Abstract
Two cytoplasmically inherited determinants related by their manifestation to the control of translation accuracy were previously described in yeast. Cells carrying one of them, [PSI(+)], display a nonsense suppressor phenotype and contain a prion form of the Sup35 protein. Another element, [PIN(+)], determines the probability of de novo generation of [PSI(+)] and results from a prion form of several proteins, which can be functionally unrelated to Sup35p. Here we describe a novel nonchromosomal determinant related to the SUP35 gene. This determinant, designated [ISP(+)], was identified as an antisuppressor of certain sup35 mutations. We observed its loss upon growth on guanidine hydrochloride and subsequent spontaneous reappearance with high frequency. The reversible curability of [ISP(+)] resembles the behavior of yeast prions. However, in contrast to known prions, [ISP(+)] does not depend on the chaperone protein Hsp104. Though manifestation of both [ISP(+)] and [PSI(+)] is related to the SUP35 gene, the maintenance of [ISP(+)] does not depend on the prionogenic N-terminal domain of Sup35p and Sup35p is not aggregated in [ISP(+)] cells, thus ruling out the possibility that [ISP(+)] is a specific form of [PSI(+)]. We hypothesize that [ISP(+)] is a novel prion involved in the control of translation accuracy in yeast.
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- Bailleul P. A., Newnam G. P., Steenbergen J. N., Chernoff Y. O. Genetic study of interactions between the cytoskeletal assembly protein sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics. 1999 Sep;153(1):81–94. doi: 10.1093/genetics/153.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
- Chen X. J., Clark-Walker G. D. The petite mutation in yeasts: 50 years on. Int Rev Cytol. 2000;194:197–238. doi: 10.1016/s0074-7696(08)62397-9. [DOI] [PubMed] [Google Scholar]
- Chernoff Y. O., Derkach I. L., Inge-Vechtomov S. G. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr Genet. 1993 Sep;24(3):268–270. doi: 10.1007/BF00351802. [DOI] [PubMed] [Google Scholar]
- Cox B. S., Tuite M. F., McLaughlin C. S. The psi factor of yeast: a problem in inheritance. Yeast. 1988 Sep;4(3):159–178. doi: 10.1002/yea.320040302. [DOI] [PubMed] [Google Scholar]
- Czaplinski K., Majlesi N., Banerjee T., Peltz S. W. Mtt1 is a Upf1-like helicase that interacts with the translation termination factors and whose overexpression can modulate termination efficiency. RNA. 2000 May;6(5):730–743. doi: 10.1017/s1355838200992392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Czaplinski K., Ruiz-Echevarria M. J., Paushkin S. V., Han X., Weng Y., Perlick H. A., Dietz H. C., Ter-Avanesyan M. D., Peltz S. W. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 1998 Jun 1;12(11):1665–1677. doi: 10.1101/gad.12.11.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Derkatch I. L., Bradley M. E., Masse S. V., Zadorsky S. P., Polozkov G. V., Inge-Vechtomov S. G., Liebman S. W. Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast? EMBO J. 2000 May 2;19(9):1942–1952. doi: 10.1093/emboj/19.9.1942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1997 Oct;147(2):507–519. doi: 10.1093/genetics/147.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1996 Dec;144(4):1375–1386. doi: 10.1093/genetics/144.4.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doel S. M., McCready S. J., Nierras C. R., Cox B. S. The dominant PNM2- mutation which eliminates the psi factor of Saccharomyces cerevisiae is the result of a missense mutation in the SUP35 gene. Genetics. 1994 Jul;137(3):659–670. doi: 10.1093/genetics/137.3.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eaglestone S. S., Ruddock L. W., Cox B. S., Tuite M. F. Guanidine hydrochloride blocks a critical step in the propagation of the prion-like determinant [PSI(+)] of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):240–244. doi: 10.1073/pnas.97.1.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gietz D., St Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992 Mar 25;20(6):1425–1425. doi: 10.1093/nar/20.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldring E. S., Grossman L. I., Krupnick D., Cryer D. R., Marmur J. The petite mutation in yeast. Loss of mitochondrial deoxyribonucleic acid during induction of petites with ethidium bromide. J Mol Biol. 1970 Sep 14;52(2):323–335. doi: 10.1016/0022-2836(70)90033-1. [DOI] [PubMed] [Google Scholar]
- Horwich A. L., Weissman J. S. Deadly conformations--protein misfolding in prion disease. Cell. 1997 May 16;89(4):499–510. doi: 10.1016/s0092-8674(00)80232-9. [DOI] [PubMed] [Google Scholar]
- Inge-Vechtomov S. G., Tikhodeev O. N., Karpova T. S. Selektivnye sistemy dlia polucheniia retsessivnykh ribosomnykh supressorov u drozhzhei sakharomitsetov. Genetika. 1988 Jul;24(7):1159–1165. [PubMed] [Google Scholar]
- Kushnirov V. V., Kochneva-Pervukhova N. V., Chechenova M. B., Frolova N. S., Ter-Avanesyan M. D. Prion properties of the Sup35 protein of yeast Pichia methanolica. EMBO J. 2000 Feb 1;19(3):324–331. doi: 10.1093/emboj/19.3.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kushnirov V. V., Kryndushkin D. S., Boguta M., Smirnov V. N., Ter-Avanesyan M. D. Chaperones that cure yeast artificial [PSI+] and their prion-specific effects. Curr Biol. 2000 Nov 16;10(22):1443–1446. doi: 10.1016/s0960-9822(00)00802-2. [DOI] [PubMed] [Google Scholar]
- Kushnirov V. V., Ter-Avanesian M. D., Dagkesamanskaia A. R., Chernov Iu O., Inge-Vechtomov S. G., Smirnov V. N. Deletsionnyi analiz gena SUP2 drozhzhei Saccharomyces cerevisiae. Mol Biol (Mosk) 1990 Jul-Aug;24(4):1037–1041. [PubMed] [Google Scholar]
- Liebman S. W., Derkatch I. L. The yeast [PSI+] prion: making sense of nonsense. J Biol Chem. 1999 Jan 15;274(3):1181–1184. doi: 10.1074/jbc.274.3.1181. [DOI] [PubMed] [Google Scholar]
- Lindquist S., Kim G. Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5301–5306. doi: 10.1073/pnas.93.11.5301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Masison D. C., Wickner R. B. Prion-inducing domain of yeast Ure2p and protease resistance of Ure2p in prion-containing cells. Science. 1995 Oct 6;270(5233):93–95. doi: 10.1126/science.270.5233.93. [DOI] [PubMed] [Google Scholar]
- 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 U S A. 2000 Oct 24;97(22):11910–11915. doi: 10.1073/pnas.97.22.11910. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moriyama H., Edskes H. K., Wickner R. B. [URE3] prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol Cell Biol. 2000 Dec;20(23):8916–8922. doi: 10.1128/mcb.20.23.8916-8922.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ono B., Ishino-Arao Y., Tanaka M., Awano I., Shinoda S. Recessive nonsense suppressors in Saccharomyces cerevisiae: action spectra, complementation groups and map positions. Genetics. 1986 Oct;114(2):363–374. doi: 10.1093/genetics/114.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Osherovich L. Z., Weissman J. S. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell. 2001 Jul 27;106(2):183–194. doi: 10.1016/s0092-8674(01)00440-8. [DOI] [PubMed] [Google Scholar]
- Paushkin S. V., Kushnirov V. V., Smirnov V. N., Ter-Avanesyan M. D. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Mol Cell Biol. 1997 May;17(5):2798–2805. doi: 10.1128/mcb.17.5.2798. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1996 Jun 17;15(12):3127–3134. [PMC free article] [PubMed] [Google Scholar]
- Rosche W. A., Foster P. L. Determining mutation rates in bacterial populations. Methods. 2000 Jan;20(1):4–17. doi: 10.1006/meth.1999.0901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanger F., Coulson A. R. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol. 1975 May 25;94(3):441–448. doi: 10.1016/0022-2836(75)90213-2. [DOI] [PubMed] [Google Scholar]
- Serio T. R., Lindquist S. L. Protein-only inheritance in yeast: something to get [PSI+]-ched about. Trends Cell Biol. 2000 Mar;10(3):98–105. doi: 10.1016/s0962-8924(99)01711-0. [DOI] [PubMed] [Google Scholar]
- Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stansfield I., Jones K. M., Kushnirov V. V., Dagkesamanskaya A. R., Poznyakovski A. I., Paushkin S. V., Nierras C. R., Cox B. S., Ter-Avanesyan M. D., Tuite M. F. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 1995 Sep 1;14(17):4365–4373. doi: 10.1002/j.1460-2075.1995.tb00111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tallóczy Z., Mazar R., Georgopoulos D. E., Ramos F., Leibowitz M. J. The [KIL-d] element specifically regulates viral gene expression in yeast. Genetics. 2000 Jun;155(2):601–609. doi: 10.1093/genetics/155.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tallóczy Z., Menon S., Neigeborn L., Leibowitz M. J. The [KIL-d] cytoplasmic genetic element of yeast results in epigenetic regulation of viral M double-stranded RNA gene expression. Genetics. 1998 Sep;150(1):21–30. doi: 10.1093/genetics/150.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1994 Jul;137(3):671–676. doi: 10.1093/genetics/137.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1994 Jul;137(3):671–676. doi: 10.1093/genetics/137.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ter-Avanesyan M. D., Kushnirov V. V., Dagkesamanskaya A. R., Didichenko S. A., Chernoff Y. O., Inge-Vechtomov S. G., Smirnov V. N. Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol. 1993 Mar;7(5):683–692. doi: 10.1111/j.1365-2958.1993.tb01159.x. [DOI] [PubMed] [Google Scholar]
- Tuite M. F., Mundy C. R., Cox B. S. Agents that cause a high frequency of genetic change from [psi+] to [psi-] in Saccharomyces cerevisiae. Genetics. 1981 Aug;98(4):691–711. doi: 10.1093/genetics/98.4.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Von Borstel R. C. Measuring spontaneous mutation rates in yeast. Methods Cell Biol. 1978;20:1–24. doi: 10.1016/s0091-679x(08)62005-1. [DOI] [PubMed] [Google Scholar]
- Wickner R. B. Double-stranded and single-stranded RNA viruses of Saccharomyces cerevisiae. Annu Rev Microbiol. 1992;46:347–375. doi: 10.1146/annurev.mi.46.100192.002023. [DOI] [PubMed] [Google Scholar]
- Wickner R. B., Taylor K. L., Edskes H. K., Maddelein M. L., Moriyama H., Roberts B. T. Prions in Saccharomyces and Podospora spp.: protein-based inheritance. Microbiol Mol Biol Rev. 1999 Dec;63(4):844-61, table of contents. doi: 10.1128/mmbr.63.4.844-861.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wickner R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science. 1994 Apr 22;264(5158):566–569. doi: 10.1126/science.7909170. [DOI] [PubMed] [Google Scholar]
- Yeast J. D., Garite T. R. The role of cervical cerclage in the management of preterm premature rupture of the membranes. Am J Obstet Gynecol. 1988 Jan;158(1):106–110. doi: 10.1016/0002-9378(88)90788-0. [DOI] [PubMed] [Google Scholar]
- Zhou P., Derkatch I. L., Uptain S. M., Patino M. M., Lindquist S., Liebman S. W. The yeast non-Mendelian factor [ETA+] is a variant of [PSI+], a prion-like form of release factor eRF3. EMBO J. 1999 Mar 1;18(5):1182–1191. doi: 10.1093/emboj/18.5.1182. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhouravleva G., Frolova L., Le Goff X., Le Guellec R., Inge-Vechtomov S., Kisselev L., Philippe M. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 1995 Aug 15;14(16):4065–4072. doi: 10.1002/j.1460-2075.1995.tb00078.x. [DOI] [PMC free article] [PubMed] [Google Scholar]