B, Mogk A. 2012. Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nature Structural & Molecular Biology 19:1347-1355. doi: 10.1038/nsmb.2442.
50. Shorter J, Lindquist S. 2004. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304:1793-1797. doi: 10.1126/science.1098007.
51. Shorter J, Lindquist S. 2006. Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Molecular Cell 23:425-438. doi: 10.1016/j.molcel.2006.05.042.
52. Shorter J, Lindquist S. 2008. Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. The EMBO Journal 27:2712-2724. doi: 10.1038/emboj.2008.194.
53. Suzuki G, Shimazu N, Tanaka M. 2012. A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336:355-359. doi: 10.1126/science.1219491.
54. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS. 2004. Conformational variations in an infectious protein determine prion strain differences. Nature 428:323-328. doi: 10.1038/nature02392.
55. Tanaka M, Weissman JS. 2006. An efficient protein transformation protocol for introducing prions into yeast. Methods in Enzymology 412:185-200. doi: 10.1016/S0076-6879(06)12012-1.
56. Taneja V, Maddelein ML, Talarek N, Saupe SJ, Liebman SW. 2007. A non-Q/N-rich prion domain of a foreign prion, [Het-s], can propagate as a prion in yeast. Molecular Cell 27:67-77. doi: 10.1016/j.molcel.2007.05.027.
57. Ter-Avanesyan MD, Dagkesamanskaya AR, Kushnirov VV, Smirnov VN. 1994. The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics 137:671-676.
58. Ter-Avanesyan MD, Kushnirov VV, Dagkesamanskaya AR, Didichenko SA, Chernoff YO, Inge-Vechtomov SG, Smirnov VN. 1993. Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Molecular Microbiology 7:683-692. doi: 10.1111/j.1365-2958.1993.tb01159.x.
59. Tipton KA, Verges KJ, Weissman JS. 2008. In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Molecular Cell 32:584-591. doi: 10.1016/j.molcel.2008.11.003.
60. True HL, Berlin I, Lindquist SL. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184-187. doi: 10.1038/nature02885.
61. True HL, Lindquist SL. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407:477-483. doi: 10.1038/35035005.
62. Tuite MF, Serio TR. 2010. The prion hypothesis: from biological anomaly to basic regulatory mechanism. Nature Reviews Molecular Cell Biology 11:823-833. doi: 10.1038/nrm3007.
63. Weibezahn J, Schlieker C, Bukau B, Mogk A. 2003. Characterization of a trap mutant of the AAA+ chaperone ClpB. The Journal of Biological Chemistry 278:32608-32617. doi: 10.1074/jbc.M303653200.
64. Weibezahn J, Tessarz P, Schlieker C, Zahn R, Maglica Z, Lee S, Zentgraf H, Weber-Ban EU, Dougan DA, Tsai FT, Mogk A, Bukau B. 2004. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119:653-655. doi: 10.1016/j.cell.2004.11.027.
65. Wickner RB. 1994. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264:566-569. doi: 10.1126/science.7909170.
66. Winkler J, Tyedmers J, Bukau B, Mogk A. 2012. Chaperone networks in protein disaggregation and prion propagation. Journal of Structural Biology 179:152-160. doi: 10.1016/j.jsb.2012.05.002.
67. Zhou P, Derkatch IL, Liebman SW. 2001. The relationship between visible intracellular aggregates that appear after overexpression of Sup35 and the yeast prion-like elements [PSI+] and [PIN+]. Molecular Microbiology 39:37-46. doi: 10.1046/j.1365-2958.2001.02224.x.