Inter-Allelic Prion Propagation Reveals Conformational Relationships among a Multitude of [] Strains
Immense diversity of prion strains is observed, but its underlying mechanism is less clear. Three [PSI] prion strains—named VH, VK, and VL—were previously isolated in the wild-type yeast genetic background. Here we report the generation and characterization of eight new [PSI] isolates, obtained by propagating the wild-type strains with Sup35 proteins containing single amino-acid alterations. The VH strain splits into two distinct strains when propagated in each of the three genetic backgrounds, harboring respectively single mutations of N21L, R28P, and Gi47 (i.e. insertion of a glycine residue at position 47) on the Sup35 N-terminal prion-forming segment. The six new strains exhibit complex inter-conversion patterns, and one of them continuously mutates into another. However, when they are introduced back into the wild-type background, all 6 strains revert to the VH strain. We obtain two more [PSI] isolates by propagating VK and VL with the Gi47 and N21L backgrounds, respectively. The two isolates do not transmit to other mutant backgrounds but revert to their parental strains in the wild-type background. Our data indicate that a large number of [PSI] strains can be built on three basic Sup35 amyloid structures. It is proposed that the three basic structures differ by chain folding topologies, and sub-strains with the same topology differ in distinct ways by local structural adjustments. This “large number of variations on a small number of basic themes” may also be operative in generating strain diversities in other prion elements. It thus suggests a possible general scheme to classify a multitude of prion strains.
Vyšlo v časopise:
Inter-Allelic Prion Propagation Reveals Conformational Relationships among a Multitude of [] Strains. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002297
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002297
Souhrn
Immense diversity of prion strains is observed, but its underlying mechanism is less clear. Three [PSI] prion strains—named VH, VK, and VL—were previously isolated in the wild-type yeast genetic background. Here we report the generation and characterization of eight new [PSI] isolates, obtained by propagating the wild-type strains with Sup35 proteins containing single amino-acid alterations. The VH strain splits into two distinct strains when propagated in each of the three genetic backgrounds, harboring respectively single mutations of N21L, R28P, and Gi47 (i.e. insertion of a glycine residue at position 47) on the Sup35 N-terminal prion-forming segment. The six new strains exhibit complex inter-conversion patterns, and one of them continuously mutates into another. However, when they are introduced back into the wild-type background, all 6 strains revert to the VH strain. We obtain two more [PSI] isolates by propagating VK and VL with the Gi47 and N21L backgrounds, respectively. The two isolates do not transmit to other mutant backgrounds but revert to their parental strains in the wild-type background. Our data indicate that a large number of [PSI] strains can be built on three basic Sup35 amyloid structures. It is proposed that the three basic structures differ by chain folding topologies, and sub-strains with the same topology differ in distinct ways by local structural adjustments. This “large number of variations on a small number of basic themes” may also be operative in generating strain diversities in other prion elements. It thus suggests a possible general scheme to classify a multitude of prion strains.
Zdroje
1. KingCYDiaz-AvalosR 2004 Protein-only transmission of three yeast prion strains. Nature 428 319 323
2. TanakaMChienPNaberNCookeRWeissmanJS 2004 Conformational variations in an infectious protein determine prion strain differences. Nature 428 323 328
3. DerkatchILChernoffYOKushnirovVVInge-VechtomovSGLiebmanSW 1996 Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144 1375 1386
4. ColbyDWGilesKLegnameGWilleHBaskakovIV 2009 Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci U S A 106 20417 20422
5. CoxBSTuiteMFMcLaughlinCS 1988 The psi factor of yeast: a problem in inheritance. Yeast 4 159 178
6. WicknerRB 1994 [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264 566 569
7. KingCY 2001 Supporting the structural basis of prion strains: induction and identification of [PSI] variants. J Mol Biol 307 1247 1260
8. Diaz-AvalosRKingCYWallJSimonMCasparDLD 2005 Strain-specific morphologies of yeast prion amyloid fibrils. Proc Natl Acad Sci U S A 102 10165 10170
9. ToyamaBHKellyMJSGrossJDWeissmanJS 2007 The structural basis of yeast prion strain variants. Nature 449 233 237
10. ChangHYLinJYLeeHCWangHLKingCY 2008 Strain-specific sequences required for yeast [PSI+] prion propagation. Proc Natl Acad Sci U S A 105 13345 13350
11. DickinsonAGOutramGW 1979 The scrapie replication-site hypothesis and its implications for pathogenesis. PrusinerSBHadlowWJ Slow transmissible diseases of the nervous system Vol 2 New York Academic Press 13 31
12. BruceMEDickinsonAG 1979 Biological stability of different classes of scrapie agent. PrusinerSBHadlowWJ Slow transmissible diseases of the nervous system Vol 2 New York Academic Press 71 86
13. BruceMEDickinsonAG 1987 Biological evidence that scrapie agent has an independent genome. J Gen Virol 68 79 89
14. BruceME 1993 Scrapie strain variation and mutation. Br Med Bull 49 822 838
15. CollingeJClarkeARA 2007 General model of prion strains and their pathogenicity. Science 318 930 936
16. MooreRCHopeJMcBridePAMcConnellISelfridgeJ 1998 Mice with gene targeted prion protein alterations show that Prnp, Sinc and Prni are congruent. Nature Genet 18 118 125
17. LiJBrowningSMahalSPOelschlegelAMWeissmannC 2010 Darwinian evolution of prions in cell culture. Science 327 869 872
18. KimberlinRHWalkerCA 1978 Evidence that the transmission of one source of scrapie agent to hamsters involves separation of agent strains from a mixture. J Gen Virol 39 487 496
19. KingCYWangHLChangHY 2006 Transformation of yeast by infectious prion particles. Methods 39 68 71
20. CasparDLD 2009 Inconvenient facts about pathological amyloid fibrils. Proc Natl Acad Sci U S A 106 20555 20556
21. DomingoESaboDTaniguchiTWeissmannC 1978 Nucleotide sequence heterogeneity of an RNA phage population. Cell 13 735 744
22. EigenMSchusterP 1977 The hypercycle. A principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 64 541 565
23. WilkeCOWangJLOfriaCLenskiREAdamiC 2001 Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412 331 333
24. LeVineH 1999 Quantification of β-sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309 274 284
25. BartzJCBessenRAMcKenzieDMarshRFAikenJM 2000 Adaptation and selection of prion protein strain conformations following interspecies transmission of transmissible mink encephalopathy. J Virol 74 5542 5547
26. KimberlinRHColeSWalkerCA 1987 Temporary and permanent modifications to a single strain of mouse scrapie on transmission to rats and hamsters. J Gen Virol 68 1875 1881
27. AngersRCKangHENapierDBrowningSSewardT 2010 Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328 1154 1158
28. DiSalvoSDerdowskiAPezzaJASerioTR 2011 Dominant prion mutants induce curing through pathways that promote chaperone-mediated disaggregation. Nat Struct Biol 18 486 492
29. VergesKJSmithMHToyamaBHWeissmanJS 2011 Strain conformation, primary structure and the propagation of the yeast prion [PSI+]. Nat Struct Biol 18 493 499
30. ChienPWeissmanJSDePaceAH 2004 Emerging principles of conformation-based prion inheritance. Annu Rev Biochem 73 617 656
31. WicknerRBEdskesHKRossEDPierceMMBaxaU 2004 Prion genetics: new rules for a new kind of gene. Annu Rev Genet 38 681 707
32. SawayaMRSambashivanSNelsonRIvanovaMISieversSA 2007 Atomic structures of amyloid cross- β spines reveal varied steric zippers. Nature 447 453 457
33. WasmerCLangeAvan MelckebekeHSiemerABRiekR 2008 Amyloid fibrils of the HET-s(218–289) prion form a β solenoid with a triangular hydrophobic core. Science 319 1523 1526
34. KajavaAVBaxaUStevenAC 2010 Beta arcades: recurring motifs in naturally occurring and disease-related amyloid fibrils. FASEB J 24 1311 1319
35. TanakaMChienPYonekuraKWeissmanJS 2005 Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 121 49 62
36. DerkatchILBradleyMEZhouPChernoffYOLiebmanSW 1997 Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147 507 519
37. VishveshwaraNLiebmanSW 2009 Heterologous cross-seeding mimics cross-species prion conversion in a yeast model. BMC Biol 7 doi:10.1186/1741-7007-7-26
38. ChenBBruceKLNewnamGPGyonevaSRomanyukAV 2010 Genetic and epigenetic control of the efficiency and fidelity of cross-species prion transmission. Mol Microbiol 76 1483 1499
39. ChenBNewnamGPChernoffYO 2007 Prion species barrier between the closely related yeast proteins is detected despite coaggregation. Proc Natl Acad Sci U S A 104 2791 2796
40. AfanasievaEGKushnirovVVTuiteMFTer-AvanesyanMD 2011 Molecular basis for transmission barrier and interference between closely related prion proteins in yeast. J Biol Chem 286 15773 15780
41. McGlincheyRPKryndushkinDWicknerRB 2011 Suicidal [PSI+] is a lethal prion. Proc Natl Acad Sci U S A 108 5337 5341
42. Ter-AvanesyanMDDagkesamanskayaARKushnirovVVSmirnovVN 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
43. ShermanF 1991 Getting started with yeast. Methods Enzymol 194 3 21
44. GietzRDSuginoA 1988 New yeast–Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74 527 534
45. SkerraASchmidtTG 2000 Use of the Strep-tag and streptavidin for detection and purification of recombinant proteins. Methods Enzymol 326 271 304
46. StudierFWRosenbergAHDunnJJDubendorffJW 1990 Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185 60 89
47. KingCYTittmannPGrossHGebertRAebiM 1997 Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc Natl Acad Sci U S A 94 6618 6622
48. GillSCvon HippelPH 1989 Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182 319 326
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 9
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The Evolutionarily Conserved Longevity Determinants HCF-1 and SIR-2.1/SIRT1 Collaborate to Regulate DAF-16/FOXO
- Genome-Wide Analysis of Heteroduplex DNA in Mismatch Repair–Deficient Yeast Cells Reveals Novel Properties of Meiotic Recombination Pathways
- Association of eGFR-Related Loci Identified by GWAS with Incident CKD and ESRD
- MicroRNA Predictors of Longevity in