Propagation of yeast prions

Mick F. Tuite; Brian S. Cox

doi:10.1038/nrm1247

journal article Nov 01, 2003

Propagation of yeast prions

Mick F. Tuite Brian S. Cox

Nature Reviews Molecular Cell Biology Vol. 4 No. 11 pp. 878-890 · Springer Science and Business Media LLC

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References

131

[1]

Prusiner, S. B., Scott, M. R., DeArmond, S. J. & Cohen, F. E. Prion protein biology. Cell 93, 337–348 (1998). 10.1016/s0092-8674(00)81163-0

[2]

Aguzzi, A., Montrasio, F. & Kaeser, P. S. Prions: health scare and biological challenge. Nature Rev. Mol. Cell Biol. 2, 118–126 (2001). 10.1038/35052063

[3]

Wickner, R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566–569 (1994). The authors of this paper suggest — for the first time — that the [ URE3 ] and the [ PSI+] determinants might be prions and provide genetic data that both support this hypothesis for [ URE3 ] and identify the underlying prion protein as Ure2. 10.1126/science.7909170

[4]

Coustou, V., Deleu, C., Saupe, S. & Begueret, J. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc. Natl Acad. Sci. USA 94, 9773–9778 (1997). 10.1073/pnas.94.18.9773

[5]

Eaglestone, S. S., Cox, B. S. & Tuite, M. F. Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO J. 18, 1974–1981 (1999). 10.1093/emboj/18.7.1974

[6]

True, H. L. & Lindquist, S. L. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407, 477–483 (2000). 10.1038/35035005

[7]

Uptain, S. M. & Lindquist, S. Prions as protein-based genetic elements. Ann. Rev. Microbiol. 56, 703–741 (2002). 10.1146/annurev.micro.56.013002.100603

[8]

Wickner, R. B. et al. Yeast prions act as genes composed of self-propagating protein amyloids. Adv. Protein Chem. 57, 313–334 (2001). 10.1016/s0065-3233(01)57026-6

[9]

Prusiner, S. B. Novel proteinaceous infectious particles cause scrapie. Science 216, 136–144 (1982). 10.1126/science.6801762

[10]

Cox, B. S. [PSI], a cytoplasmic suppressor of super-suppressors in yeast. Heredity 20, 505–521 (1965). 10.1038/hdy.1965.65

[11]

Lacroute, F. Non-Mendelian mutation allowing ureidosuccinic acid uptake in yeast. J. Bacteriol. 106, 519–522 (1971). 10.1128/jb.106.2.519-522.1971

[12]

Aigle, M. & Lacroute, F. Genetical aspects of [URE3], a non-Mendelian, cytoplasmically-inherited mutation in yeast. Mol. Gen. Genet. 136, 327–335 (1975). 10.1007/bf00341717

[13]

Cox, K. H. et al. Saccharomyces cerevisiae GATA sequences function as TATA elements during nitrogen catabolite repression and when Gln3p is excluded from the nucleus by overproduction of Ure2p. J. Biol. Chem. 275, 17611–17618 (2000). 10.1074/jbc.m001648200

[14]

Kulkarni, A. A., Abul-Hamd, A. T., Rai, R., El Berry, H. & Cooper, T. G. Gln3p nuclear localization and interaction with Ure2p in Saccharomyces cerevisiae. J. Biol. Chem. 276, 32136–32144 (2001). 10.1074/jbc.m104580200

[15]

Cox, B. S. A recessive lethal super-suppressor mutation in yeast and other psi phenomena. Heredity 26, 211–232 (1971). 10.1038/hdy.1971.28

[16]

Patino, M. M., Liu, J. J., Glover, J. R. & Lindquist, S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273, 622–626 (1996). In addition to showing that Sup35 undergoes an Hsp104-dependent change in state in [ PSI+] cells, the authors also show for the first time that the Sup35 prion-forming domain is modular and can transfer prion properties to another protein — in this case, green fluorescent protein (see also reference 17). 10.1126/science.273.5275.622

[17]

Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N. & Ter-Avanesyan, M. D. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15, 3127–3134 (1996). The first demonstration that Sup35 aggregation occurs in a [ PSI+]-dependent manner. Also provides data to support the theory that Hsp104 disrupts these aggregates to ensure effective transmission of the prion form of Sup35 during cell division (see also reference 16). 10.1002/j.1460-2075.1996.tb00675.x

[18]

Stansfield, I. et al. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14, 4365–4373 (1995). 10.1002/j.1460-2075.1995.tb00111.x

[19]

Sondheimer, N. & Lindquist, S. Rnq1: an epigenetic modifier of protein function in yeast. Mol. Cell 5, 163–172 (2000). 10.1016/s1097-2765(00)80412-8

[20]

Osherovich, L. Z. & Weissman, J. S. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI+] prion. Cell 106, 183–194 (2001). In demonstrating that the aggregation of the QN-rich regions of two proteins New1 and Rnq1 allow for high-level de novo formation of prion-like aggregates of Sup35, the authors provide an explanation for the molecular basis of the [ PIN+] effect (see also reference 73). 10.1016/s0092-8674(01)00440-8

[21]

Prusiner, S. B. et al. Further purification and characterization of scrapie prions. Biochemistry 21, 6942–6950 (1982). 10.1021/bi00269a050

[22]

Prusiner, S. B. et al. Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35, 349–358 (1983). 10.1016/0092-8674(83)90168-x

[23]

Masison, D. C. & Wickner, R. B. Prion-inducing domain of yeast Ure2p and protease resistance of Ure2p in prion-containing cells. Science 270, 93–95 (1995). The authors show that the Ure2 protein has a 'prion-inducing domain' at its amino terminus that is functionally distinct from the remainder of the protein and show a role for this domain in the regulation of nitrogen assimilation. 10.1126/science.270.5233.93

[24]

Taylor, K. L., Cheng, N., Williams, R. W., Steven, A. C. & Wickner, R. B. Prion domain initiation of amyloid formation in vitro from native Ure2p. Science 283, 1339–1343 (1999). 10.1126/science.283.5406.1339

[25]

Schlumpberger, M. et al. The prion domain of yeast Ure2p induces autocatalytic formation of amyloid fibers by a recombinant fusion protein. Protein Sci. 9, 440–451 (2000). 10.1110/ps.9.3.440

[26]

Glover, J. R. et al. Self-seeded fibers formed by Sup35, the protein determinant of PSI+, a heritable prion-like factor of S. cerevisiae. Cell 89, 811–819 (1997). By showing that Sup35 in vitro forms protein fibres that have all the biophysical properties of an amyloid, the authors establish that the yeast prion shows remarkably similar properties to a number of proteins implicated in human amyloidoses including transmissible spongiform encephalopathies. 10.1016/s0092-8674(00)80264-0

[27]

King, C. Y. et al. Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc. Natl Acad. Sci. USA 94, 6618–6622 (1997). 10.1073/pnas.94.13.6618

[28]

Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N. & Ter-Avanesyan, M. D. In vitro propagation of the prion-like state of yeast Sup35 protein. Science 277, 381–383 (1997). Provides evidence that the aggregated form of Sup35 can seed the polymerization of soluble Sup35 through several consecutive cycles, thereby providing support for the 'protein-only' hypothesis for prion propagation in yeast. 10.1126/science.277.5324.381

[29]

Sparrer, H. E., Santoso, A., Szoka, F. C. & Weissman, J. S. Evidence for the prion hypothesis: induction of the yeast [PSI+] factor by in vitro-converted Sup35 protein. Science 289, 595–599 (2000). 10.1126/science.289.5479.595

[30]

Maddelein, M. L., Dos Reis, S., Duvezin-Caubet, S., Coulary-Salin, B. & Saupe, S. J. Amyloid aggregates of the HET-s prion protein are infectious. Proc. Natl Acad. Sci. USA 99, 7402–7407 (2002). 10.1073/pnas.072199199

[31]

Michelitsch, M. D. & Weissman, J. S. A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc. Natl Acad. Sci. USA 97, 11910–11915 (2000). 10.1073/pnas.97.22.11910

[32]

Nakayashiki, T., Ebihara, K., Bannai, H. & Nakamura, Y. Yeast [PSI+] 'prions' that are cross-transmissible and susceptible beyond a species barrier through a quasi-prion state. Mol. Cell 7, 1121–1130 (2001). 10.1016/s1097-2765(01)00259-3

[33]

Ter-Avanesyan, M. D., Dagkesamanskaya, A. R., Kushnirov, V. V. & Smirnov, V. N. 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 (1994). The first demonstration that the maintenance of the [ PSI+] prion requires the amino-terminal 114 amino acids of Sup35, thereby providing crucial evidence that Sup35 and the [ PSI+] prion are in some way linked (see also reference 53). 10.1093/genetics/137.3.671

[34]

Masison, D. C., Maddelein, M. L. & Wickner, R. B. The prion model for [URE3] of yeast: spontaneous generation and requirements for propagation. Proc. Natl Acad. Sci. USA 94, 12503–12508 (1997). 10.1073/pnas.94.23.12503

[35]

Tuite, M. F. Yeast prions and their prion-forming domain. Cell 100, 289–292 (2000). 10.1016/s0092-8674(00)80663-7

[36]

Li, L. & Lindquist, S. Creating a protein-based element of inheritance. Science 287, 661–664 (2000). 10.1126/science.287.5453.661

[37]

Maddelein, M. L. & Wickner, R. B. Two prion-inducing regions of Ure2p are non-overlapping. Mol. Cell. Biol. 19, 4516–4524 (1999). 10.1128/mcb.19.6.4516

[38]

Baxa, U., Speransky, V., Steven, A. C. & Wickner, R. B. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl Acad. Sci. USA 99, 5253–5260 (2002). 10.1073/pnas.082097899

[39]

Lund, P. M. & Cox, B. S. Reversion analysis of [psi−] mutations in Saccharomyces cerevisiae. Genet. Res. 37, 173–182 (1981). 10.1017/s0016672300020140

[40]

Liu, J. J. & Lindquist, S. Oligopeptide-repeat expansions modulate 'protein-only' inheritance in yeast. Nature 400, 573–576 (1999). 10.1038/23048

[41]

Derkatch, I. L., Chernoff, Y. O., Kushnirov, V. V., Inge-Vechtomov, S. G. & Liebman, S. W. Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144, 1375–1386 (1996). The authors show that overexpression of the amino-terminal region of Sup35 can induce de novo different, but stable, [ PSI+] prions and conclude that these different states might be analogous to the 'strains' reported for mammalian prions. 10.1093/genetics/144.4.1375

[42]

Derkatch, I. L., Bradley, M. E., Zhou, P., Chernoff, Y. O. & Liebman, S. W. Genetic and environmental factors affecting the de novo appearance of the PSI+ prion in Saccharomyces cerevisiae. Genetics 147, 507–519 (1997). 10.1093/genetics/147.2.507

[43]

Fernandez-Bellot, E., Guillemet, E. & Cullin, C. The yeast prion [URE3] can be greatly induced by a functional mutated URE2 allele. EMBO J. 19, 3215–3222 (2000). 10.1093/emboj/19.13.3215

[44]

Parham, S. N., Resende, C. G. & Tuite, M. F. Oligopeptide repeats in the yeast protein Sup35p stabilize intermolecular prion interactions. EMBO J. 20, 2111–2119 (2001). 10.1093/emboj/20.9.2111

[45]

Liu, J. J., Sondheimer, N. & Lindquist, S. L. Changes in the middle region of Sup35 profoundly alter the nature of epigenetic inheritance for the yeast prion [PSI+]. Proc. Natl Acad. Sci. USA 99, 16446–16453 (2002). 10.1073/pnas.252652099

[46]

DePace, A. H., Santoso, A., Hillner, P. & Weissman, J. S. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93, 1241–1252 (1998). 10.1016/s0092-8674(00)81467-1

[47]

Young, C. S. H. & Cox, B. S. Extrachromosomal elements in a super-suppression system of yeast. I. A nuclear gene controlling the inheritance of the extrachromosomal elements. Heredity 26, 413–422 (1971). 10.1038/hdy.1971.52

[48]

Kochneva-Pervukhova, N. V. et al. Mechanism of inhibition of Psi(+) prion determinant propagation by a mutation of the N-terminus of the yeast Sup35 protein. EMBO J. 17, 5805–5810 (1998). 10.1093/emboj/17.19.5805

[49]

McCready, S. J., Cox, B. S. & McLaughlin, C. S. The extrachromosomal control of nonsense suppression in yeast: an analysis of the elimination of [psi+] in the presence of a nuclear gene PNM. Mol. Gen. Genet. 150, 265–270 (1977). 10.1007/bf00268125

[50]

Kushnirov, V. V. et al. Nucleotide sequence of the Sup2 (Sup35) Gene of Saccharomyces cerevisiae. Gene 66, 45–54 (1988). 10.1016/0378-1119(88)90223-5

Showing 50 of 131 references

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Published: Nov 01, 2003
Vol/Issue: 4(11)
Pages: 878-890
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Cite This Article

Mick F. Tuite, Brian S. Cox (2003). Propagation of yeast prions. Nature Reviews Molecular Cell Biology, 4(11), 878-890. https://doi.org/10.1038/nrm1247

Propagation of yeast prions

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