DOI QR코드

DOI QR Code

Heterogeneous interaction network of yeast prions and remodeling factors detected in live cells

  • Pack, Chan-Gi (Asan Institute for Life Sciences, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Inoue, Yuji (Department of Biomolecular Engineering, Graduate School of Biosciences and Biotechnology, Tokyo Institute of Technology) ;
  • Higurashi, Takashi (Department of Biochemistry, University of Wisconsin) ;
  • Kawai-Noma, Shigeko (Department of Biomolecular Engineering, Graduate School of Biosciences and Biotechnology, Tokyo Institute of Technology) ;
  • Hayashi, Daigo (Department of Biomolecular Engineering, Graduate School of Biosciences and Biotechnology, Tokyo Institute of Technology) ;
  • Craig, Elizabeth (Department of Biochemistry, University of Wisconsin) ;
  • Taguchi, Hideki (Department of Biomolecular Engineering, Graduate School of Biosciences and Biotechnology, Tokyo Institute of Technology)
  • Received : 2017.05.24
  • Accepted : 2017.08.31
  • Published : 2017.09.30

Abstract

Budding yeast has dozens of prions, which are mutually dependent on each other for the de novo prion formation. In addition to the interactions among prions, transmissions of prions are strictly dependent on two chaperone systems: the Hsp104 and the Hsp70/Hsp40 (J-protein) systems, both of which cooperatively remodel the prion aggregates to ensure the multiplication of prion entities. Since it has been postulated that prions and the remodeling factors constitute complex networks in cells, a quantitative approach to describe the interactions in live cells would be required. Here, the researchers applied dual-color fluorescence cross-correlation spectroscopy to investigate the molecular network of interaction in single live cells. The findings demonstrate that yeast prions and remodeling factors constitute a network through heterogeneous protein-protein interactions.

Keywords

References

  1. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95, 13363-13383 https://doi.org/10.1073/pnas.95.23.13363
  2. Wickner RB (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566-569 https://doi.org/10.1126/science.7909170
  3. Tuite MF and Cox BS (2003) Propagation of yeast prions. Nat Rev Mol Cell Biol 4, 878-890 https://doi.org/10.1038/nrm1247
  4. Tuite MF and Serio TR (2010) The prion hypothesis: from biological anomaly to basic regulatory mechanism. Nat Rev Mol Cell Biol 11, 823-833
  5. Wickner RB, Edskes HK, Shewmaker F et al (2007) Yeast prions: evolution of the prion concept. Prion 1, 94-100 https://doi.org/10.4161/pri.1.2.4664
  6. Inoue Y (2009) Life cycle of yeast prions: propagation mediated by amyloid fibrils. Protein Pept Lett 16, 271-276 https://doi.org/10.2174/092986609787601796
  7. Taguchi H and Kawai-Noma S (2010) Amyloid oligomers: diffuse oligomer-based transmission of yeast prions. FEBS J 277, 1359-1368 https://doi.org/10.1111/j.1742-4658.2010.07569.x
  8. Liebman SW and Chernoff YO (2012) Prions in yeast. Genetics 191, 1041-1072 https://doi.org/10.1534/genetics.111.137760
  9. Sondheimer N and Lindquist S (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5, 163-172 https://doi.org/10.1016/S1097-2765(00)80412-8
  10. Derkatch IL, Bradley ME, Hong JY and Liebman SW (2001) Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106, 171-182 https://doi.org/10.1016/S0092-8674(01)00427-5
  11. Osherovich LZ and Weissman JS (2001) Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106, 183-194 https://doi.org/10.1016/S0092-8674(01)00440-8
  12. Du Z, Park KW, Yu H, Fan Q and Li L (2008) Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat Genet 40, 460-465 https://doi.org/10.1038/ng.112
  13. Alberti S, Halfmann R, King O, Kapila A and Lindquist S (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137, 146-158 https://doi.org/10.1016/j.cell.2009.02.044
  14. Suzuki G, Shimazu N and Tanaka M (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336, 355-359 https://doi.org/10.1126/science.1219491
  15. Bradley ME, Edskes HK, Hong JY, Wickner RB and Liebman SW (2002) Interactions among prions and prion "strains" in yeast. Proc Natl Acad Sci U S A 99 Suppl 4, 16392-16399 https://doi.org/10.1073/pnas.152330699
  16. Bosl B, Grimminger V and Walter S (2006) The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J Struct Biol 156, 139-148 https://doi.org/10.1016/j.jsb.2006.02.004
  17. Doyle SM and Wickner S (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34, 40-48 https://doi.org/10.1016/j.tibs.2008.09.010
  18. Masison DC, Kirkland PA and Sharma D (2009) Influence of Hsp70s and their regulators on yeast prion propagation. Prion 3, 65-73 https://doi.org/10.4161/pri.3.2.9134
  19. Aron R, Higurashi T, Sahi C and Craig EA (2007) J-protein co-chaperone Sis1 required for generation of [RNQ+] seeds necessary for prion propagation. EMBO J 26, 3794-3803 https://doi.org/10.1038/sj.emboj.7601811
  20. Higurashi T, Hines JK, Sahi C, Aron R and Craig EA (2008) Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci U S A 105, 16596-16601 https://doi.org/10.1073/pnas.0808934105
  21. Shorter J and Lindquist S (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J 27, 2712-2724 https://doi.org/10.1038/emboj.2008.194
  22. Romanova NV and Chernoff YO (2009) Hsp104 and prion propagation. Protein Pept Lett 16, 598-605 https://doi.org/10.2174/092986609788490078
  23. Winkler J, Tyedmers J, Bukau B and Mogk A (2012) Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 179, 152-160 https://doi.org/10.1016/j.jsb.2012.05.002
  24. Allen KD, Wegrzyn RD, Chernova TA et al (2005) Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI+]. Genetics 169, 1227-1242 https://doi.org/10.1534/genetics.104.037168
  25. Bagriantsev SN, Gracheva EO, Richmond JE and Liebman SW (2008) Variant-specific [PSI+] infection is transmitted by Sup35 polymers within [PSI+] aggregates with heterogeneous protein composition. Mol Biol Cell 19, 2433-2443 https://doi.org/10.1091/mbc.E08-01-0078
  26. Salnikova AB, Kryndushkin DS, Smirnov VN, Kushnirov VV and Ter-Avanesyan MD (2005) Nonsense suppression in yeast cells overproducing Sup35 (eRF3) is caused by its non-heritable amyloids. J Biol Chem 280, 8808-8812 https://doi.org/10.1074/jbc.M410150200
  27. Derkatch IL, Uptain SM, Outeiro TF, Krishnan R, Lindquist SL and Liebman SW (2004) Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. Proc Natl Acad Sci U S A 101, 12934-12939 https://doi.org/10.1073/pnas.0404968101
  28. Kaganovich D, Kopito R and Frydman J (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095 https://doi.org/10.1038/nature07195
  29. Winkler J, Tyedmers J, Bukau B and 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
  30. Saibil HR, Seybert A, Habermann A et al (2012) Heritable yeast prions have a highly organized three-dimensional architecture with interfiber structures. Proc Natl Acad Sci U S A 109, 14906-14911 https://doi.org/10.1073/pnas.1211976109
  31. Kawai-Noma S, Ayano S, Pack CG et al (2006) Dynamics of yeast prion aggregates in single living cells. Genes Cells 11, 1085-1096 https://doi.org/10.1111/j.1365-2443.2006.01004.x
  32. Kawai-Noma S, Pack CG, Kojidani T et al (2010) In vivo evidence for the fibrillar structures of Sup35 prions in yeast cells. J Cell Biol 190, 223-231 https://doi.org/10.1083/jcb.201002149
  33. Kawai-Noma S, Pack CG, Tsuji T, Kinjo M and Taguchi H (2009) Single mother-daughter pair analysis to clarify the diffusion properties of yeast prion Sup35 in guanidine- HCl-treated [PSI] cells. Genes Cells 14, 1045-1054 https://doi.org/10.1111/j.1365-2443.2009.01333.x
  34. Greene LE, Park YN, Masison DC and Eisenberg E (2009) Application of GFP-labeling to study prions in yeast. Protein Pept Lett 16, 635-641 https://doi.org/10.2174/092986609788490221
  35. Pack CG, Yukii H, Toh-e A et al (2014) Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome. Nat Commun 5, 3396 https://doi.org/10.1038/ncomms4396

Cited by

  1. Protein Co-Aggregation Related to Amyloids: Methods of Investigation, Diversity, and Classification vol.19, pp.8, 2018, https://doi.org/10.3390/ijms19082292
  2. Impact of ConcanavalinA affinity in the intracellular fate of Protein Corona on Glucosamine Au nanoparticles vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-27418-w