From past to future: suppressor mutations in yeast genes encoding translation termination factors
DOI:
https://doi.org/10.21638/spbu03.2019.202Abstract
The study of the SUP45 and SUP35 genes of yeast Saccharomyces cerevisiae in the laboratory of Physiological Genetics of St. Petersburg State University began in 1964 when the first omnipotent nonsense suppressor mutations were obtained. During the following 55 years, a lot of information about these genes has been gained through the research efforts of various laboratories. Now we know that SUP45 and SUP35 encode translation termination factors eRF1 and eRF3, respectively. Both genes are essential, and sup45 and sup35 mutations lead not only to impaired translation but also to multiple pleiotropic effects. The aim of this review is to summarize known data about suppressor mutations in SUP45 or SUP35 genes.
Keywords:
translation termination, suppression, SUP45, SUP35, eRF1, eRF3, nonsense mutations, missense mutations, [PSI ] prion, S. cerevisiae
Downloads
Download data is not yet available.
References
Akhmaloka, P. E. S. and Subandi, F. M. 2008. Mutation at tyrosine in AMLRY (GILRY like) motif of yeast eRF1 on nonsense codons suppression and binding affinity to eRF3. International journal of biological sciences 4(2):87. https://doi.org/10.7150/ijbs.4.87
Aksenova, A. Y., Volkov, K. V., Rovinsky, N. S., Svitin, A. V., and Mironova, L. N. 2006. Phenotypic expression of epigenetic determinant [ISP+] in Saccharomyces cerevisiae depends on the combination of sup35 and sup45 mutations. Molecular Biology 40(5):758–763. https://doi.org/10.1134/S0026893306050104
Alkalaeva, E. Z., Pisarev, A. V., Frolova, L. Y., Kisselev, L. L., and Pestova, T. V. 2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell 125:1125–1136. https://doi.org/10.1016/j.cell.2006.04.035
All-Robyn, J. A., Kelley-Geraghty, D., Griffin, E., Brown, N., and Liebman, S. W. 1990. Isolation of omnipotent suppressors in an [eta+] yeast strain. Genetics 124:505–514.
Atkinson, G. C., Baldauf, S. L., and Hauryliuk, V. 2008. Evolution of nonstop, no-go and nonsense-mediated mRNA decay and their termination factor-derived components. BMC Evolutionary Biology 8(1):290. https://doi.org/10.1186/1471-2148-8-290
Beaudet, A. L. and Caskey, C. T. 1971. Mammalian peptide chain termination, II. Codon specificity and GTPase activity of release factor. Proceedings of the National Academy of Sciences USA 68:619–624. https://doi.org/10.1073/pnas.68.3.619
Beier, H. and Grimm, M. 2001. Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Research 29:4767–4782. https://doi.org/10.1093/nar/29.23.4767
Bertram, G., Bell, H. A., Ritchie, D. W., Fullerton, G., and Stansfield, I. 2000. Terminating eukaryote translation: domain 1 of release factor eRF1 functions in stop codon recognition. RNA 6:1236–1247. https://doi.org/10.1017/S1355838200000777
Bertram, G., Innes, S., Minella, O., Richardson, J. P., and Stansfield, I. 2001. Endless possibilities: Translation termination and stop codon recognition. Microbiology 147:255–269. https://doi.org/10.1099/00221287-147-2-255
Betney, R., de Silva, E., Mertens, C., Knox, Y., Krishnan, J., and Stansfield, I. 2012. Regulation of release factor expression using a translational negative feedback loop: a systems analysis. RNA 18:2320–2334. https://doi.org/10.1261/rna.035113.112
Bidou, L., Stahl, G., Hatin, I., Namy, O., Rousset, J.-P., and Farabaugh, P. J. 2000. Nonsense-mediated decay mutants do not affect programmed −1 frameshifting. RNA 6:952–961. https://doi.org/10.1017/S1355838200000443
Bonetti, B., Fu, L., Moon, J., and Bedwell, D. M. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. Journal of Molecular Biololgy 251:334–345. https://doi.org/10.1006/jmbi.1995.0438
Bradley, M. E., Bagriantsev, S., Vishveshwara, N., and Liebman, S. W. 2003. Guanidine reduces stop codon read-through caused by missense mutations in SUP35 or SUP45. Yeast 20:625–632. https://doi.org/10.1002/yea.985
Breining, P., Surguchov, A.P., and Piepersberg, W. 1984. Cloning and identification of a DNA fragment coding for the sup1 gene of Saccharomyces cerevisiae. Current Genetics 8:467–470. https://doi.org/10.1007/BF00433913
Breining, P. and Piepersberg, W. 1986. Yeast omnipotent supressor SUP1 (SUP45): nucleotide sequence of the wild type and a mutant gene. Nucleic Acids Res 14:5187–5197. https://doi.org/10.1093/nar/14.13.5187
Carr-Schmid, A., Durko, N., Cavallius, J., Merrick, W. C., and Kinzy, T. G. 1999. Mutations in a GTP-binding motif of eukaryotic elongation factor 1A reduce both translational fidelity and the requirement for nucleotide exchange. Journal of Molecular Biololgy 274:30297–30302. https://doi.org/10.1074/jbc.274.42.30297
Cassan, M. and Rousset, J.-P. 2001. UAG readthrough in mammalian cells: effect of upstream and downstream stop codon contexts reveal different signals. BMC Molecular Biology 2:3. https://doi.org/10.1186/1471-2199-2-3
Chabelskaya, S., Kiktev, D., Inge-Vechtomov, S., Philippe, M., and Zhouravleva, G. 2004. Nonsense mutations in the essential gene SUP35 of Saccharomyces cerevisiae are non-lethal. Molecular Genetics and Genomics 272:297–307. https://doi.org/10.1007/s00438-004-1053-1
Chapman, B. and Brown, C. 2004. Translation termination in Arabidopsis thaliana: characterisation of three versions of release factor 1. Gene 341:219–225. https://doi.org/10.1016/j.gene.2004.06.053
Chavatte, L., Frolova, L., Kisselev, L., and Favre, A. 2001. The polypeptide chain release factor eRF1 specifically contacts the s4UGA stop codon located in the A site of eukaryotic ribosomes. European Journal of Biochemistry 268:2896–2904. https://doi.org/10.1046/j.1432-1327.2001.02177.x
Chavatte, L., Kervestin, S., Favre, A., and Jean-Jean, O. 2003. Stop codon selection in eukaryotic translation termination: comparison of the discriminating potential between human and ciliate eRF1s. The EMBO Journal 22:1644–1653. https://doi.org/10.1093/emboj/cdg146
Cheng, Z., Saito, K., Pisarev, A. V., Wada, M., Pisareva, V. P., Pestova, T. V., Gajda, M., Round, A., Kong, C., Lim, M., Nakamura, Y., Svergun, D. I., Ito, K., and Song, H. 2009. Structural insights into eRF3 and stop codon recognition by eRF1. Genes & Development 23:1106–1118. https://doi.org/10.1101/gad.1770109
Chernoff, Y. O., Derkatch, I. L., Dagkesamanskaya, A. R., Tikhomirova, V. L., and Ter-Avanesyan, M. D. 1988. Nonsense-suppression by amplification of translational protein factor gene. Doklady Akademii Nauk SSSR (Proceedings of USSR Academy of Sciences, in Russian) 301:1227–1229.
Chernoff, Y. O., Derkatch, I. L., and Inge-Vechtomov, S. G. 1993. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Current Genetics 24:268–270. https://doi.org/10.1007/BF00351802
Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G., and Liebman, S. W. 1995. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [PSI+]. Science 268:880–884. https://doi.org/10.1126/science.7754373
Cosson, B., Couturier, A., Chabelskaya, S., Kiktev, D., Inge-Vechtomov, S., Philippe, M., and Zhouravleva, G. 2002. Poly (A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI+] propagation. Molecular and Cellular Biology 22:3301–3315. https://doi.org/10.1128/MCB.22.10.3301-3315.2002
Cox, B. 1965. [PSI+], a cytoplasmic suppressor of super-suppressor in yeast. Heredity 20:505–521. https://doi.org/10.1038/hdy.1965.65
Cox, B., Tuite, M. F., and McLaughlin, C. S. 1988. The ψ factor of yeast: A problem in inheritance. Yeast 4:159–178. https://doi.org/10.1002/yea.320040302
Cox, B. S. 1971. A recessive lethal super-suppressor mutation in yeast and other ψ phenomena. Heredity 26:211. https://doi.org/10.1038/hdy.1971.28
Craigen, W. J., Cook, R. G., Tate, W. P., and Caskey, C. T. 1985. Bacterial peptide chain release factors: conserved primary structure and possible frameshift regulation of release factor 2. Proceedings of the National Academy of Sciences USA 82:3616–3620. https://doi.org/10.1073/pnas.82.11.3616
Craigen, W. J. and Caskey, C. T. 1987. The function, structure and regulation of E. coli peptide chain release factors. Biochimie 69:1031–1041. https://doi.org/10.1016/0300-9084(87)90003-4
Crouzet, M. and Tuite, M. F. 1987. Genetic control of translational fidelity in yeast: molecular cloning and analysis of the allosuppressor gene SAL3. Molecular Genetics and Genomics 210:581–583. https://doi.org/10.1007/BF00327216
Crouzet, M., Izgu, F., Grant, C. M., and Tuite, M. F. 1988. The allosuppressor gene SAL4 encodes a protein important for maintaining translational fidelity in Saccharomyces cerevisiae. Current Genetics 14:537–543. https://doi.org/10.1007/BF00434078
Derkatch, I. L., Chernoff, Y. O., Kushnirov, V. V., Inge-Vechtomov, S. G., and Liebman, S. W. 1996. Genesis and variability of [PSI+] prion factors in Saccharomyces cerevisiae. Genetics 144:1375–1386.
Didichenko, S. A., Ter-Avanesyan, M. D., and Smirnov, V. N. 1991. Ribosome-bound EF-1α-like protein of yeast Saccharomyces cerevisiae. European Journal of Biochemistry 198:705–711. https://doi.org/10.1111/j.1432-1033.1991.tb16070.x
Doel, S. M., McCready, S. J., Nierras, C. R., and Cox, B. 1994. The dominant PNM2-mutation which eliminates the ψ factor of Saccharomyces cerevisiae is the result of a missense mutation in the SUP35 gene. Genetics 137:659–670.
Drozdova, P. B., Tarasov, O. V., Matveenko, A. G., Radchenko, E. A., Sopova, J. V., Polev, D. E., Inge-Vechtomov S. G., and Dobrynin, P. V. 2016. Genome sequencing and comparative analysis of Saccharomyces cerevisiae strains of the Peterhof genetic collection. PLoS One 11(5):e0154722. https://doi.org/10.1371/journal.pone.0154722
Ebihara, K. and Nakamura, Y. 1999. C-terminal interaction of translational release factors eRF1 and eRF3 of fission yeast: G-domain uncoupled binding and the role of conserved amino acids. RNA 5(5):739–750. https://doi.org/10.1017/S135583829998216X
Ehrenberg, M. and Tenson, T. 2002. A new beginning of the end of translation. Nature Structural & Molecular Biology 9:85. https://doi.org/10.1038/nsb0202-85
Eurwilaichitr, L., Graves, F. M., Stansfield, I., and Tuite, M. F. 1999. The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Molecular Microbiology 32:485–496. https://doi.org/10.1046/j.1365-2958.1999.01346.x
Eustice, D. C., Wakem, L. P., Wilhelm, J. M., and Sherman, F. 1986. Altered 40S ribosomal subunits in omnipotent suppressors of yeast. Journal of Molevular Biology 188:207–214. https://doi.org/10.1016/0022-2836(86)90305-0
Fabret, C., Cosnier, B., Lekomtsev, S., Gillet, S., Hatin, I., Maréchal, P. Le, and Rousset, J. P. 2008. A novel mutant of the Sup35 protein of Saccharomyces cerevisiae defective in translation termination and in GTPase activity still supports cell viability. BMC Molecular Biology 9(1):22. https://doi.org/10.1186/1471-2199-9-22
Fan-Minogue, H., Du, M., Pisarev, A. V., Kallmeyer, A. K., Salas-Marco, J., Keeling, K. M., Thompson, S. R., Pestova, T. V., David M., and Bedwell, D. M. 2008. Distinct eRF3 requirements suggest alternate eER1 conformations mediate peptide release during eukaryotic translation termination. Molecular Cell 30:599–609. https://doi.org/10.1016/j.molcel.2008.03.020
Firoozan, M., Grant, C.M., Duarte, J. A. B., and Tuite, M. F. 1991. Quantitation of readthrough of termination codons in yeast using a novel gene fusion assay. Yeast 7:173–183. https://doi.org/10.1002/yea.320070211
Franzmann, T. M., Jahnel, M., Pozniakovsky, A., Mahamid, J., Holehouse, A.S., Nüske, E., Richter, D., Baumeister, W., Grill, S. W., Pappu, R. V., Hyman A. A., and Alberti S. 2018. Phase separation of a yeast prion protein promotes cellular fitness. Science 359(6371):eaao5654. https://doi.org/10.1126/science.aao5654
Frolova, L. Y., Dalphin, M. E., Justesen, J., Powell, R. J., Drugeon, G., McCaughan, K. K., Kisselev, L. L., Tate, W. P., and Haenni, A. L. 1993. Mammalian polypeptide chain release factor and tryptophanyl-tRNA synthetase are distinct proteins. The EMBO Journal 12:4013–4019. https://doi.org/10.1002/j.1460-2075.1993.tb06079.x
Frolova, L. Y., Goff, X. Le, Rasmussen, H. H., Cheperegin, S., Drugeon, G., Kress, M., Arman, I., Haenni, A.-L., Celis J. E., Phllippe M., Justesen J., and Kisselev L. 1994. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature 372:701–703. https://doi.org/10.1038/372701a0
Frolova, L. Y., Goff, X. Le, Zhouravleva, G., Davydova, E., Philippe, M., and Kisselev, L. L. 1996. Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA 2:334–341.
Frolova, L. Y., Simonsen, J. L., Merkulova, T. I., Litvinov, D. Y., Martensen, P. M., and Rechinsky, V. O. 1998. Functional expression of eukaryotic polypeptide chain release factors 1 and 3 by means of baculovirus/insect cells and complex formation between the factors. European Journal of Biochemistry 256:36–43. https://doi.org/10.1046/j.1432-1327.1998.2560036.x
Frolova, L. Y., Tsivkovskii, R. Y., Sivolobova, G. F., Oparina, N. Y., Serpinsky, O. I., Blinov, V. M., Tatkov, S. I., and Kisselev, L. L. 1999. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5:1014–1020. https://doi.org/10.1017/S135583829999043X
Frolova, L., Seit-Nebi, A., and Kisselev, L. 2002. Highly conserved NIKS tetrapeptide is functionally essential in eukaryotic translation termination factor eRF1. RNA 8:129–136. https://doi.org/10.1017/S1355838202013262
Gerlach, W. L. 1976. Mutational properties of supP amber-ochre suppressors in Saccharomyces cerevisiae. Molecular Genetics and Genomics 144:213–215. https://doi.org/10.1007/BF02428111
Grentzmann, G., Brechemier-Baey, D., Heurgue, V., Mora, L., and Buckingham, R. H. 1994. Localization and characterization of the gene encoding release factor RF3 in Escherichia coli. Proceedings of the National Academy of Sciences USA 91:5848–5852. https://doi.org/10.1073/pnas.91.13.5848
Helsen, C. W. and Glover, J. R. 2012. Insight into molecular basis of curing of [PSI+] prion by overexpression of 104-kDa heat shock protein (Hsp104). Journal of Biological Chemistry 287(1):542–556. https://doi.org/10.1074/jbc.M111.302869
Hatin, I., Fabret, C., Namy, O., Decatur, W. A., and Rousset, J. P. 2007. Fine-tuning of translation termination efficiency in Saccharomyces cerevisiae involves two factors in close proximity to the exit tunnel of the ribosome. Genetics 177:1527–1537. https://doi.org/10.1534/genetics.107.070771
Hatin, I., Fabret, C., Rousset, J. P., and Namy, O. 2009. Molecular dissection of translation termination mechanism identifies two new critical regions in eRF1. Nucleic Acids Research 37:1789–1798. https://doi.org/10.1093/nar/gkp012
Hawthorne, D. C. and Leupold, U. 1974. Suppressors in yeast. Current Topics in Microbiology and Immunology 64:1–47. https://doi.org/10.1007/978-3-642-65848-8_1
Himmelfarb, H. J., Maicas, E., and Friesen, J. D. 1985. Isolation of the SUP45 omnipotent suppressor gene of Saccharomyces cerevisiae and characterization of its gene product. Molecular and Cellular Biology 5:816–822. https://doi.org/10.1128/MCB.5.4.816
Hoshino, S. I., Imai, M., Mizutani, M., Kikuchi, Y., Hanaoka, F., Ui, M., and Katada, T. 1998. Molecular cloning of a novel member of the eukaryotic polypeptide chain-releasing factors (eRF) its identification as eRF3 interacting with eRF1. Journal of Biological Chemistry 273:22254–22259. https://doi.org/10.1074/jbc.273.35.22254
Inagaki, Y., Blouin, C., Doolittle, W. F., and Roger, A. J. 2002. Convergence and constraint in eukaryotic release factor 1 (eRF1) domain 1: the evolution of stop codon specificity. Nucleic Acids Research 30:532–544. https://doi.org/10.1093/nar/30.2.532
Inagaki, Y. and Doolittle, W. F. 2001. Class I release factors in ciliates with variant genetic codes. Nucleic Acids Research 29:921–927. https://doi.org/10.1093/nar/29.4.921
Inge-Vechtomov, S. G. 1964. Reversions to prototrophy in adenineless yeast. Vestnik Leningradskogo Universiteta 2:112–117.
Inge-Vechtomov, S. G. and Andrianova, V. M. 1970. Recessive supersuppressors in yeast. Genetika 6:103–116.
Inge-Vechtomov, S. G. and Andrianova, V. M. 1972. New type of supersuppressors in yeast. Molecular Mechanisms of Genetic Processes, Nauka, Moskow. pp. 189–195.
Inge-Vechtomov, S. G., Tikhodeev, O. N., and Karpova, T. S. 1988. Selective systems for obtaining recessive ribosomal suppressors in Saccharomycete yeasts. Genetika 24:1159–1165.
Inge-Vechtomov, S., Zhouravleva, G., and Philippe, M. 2003. Eukaryotic release factors (eRFs) history. Biology of the Cell 95:195–209. https://doi.org/10.1016/S0248-4900(03)00035-2
Ito-Harashima, S., Hartzog, P.E., Sinha, H., and McCusker, J. H. 2002. The tRNA-Tyr gene family of Saccharomyces cerevisiae: agenzs of phenotypic variation and position effects on mutation frequency. Genetics 161:1395–1410.
Ito, K., Ebihara, K., Uno, M., and Nakamura, Y. 1996. Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: tRNA-protein mimicry hypothesis. Proceedings of the National Academy of Sciences USA 93:5443–5448. https://doi.org/10.1073/pnas.93.11.5443
Ito, K., Uno, M., and Nakamura, Y. 1998. Single amino acid substitution in prokaryote polypeptide release factor 2 permits it to terminate translation at all three stop codons. Proceedings of the National Academy of Sciences USA 95:8165–8169. https://doi.org/10.1073/pnas.95.14.8165
Ito, K., Frolova, L. Y., Seit-Nebi, A., Karamyshev, A., Kisselev, L., and Nakamura, Y. 2002. Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within domain 1. Proceedings of the National Academy of Sciences USA 99:8494–8499. https://doi.org/10.1073/pnas.142690099
Kabani, M., Cosnier, B., Bousset, L., Rousset, J. P., Melki, R., and Fabret, C. 2011. A mutation within the C-terminal domain of Sup35p that affects [PSI+] prion propagation. Molecular Microbiology 81:640–658. https://doi.org/10.1111/j.1365-2958.2011.07719.x
Kobayashi, T., Funakoshi, Y., Hoshino, S. I., and Katada, T. 2004. The GTP-binding release factor eRF3 as a key mediator coupling translation termination to mRNA decay. Journal of Biological Chemistry 279:45693–45700. https://doi.org/10.1074/jbc.M405163200
Kallmeyer A. K., Keeling K. M., and Bedwell D. M. 2006. Eukaryotic release factor 1 phosphorylation by CK2 protein kinase is dynamic but has little effect on the efficiency of translation termination in Saccharomyces cerevisiae. Eukaryotic Cell 5:1378–1387. https://doi.org/10.1128/EC.00073-06
Karamyshev, A. L., Ito, K., and Nakamura, Y. 1999. Polypeptide release factor eRF1 from Tetrahymena thermophila: cDNA cloning, purification and complex formation with yeast eRF3. FEBS Letters 457:483–488. https://doi.org/10.1016/S0014-5793(99)01089-3
Kiktev, D., Moskalenko, S., Murina, O., Baudin-Baillieu, A., Rousset, J. P., and Zhouravleva, G. 2009. The paradox of viable sup45 STOP mutations: A necessary equilibrium between translational readthrough, activity and stability of the protein. Molecular genetics and genomics 282(1):83–96. https://doi.org/10.1007/s00438-009-0447-5
Kikuchi, Y., Shimatake, H., and Kikuchi, A. 1988. A yeast gene required for the G1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. The EMBO Journal 7:1175–1182. https://doi.org/10.1002/j.1460-2075.1988.tb02928.x
Kim, O. T. P., Yura, K., Go, N., and Harumoto, T. 2005. Newly sequenced eRF1s from ciliates: the diversity of stop codon usage and the molecular surfaces that are important for stop codon interactions. Gene 346:277–286. https://doi.org/10.1016/j.gene.2004.11.046
Kim, O. T. P., Sakurai, A., Saito, K., Ito, K., Ikehara, K., and Harumoto, T. 2008. Ciliates use both variant and universal genetic codes: evidence of omnipotent eRF1s in the class Litostomatea. Gene 417:51–58. https://doi.org/10.1016/j.gene.2008.03.018
Kisselev, L. L. and Buckingham, R. H. 2000. Translational termination comes of age. Trends in Biochemical Sciences 25:561–566. https://doi.org/10.1016/S0968-0004(00)01669-8
Kisselev, L., Ehrenberg, M., and Frolova, L. 2003. Termination of translation: interplay of mRNA, rRNA and release factors? The EMBO Journal 22:175–182. https://doi.org/10.1093/emboj/cdg017
Kobayashi, T., Funakoshi, Y., Hoshino, S., and Katada, T. 2004. The GTP-binding Release Factor eRF3 as a Key Mediator Coupling Translation Termination to mRNA Decay. The Journal of Biological Chemistry 279:45693–45700. https://doi.org/10.1074/jbc.M405163200
Konecki, D. R., Aune, K. C., Tate, W. P., and Caskey, T. C. 1977. Characterization of reticulocyte release factor. The Journal of Biological Chemistry 252:4514–4520.
Kong, C., Ito, K., Walsh, M. A., Wada, M., Liu, Y., Kumar, S., Barford, D, Nakamura, Y., and Song, H. 2004. Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe. Molecular Cell 14:233–245. https://doi.org/10.1016/S1097-2765(04)00206-0
Kopczynski, J. B., Raff, A. C., and Bonner, J. J. 1992. Translational readthrough at nonsense mutations in the HSF1 gene of Saccharomyces cerevisme. Molecular Genetics and Genomics 234:369–378. https://doi.org/10.1007/BF00538696
Kushnirov, V. V., Ter-Avanesyan, M. D., Surguchov, A. P., Smirnov, V. N., and Inge-Vechtomov, S. G. 1987. Localization of possible functional domains in sup2 gene product of the yeast Saccharomyces cerevisiae. FEBS letters 215(2):257–260. https://doi.org/10.1016/0014-5793(87)80157-6
Kushnirov, V. V., Ter-Avanesyan, M. D., Telckov, M. V., Surguchov, A. P., Smirnov, V. N., and Inge-Vechtomov, S. G. 1988. Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene 66:45–54. https://doi.org/10.1016/0378-1119(88)90223-5
Lee, C. C., Craigen, W. J., Muzny, D. M., Harlow, E., and Caskey, C. T. 1990. Cloning and expression of a mammalian peptide chain release factor with sequence similarity to tryptophanyl-tRNA synthetases. Proceedings of the National Academy of Sciences USA 87:3508–3512. https://doi.org/10.1073/pnas.87.9.3508
Liang, A., Brünen-Nieweler, C., Muramatsu, T., Kuchino, Y., Beier, H., and Heckmann, K. 2001. The ciliate Euplotes octocarinatus expresses two polypeptide release factors of the type eRF1. Gene 262:161–168. https://doi.org/10.1016/S0378-1119(00)00538-2
Liebman, J. W. and Sherman, F. 1979. Extrachromosomal [PSI+] determinant suppresses nonsense mutations in yeast. Journal of Bacteriology 139(3):1068–1071.
Liebman, S. W. and All-Robyn, J. A. 1984. A non-Mendelian factor, [eta+], causes lethality of yeast omnipotent-suppressor strains. Current Genetics 22:567–573. https://doi.org/10.1007/BF00395701
Liu, Q. 2005. Comparative analysis of base biases around the stop codons in six eukaryotes. Biosystems 81:281–289. https://doi.org/10.1016/j.biosystems.2005.05.005
Lozupone, C. A., Knight, R. D., and Landweber, L. F. 2001. The molecular basis of nuclear genetic code change in ciliates. Current Biology 11:65–74. https://doi.org/10.1016/S0960-9822(01)00028-8
Matveenko, A. G., Drozdova, P. B., Moskalenko, S. E., Tarasov, O. V., and Zhouravleva, G. A. 2019. Whole genome sequencing data and analyses of the underlying SUP35 transcriptional regulation for a Saccharomyces cerevisiae nonsense suppressor mutant. Data in Brief 2:103694. https://doi.org/10.1016/j.dib.2019.01.042
Merritt, G. H., Naemi, W. R., Mugnier, P., Webb, H. M., Tuite, M. F., and von der Haar, T. 2010. Decoding accuracy in eRF1 mutants and its correlation with pleiotropic quantitative traits in yeast. Nucleic Acids Research 38(16):5479–5492. https://doi.org/10.1093/nar/gkq338
Merkulova, T. I., Frolova, L. Y., Lazar, M., Camonis, J., and Kisselev, L. L. 1999. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Letters 443:41–47. https://doi.org/10.1016/S0014-5793(98)01669-X
Mikuni, O., Ito, K., Moffat, J., Matsumura, K., McCaughan, K., Nobukuni, T., Tate, W., and Nakamura, Y. 1994. Identification of the prfC gene, which encodes peptide-chain-release factor 3 of Escherichia coli. Proceedings of the National Academy of Sciences USA 91:5798–5802. https://doi.org/10.1073/pnas.91.13.5798
Mironova, L. N., Samsonova, M. G., Zhouravleva, G. A., Kulikov, V. N., and Soom, M. J. 1995. Reversions to respiratory competence of omnipotent sup45 suppressor mutants may be caused by secondary sup45 mutations. Current genetics 27(3):195–200. https://doi.org/10.1007/BF00326148
Moskalenko, S. E., Chabelskaya, S. V., Inge-Vechtomov, S. G., Philippe, M., and Zhouravleva, G. A. 2003. Viable nonsense mutants for the essential gene SUP45 of Saccharomyces cerevisiae. BMC Molecular Biology 4:2. https://doi.org/10.1186/1471-2199-4-2
Moskalenko, S. E., Zhouravleva, G. A., Soom, M. J., Chabelskaya, S. V., Volkov, K. V., Zemlyamko, O. M., Philippe, M., Mironova, L. N., and Inge-Vechtomov, S. G. 2004. Characterization of missense mutations in the SUP45 gene of Saccharomyces cerevisiae encoding translation termination factor eRF1. Russian Journal of Genetics 40(5):478–484. https://doi.org/10.1023/B:RUGE.0000029148.58151.91
Mottagui-Tabar, S., Tuite, M. F., and Isaksson, L. A. 1998. The influence of 5′-codon context on translation termination in Saccharomyces cerevisiae. European Journal of Biochemistry 257:249–254. https://doi.org/10.1046/j.1432-1327.1998.2570249.x
Muramatsu, T., Heckmann, K., Kitanaka, C., and Kuchino, Y. 2001. Molecular mechanism of stop codon recognition by eRF1: a wobble hypothesis for peptide anticodons. FEBS Letters 488:105–109. https://doi.org/10.1016/S0014-5793(00)02391-7
Nakamura, Y. and Ito, K. 2003. Making sense of mimic in translation termination. Trends in Biochemical Sciences 28:99–105. https://doi.org/10.1016/S0968-0004(03)00006-9
Nakayashiki, T., Kurtzman, C. P., Edskes, H. K., and Wickner, R. B. 2005. Yeast prions [URE3] and [PSI+] are diseases. Proceedings of the National Academy of Sciences USA 102:10575–10580. https://doi.org/10.1073/pnas.0504882102
Namy, O., Hatin, I., and Rousset, J. 2001. Impact of the six nucleotides downstream of the stop codon on translation termination. EMBO Reports 2:787–793. https://doi.org/10.1093/embo-reports/kve176
Namy, O., Hatin, I., Stahl, G., Liu, H., Barnay, S., Bidou, L., and Rousset, J.-P. 2002. Gene overexpression as a tool for identifying new trans-acting factors involved in translation termination in Saccharomyces cerevisiae. Genetics 161:585–594.
Ono, B.-I., Moriga, N., Ishihara, K., Ishiguro, J., Ishino, Y., and Shinoda, S. 1984. Omnipotent suppressors effective in ψ+ strains of Saccharomyces cerevisiae: recessiveness and dominance. Genetics 107:219–230.
Ono, B.-I., Ishino-Arao, Y., Tanaka, M., Awano, I., and Shinoda, S. 1986. Recessive nonsense suppressors in Saccharomyces cerevisiae: action spectra, complementation groups and map positions. Genetics 114:363–374.
Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N., and Ter-Avanesyan, M. D. 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. https://doi.org/10.1002/j.1460-2075.1996.tb00675.x
Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N., and Ter-Avanesyan, M. D. 1997. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Molecular and cellular biology 17(5):2798–2805. https://doi.org/10.1128/MCB.17.5.2798
Percudani, R., Pavesi, A., and Ottonello, S. 1997. Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. Journal of Molecular Biology 268:322–330. https://doi.org/10.1006/jmbi.1997.0942
Poole, E. S., Brown, C. M., and Tate, W. P. 1995. The identity of the base following the stop codon determines the efficiency of in vivo translational termination in Escherichia coli. The EMBO Journal 14:151–158. https://doi.org/10.1002/j.1460-2075.1995.tb06985.x
Preis, A., Heuer, A., Barrio-Garcia, C., Hauser, A., Eyler, D. E., Berninghausen, O., Green, R., Becker, T., and Beckmann, R. 2014. Cryoelectron microscopic structures of eukaryotic translation termination complexes containing eRF1-eRF3 or eRF1-ABCE1. Cell reports 8:59–65. https://doi.org/10.1016/j.celrep.2014.04.058
Roberts, D. M., Besl, L., Oh, S.-H., Masterson, R. V., Schell, J., and Stacey, G. 1992. Expression of a calmodulin methylation mutant affects the growth and development of transgenic tobacco plants. Proceedings of the National Academy of Sciences USA 89:8394–8398. https://doi.org/10.1073/pnas.89.17.8394
Salas-Marco, J. and Bedwell, D. M. 2004. GTP hydrolysis by erf3 facilitates stop codon decoding during eukaryotic translation termination GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Molecular and Cellular Biology 24:7769–7778. https://doi.org/10.1128/MCB.24.17.7769-7778.2004
Salas-Marco, J., Fan-Minogue, H., Kallmeyer, A. K., Klobutcher, L. A., Farabaugh, P. J., and Bedwell, D. M. 2006. Distinct paths to stop codon reassignment by the variant-code organisms tetrahymena and euplotes. Molecular and Cellular Biology 26:438–447. https://doi.org/10.1128/MCB.26.2.438-447.2006
Seit-Nebi, A., Frolova, L., Justesen, J., and Kisselev, L. 2001. Class-1 translation termination factors: invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition. Nucleic Acids Research 29(19):3982–3987. https://doi.org/10.1093/nar/29.19.3982
Seit-Nebi, A., Frolova, L. Y., and Kisselev, L. 2002. Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Reports 3:881–886. https://doi.org/10.1093/embo-reports/kvf178
Shapiro, R. and Vallee, B. L. 1989. Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis. Biochemistry 28:7401–7408. https://doi.org/10.1021/bi00444a038
Sherman, F. and Stewart, J. W. 1982. The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
Shorter, J. and Lindquist, S. 2005. Prions as adaptive conduits of memory and inheritance. Nature Reviews Genetics 6:435. https://doi.org/10.1038/nrg1616
Schuller A. P. and Green R. 2018. Roadblocks and resolutions in eukaryotic translation. Nature Reviews Molecular Cell Biology 19:526–541. https://doi.org/10.1038/s41580-018-0011-4
Smirnov, V. N., Kreier, V. G., Lizlova, L. V, Andrianova, V. M., and Inge-Vechtomov, S. G. 1974. Recessive super-suppression in yeast. Molecular Genetics and Genomics 129:105–121. https://doi.org/10.1007/BF00268625
Smirnov, V. N., Surguchov, A. P., Fominykch, E. S., Lizlova, L. V, Saprygina, T. V., and Inge-Vechtomov, S. G. 1976. Recessive nonsense-suppression in yeast: further characterization of a defect in translation. FEBS Letters 66:12–15. https://doi.org/10.1016/0014-5793(76)80573-X
Song, H., Mugnier, P., Das, A. K., Webb, H. M., Evans, D. R., Tuite, M. F., Hemmings, B. A., and Barford, D. 2000. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100:311–321. https://doi.org/10.1016/S0092-8674(00)80667-4
Song, J. M. and Liebman, S. W. 1985. Interaction of UAG suppressors and omnipotent suppressors in Saccharomyces cerevisiae. Journal of Bacteriology 161:778–780.
Stansfield, I., Grant, C. M., and Tuite, M. F. 1992. Ribosomal association of the yeast SAL4 (SUP45) gene product: implications for its role in translation fidelity and termination. Molecular Microbiology 6:3469–3478. https://doi.org/10.1111/j.1365-2958.1992.tb01782.x
Stansfield, I. and Tuite, M. F. 1994. Polypeptide chain termination in Saccharomyces cerevisiae. Current Genetics 25:385–395. https://doi.org/10.1007/BF00351776
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., and Tuite, M. F. 1995. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. The EMBO Journal 14:4365–4373. https://doi.org/10.1002/j.1460-2075.1995.tb00111.x
Stansfield, I., Eurwilaichitr, L., Akhmaloka, and Tuite, M. F. 1996. Depletion in the levels of the release factor eRF1 causes a reduction in the efficiency of translation termination in yeast. Molecular Microbiology 20:1135–1143. https://doi.org/10.1111/j.1365-2958.1996.tb02634.x
Studte, P., Zink, S., Jablonowski, D., Bär, C., von der Haar, T., Tuite, M. F., and Schaffrath, R. 2008. tRNA and protein methylase complexes mediate zymocin toxicity in yeast. Molecular Microbiology 69:1266–1277. https://doi.org/10.1111/j.1365-2958.2008.06358.x
Surguchov, A. P., Berestetskaya, Y. V., Fominykch, E. S., Pospelova, E. M., Smirnov, V. N., Ter-Avanesyan, M. D., and Inge-Vechtomov, S. G. 1980. Recessive suppression in yeast Saccharomyces cerevisiae is mediated by a ribosomal mutation. FEBS Letters 111:175–178. https://doi.org/10.1016/0014-5793(80)80786-1
Surguchev, A. P., Piepersberg, W., Smirnov, V. N., Ter-Avanesian, M. D., and Inge-Vechtomov, S. G. 1983. Cloning of the gene sup 1 of Saccharomyces cerevisiae yeasts. Doklad Akademii Nauk SSSR 272:987.
Tate, W. P. and Mannering, S. A. 1996. Three, four or more: the translational stop signal at length. Molecular Microbiology 21:213–219. https://doi.org/10.1046/j.1365-2958.1996.6391352.x
Telkov, M. V, Surguchev, A. P., Dagkesamanskaya, A. R., and Avanesyan, M. D. 1986. Isolation of a chromosomal DNA fragment containing sup2 gene of the yeast S. cerevisiae. Genetika 22:17–25.
Ter-Avanesyan, M. D., Kushnirov, V. V., Dagkesamanskaya, A. R., Didichenko, S. A., Chernoff, Y. O., Inge-Vechtomov, S. G., and Smirnov, V. N. 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. https://doi.org/10.1111/j.1365-2958.1993.tb01159.x
Ter-Avanesyan, M. D., Dagkesamanskaya, A. R., Kushnirov, V. V., and Smirnov, V. N. 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.
Tieg B. and Krebber H. 2013. Dbp5 – from nuclear export to translation. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1829:791–798. https://doi.org/10.1016/j.bbagrm.2012.10.010
Tork, S., Hatin, I., Rousset, J., and Fabret, C. 2004. The major 5′-determinant in stop codon read-through involves two adjacent adenines. Nucleic Acids Research 32:415–421. https://doi.org/10.1093/nar/gkh201
True, H. L. and Lindquist, S. L. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407:477. https://doi.org/10.1038/35035005
True, H. L., Berlin, I., and Lindquist, S. L. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184. https://doi.org/10.1038/nature02885
Uptain, S. M., Sawicki, G. J., Caughey, B., and Lindquist, S. 2001. Strains of [PSI+] are distinguished by their efficiencies of prion-mediated conformational conversion. The EMBO Journal 20:6236–6245. https://doi.org/10.1093/emboj/20.22.6236
Valouev, I. A., Urakov, V. N., Kochneva-Pervukhova, N. V., Smirnov, V. N., and Ter-Avanesyan, M. D. 2004. Translation termination factors function outside of translation: yeast eRF1 interacts with myosin light chain, Mlc1p, to effect cytokinesis. Molecular Microbiology 53(2):687–696. https://doi.org/10.1111/j.1365-2958.2004.04157.x
Volkov, K. V., Kurishko, K., Inge-Vechtomov, S. G., and Mironova, L. N. 2000. Polymorphism of the SUP35 gene and its product in the Saccharomyces cerevisiae yeasts. Genetika 36:155–158.
Volkov, K. V., Aksenova, A. Y., Soom, M. J., Osipov, K. V., Svitin, A. V., Kurischko, C., and Mironova, L. N. 2002. Novel non-Mendelian determinant involved in the control of translation accuracy in Saccharomyces cerevisiae. Genetics 160:25–36.
Volkov, K. V., Osipov, K. V., Valouev, I. А., Inge-Vechtomov, S. G., and Mironova, L. N. 2007. N-terminal extension of Saccharomyces cerevisiae translation termination factor eRF3 inuences the suppression efficiency of sup35 mutations. FEMS Yeast Research 7:1–10. https://doi.org/10.1111/j.1567-1364.2006.00176.x
Wickner, R. B. 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
Wickner, R. B., Masison, D. C., and Edskes, H. K. 1995. [PSI+] and [URE3] as yeast prions. Yeast 11:1671–1685. https://doi.org/10.1002/yea.320111609
Wilson, P. G. and Culbertson, M. R. 1988. SUF12 suppressor protein of yeast. A fusion protein related to the EF-1 family of elongation factors. Journal of Molecular Biology 199:559–573. https://doi.org/10.1016/0022-2836(88)90301-4
Zavialov, A. V., Buckingham, R. H., and Ehrenberg, M. 2001. A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107:115–124. https://doi.org/10.1016/S0092-8674(01)00508-6
Zhou, P. 1999. The yeast non-Mendelian factor [ETA+] is a variant of [PSI+], a prion-like form of release factor eRF3. The EMBO Journal 18:1182–1191. https://doi.org/10.1093/emboj/18.5.1182
Zhouravleva, G., Frolova, L.Y., Goff, X. Le, Guellec, R. Le, Inge-Vechtomov, S., Kisselev, L., and Philippe, M. 1995. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. The EMBO Journal 14:4065–4072. https://doi.org/10.1002/j.1460-2075.1995.tb00078.x
Zhouravleva, G. A., Moskalenko, S. E., Murina, O. A., and Inge-Vechtomov, S. G. 2007. Viable nonsense mutants for the SUP45 gene in the yeast Saccharomyces cerevisiae are lethal at increased temperature. Russian Journal of Genetics 43:1139–1146. https://doi.org/10.1134/S1022795407100079
Downloads
Published
2019-08-27
How to Cite
Trubitsina, N., Zemlyanko, O., Moskalenko, S., & Zhouravleva, G. (2019). From past to future: suppressor mutations in yeast genes encoding translation termination factors. Biological Communications, 64(2), 89–109. https://doi.org/10.21638/spbu03.2019.202
Issue
Section
Review communications
License
Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.
