{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T03:58:07Z","timestamp":1790049487462,"version":"4.0.1"},"reference-count":116,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>A secreted protein toxin encoded by a satellite dsRNA-enabled dissection of the genetic control of replication and expression of a single-segment dsRNA virus, the first Totivirus, L-A. Among the then-novel findings were i. \u201chead-full replication\u201d, ii. a supposedly forbidden \u201cT = 2\u201d capsid symmetry based on an asymmetric dimer, iii. a host N-acetyltransferase whose modification of the coat protein is necessary for packaging, iv. Kex1 and Kex2 pro-toxin peptidases leading to discovery of the pre-pro-insulin processing enzymes, and v. specific viral (+) strand sites\/structures needed for RNA packaging and (-) strand synthesis. L-A viral (+) strands made in the particle are extruded to the cytoplasm. Those destined for translation are 5\u2032 7meGMP-capped by a coat protein activity that steals the cap from cellular mRNAs. (+) strands destined for encapsidation in new coats are not capped. Three host-encoded anti-viral systems were found, one based on blocking translation of the viral non-polyA mRNAs (Ski2,3,8 complex), another a 5\u2032-&gt;3\u2032 exoribonuclease specific for uncapped molecules (such as the viral (+) strands)(Ski1\/Xrn1), and the third a mitochondrial nuclease released in cells undergoing meiosis\/sporulation (Nuc1). All of these systems protect cells from virus-induced pathology and have clear animal homologs. The 3\u2032 polyA of yeast mRNAs is dispensable for translation in ski2\u0394 slh1\u0394 cells, and such cells are healthy unless the L-A and M dsRNAs are present, suggesting that this polyA is primarily a device allowing cells to distinguish viral and cellular mRNAs. We suggest that the ribosome-associated Ski2,3,8 proteins block 60S subunit joining on polyA\u2212 mRNAs. Recent evidence of roles for other cellular components controlling viral expression and replication suggests that yeast viruses will continue to be a fertile area for study of viral pathogenesis and host anti-viral systems.<\/jats:p>","DOI":"10.3390\/v18080920","type":"journal-article","created":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T11:37:34Z","timestamp":1787312254000},"page":"920","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["The L-A dsRNA Virus and Its Satellites: Totiviruses and Killers in Saccharomyces cerevisiae"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0273-8247","authenticated-orcid":false,"given":"Reed B.","family":"Wickner","sequence":"first","affiliation":[{"name":"Laboratory of Biochemistry and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2708-2961","authenticated-orcid":false,"given":"Herman K.","family":"Edskes","sequence":"additional","affiliation":[{"name":"Laboratory of Biochemistry and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,21]]},"reference":[{"key":"ref_1","first-page":"202","article-title":"The inheritance of a killer character in yeast (Saccharomyces cerevisiae)","volume":"XI:1","author":"Makower","year":"1963","journal-title":"Proc. Int. Congr. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1099\/00221287-51-1-115","article-title":"Studies on the nature of the killer factor produced by Saccharomyces cerevisiae","volume":"51","author":"Woods","year":"1968","journal-title":"J. Gen. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/S0016672300002743","article-title":"The inheritance of the killer character of yeast","volume":"13","author":"Somers","year":"1968","journal-title":"Genet. Res."},{"key":"ref_4","unstructured":"Howley, P.M., Knipe, D.M., and Enquist, L.W. (2023). Fields Virology: Fundamentals, Wolters Kluwer. [8th ed.]."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1038\/245081b0","article-title":"Preliminary characterization of two species of dsRNA in yeast and their relationship to the \u201ckiller\u201d character","volume":"245","author":"Bevan","year":"1973","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1128\/jb.117.2.681-686.1974","article-title":"Yeast killer mutants with altered double-stranded ribonucleic acid","volume":"117","author":"Vodkin","year":"1974","journal-title":"J. Bacteriol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/0092-8674(82)90136-2","article-title":"Yeast L dsRNA consists of at least three distinct RNAs; evidence that the non-Mendelian genes [HOK], [NEX] and [EXL] are on one of these dsRNAs","volume":"31","author":"Sommer","year":"1982","journal-title":"Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"9010","DOI":"10.1016\/S0021-9258(17)38338-2","article-title":"Translation of the L-species dsRNA genome of the killer-associated virus-like particles of Saccharomyces cerevisiae","volume":"252","author":"Hopper","year":"1977","journal-title":"J. Biol. Chem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6716","DOI":"10.1016\/S0021-9258(18)83488-3","article-title":"The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames","volume":"264","author":"Icho","year":"1989","journal-title":"J. Biol. Chem."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1006\/viro.1996.0083","article-title":"A second double-stranded RNA virus from yeast","volume":"216","author":"Park","year":"1996","journal-title":"Virology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/0092-8674(80)90514-0","article-title":"Translational analysis of the killer-associated virus-like particle dsRNA genome of S. cerevisiae: M dsRNA encodes toxin","volume":"19","author":"Bostian","year":"1980","journal-title":"Cell"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2365","DOI":"10.1093\/nar\/8.11.2365","article-title":"Transcription of killer virion double-stranded RNA in vitro","volume":"8","author":"Welsh","year":"1980","journal-title":"Nucleic Acids Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/S0021-9258(19)57414-2","article-title":"Replicase of L-A virus-like particles of Saccharomyces cerevisiae. In vitro conversion of exogenous L-A and M1 single-stranded RNAs to double-stranded form","volume":"263","author":"Fujimura","year":"1988","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1128\/jvi.62.4.1278-1285.1988","article-title":"A deletion mutant of L-A double-stranded RNA replicates like M1 double-stranded RNA","volume":"62","author":"Esteban","year":"1988","journal-title":"J. Virol."},{"key":"ref_15","first-page":"1552","article-title":"Three different M1 RNA-containing viruslike particle types in Saccharomyces cerevisiae: In vitro M1 double-stranded RNA synthesis","volume":"6","author":"Esteban","year":"1986","journal-title":"Mol. Cell. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1101\/SQB.1962.027.001.005","article-title":"Physical principles in the construction of regular viruses","volume":"Volume 27","author":"Caspar","year":"1962","journal-title":"Cold Spring Harbor Symposia on Quantitative Biology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"15549","DOI":"10.1073\/pnas.0406935101","article-title":"Viruses and the physics of soft condensed matter","volume":"101","author":"Zlotnick","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1006\/jmbi.1994.1726","article-title":"Fungal virus capsids are cytoplasmic compartments for the replication of double-stranded RNA formed as icosahedral shells of assymetric Gag dimers","volume":"244","author":"Cheng","year":"1994","journal-title":"J. Mol. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/nsb844","article-title":"L-A dsRNA virus at 3.4 Angstroms resolution reveals particle architecture and mRNA decapping mechanism","volume":"9","author":"Naitow","year":"2002","journal-title":"Nat. Struct. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/26694","article-title":"The atomic structure of the bluetongue virus core","volume":"395","author":"Grimes","year":"1998","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1038\/35010041","article-title":"Structure of the reovirus core at 3.6 A resolution","volume":"404","author":"Reinisch","year":"2000","journal-title":"Nature"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1038\/emboj.2009.109","article-title":"The picobirnavirus crystal structure provides functional insights into virion assembly and cell entry","volume":"28","author":"Duquerroy","year":"2009","journal-title":"EMBO J."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2435","DOI":"10.1099\/vir.0.000182","article-title":"Megabirnavirus structure reveals a putative 120-subunit capsid formed by asymmetrical dimers with distinctive large protrusions","volume":"96","author":"Miyazaki","year":"2015","journal-title":"J. Gen. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1182","DOI":"10.1128\/JVI.02745-14","article-title":"Three-dimensional structure of a protozoal double-stranded RNA virus that infects the enteric pathogen Giardia lamblia","volume":"89","author":"Janssen","year":"2015","journal-title":"J. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Dunn, S.E., Li, H., Cardone, G., Nibert, M.L., Ghabrial, S.A., and Baker, T.S. (2013). Three-dimensional structure of victorivirus HvV190S suggests coat proteins in most totiviruses share a conserved core. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003225"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/S0022-2836(03)00695-8","article-title":"Three-dimensional structure of Penicillium chrysogenum virus: A double-stranded RNA virus with a genuine T=1 capsid","volume":"331","author":"Caston","year":"2003","journal-title":"J. Mol. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Wei, H., Cheng, R.H., Berriman, J., Rice, W.J., Stokes, D.L., Katz, A., Morgan, D.G., and Gottlieb, P. (2009). Three-dimensional structure of the enveloped bacteriophage \u03a612: An incomplete T=13 lattice is superposed on an enclosed T=1 shell. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0006850"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1083\/jcb.138.5.975","article-title":"Structure of L-A virus: A specialized compartment for the transcription and replication of double-stranded RNA","volume":"138","author":"Caston","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1126\/science.1176945","article-title":"RNAi in budding yeast","volume":"326","author":"Drinnenberg","year":"2009","journal-title":"Science"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1126\/science.1209575","article-title":"Compatibility with killer explains the rise of RNAi-deficient fungi","volume":"333","author":"Drinnenberg","year":"2011","journal-title":"Science"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"10575","DOI":"10.1073\/pnas.0504882102","article-title":"Yeast prions [URE3] and [PSI+] are diseases","volume":"102","author":"Nakayashiki","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Wickner, R.B., and Edskes, H.K. (2015). Yeast killer elements hold their hosts hostage. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005139"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Kast, A., Voges, R., Schroth, M., Schaffrath, R., Klassen, R., and Meinhardt, F. (2015). Autoselection of cytoplasmic yeast virus like elements encoding toxin\/antitoxin systems involves a nuclear barrier for immunity gene expression. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005005"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e62238","DOI":"10.7554\/eLife.62238","article-title":"Adaptive evolution of nontransitive fitness in yeast","volume":"9","author":"Buskirk","year":"2020","journal-title":"eLife"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1128\/jb.136.3.1002-1007.1978","article-title":"Chromosomal superkiller mutants of Saccharomyces cerevisiae","volume":"136","author":"Guerry","year":"1978","journal-title":"J. Bacteriol."},{"key":"ref_36","first-page":"761","article-title":"Superkiller mutations in Saccharomyces cerevisiae suppress exclusion of M2 double-stranded RNA by L-A-HN and confer cold sensitivity in the presence of M and L-A-HN","volume":"4","author":"Ridley","year":"1984","journal-title":"Mol. Cell. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2719","DOI":"10.1128\/MCB.15.5.2719","article-title":"Synthetic lethality of sep1 (xrn1) ski2 and sep1 (xrn1) ski3 mutants of Saccharomyces cerevisiae is independent of killer virus and suggests a general role for these genes in translation control","volume":"15","author":"Johnson","year":"1995","journal-title":"Mol. Cell. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3080","DOI":"10.1016\/S0021-9258(19)85855-6","article-title":"Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yeilds 5\u2032 mononucleotides by a 5 \u2032-> 3\u2032 mode of hydrolysis","volume":"255","author":"Stevens","year":"1980","journal-title":"J. Biol. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/0378-1119(92)90008-D","article-title":"Characterization of the XRN1 gene encoding a 5 \u2032-> 3\u2032 exoribonuclease: Sequence data and analysis of disparate protein and mRNA levels of gene-disrupted cells","volume":"120","author":"Larimer","year":"1992","journal-title":"Gene"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/0042-6822(87)90338-2","article-title":"Gene disruption indicates that the only essential function of the SKI8 chromosomal gene is to protect Saccharomyces cerevisiae from viral cytopathology","volume":"157","author":"Sommer","year":"1987","journal-title":"Virology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/yea.320050304","article-title":"Structure and nuclear localization signal of the SKI3 antiviral protein of Saccharomyces cerevisiae","volume":"5","author":"Rhee","year":"1989","journal-title":"Yeast"},{"key":"ref_42","first-page":"4331","article-title":"Evidence that the SKI antiviral system of Saccharomyces cerevisiae acts by blocking expression of viral mRNA","volume":"13","author":"Widner","year":"1993","journal-title":"Mol. Cell. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2763","DOI":"10.1128\/MCB.15.5.2763","article-title":"Decoying the cap\u2014 mRNA degradation system by a double-stranded RNA virus and Poly(A)\u2014 mRNA surveillance by a yeast antiviral system","volume":"15","author":"Masison","year":"1995","journal-title":"Mol. Cell. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"9133","DOI":"10.1073\/pnas.97.16.9133","article-title":"3\u2032 poly(A) is dispensable for translation","volume":"97","author":"Searfoss","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","first-page":"1566","article-title":"A cis-acting element known to block 3\u2032 mRNA degradation enhances expression of polyA-minus mRNA in wild-type yeast cells and phenocopies a ski mutant","volume":"7","author":"Brown","year":"2001","journal-title":"RNA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1093\/genetics\/107.2.199","article-title":"Genetic control of L-A and L-BC dsRNA copy number in killer systems of Saccharomyces cerevisiae","volume":"107","author":"Ball","year":"1984","journal-title":"Genetics"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"7628","DOI":"10.1073\/pnas.87.19.7628","article-title":"Circular single-stranded RNA replicon in Saccharomyces cerevisiae","volume":"87","author":"Matsumoto","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"25812","DOI":"10.1074\/jbc.M804400200","article-title":"20S RNA narnavirus defies the antiviral activity of SKI1\/XRN1 in Saccharomyces cerevisiae","volume":"283","author":"Esteban","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"jkac337","DOI":"10.1093\/g3journal\/jkac337","article-title":"A novel narnavirus is widespread in Saccharomyces cerevisiae and impacts multiple host phenotypes","volume":"13","author":"Vijayraghavan","year":"2023","journal-title":"G3"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3297","DOI":"10.1093\/nar\/16.8.3297","article-title":"Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae","volume":"16","author":"Vincent","year":"1988","journal-title":"Nucleic Acids Res."},{"key":"ref_51","first-page":"3323","article-title":"Overproduction of yeast virus-like particle coat protein genome in strains deficient in a mitochondrial nuclease","volume":"9","author":"Liu","year":"1989","journal-title":"Mol. Cell. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1002\/j.1460-2075.1987.tb04813.x","article-title":"A yeast mutant lacking mitochondrial porin is respiratory-deficient, but can recover respiration with simultaneous accumulation of an 86 kd extramitochondrial protein","volume":"6","author":"Dihanich","year":"1987","journal-title":"EMBO J."},{"key":"ref_53","first-page":"1100","article-title":"Accumulation of viruslike particles in a yeast mutant lacking a mitochondrial pore protein","volume":"9","author":"Dihanich","year":"1989","journal-title":"Mol. Cell. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"16454","DOI":"10.1073\/pnas.1900751116","article-title":"Meiotic viral attenuation through an ancestral apoptotic pathway","volume":"116","author":"Gao","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"32","DOI":"10.15698\/mic2020.02.705","article-title":"Viral attenuation by endonuclease G during yeast gametogenesis: Insights into ancestral roles of programmed cell death?","volume":"7","author":"Gao","year":"2019","journal-title":"Microb. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e2208695120","DOI":"10.1073\/pnas.2208695120","article-title":"Diverse yeast antiviral systems prevent lethal pathogenesis caused by the L-A mycovirus","volume":"120","author":"Chau","year":"2023","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1038\/s41586-024-08015-6","article-title":"Structural basis of mRNA decay by the human exosome-ribosome supercomplex","volume":"635","author":"Kogel","year":"2024","journal-title":"Nature"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/s41564-020-00846-z","article-title":"The SARS-CoV-2 RNA-protein interactome in infected human cells","volume":"6","author":"Schmidt","year":"2021","journal-title":"Nat. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"17667","DOI":"10.1073\/pnas.1111900108","article-title":"Cap-snatching mechanism in yeast L-A double-stranded RNA virus","volume":"108","author":"Fujimura","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"12797","DOI":"10.1074\/jbc.M111.327676","article-title":"Cap snatching of yeast L-A double-stranded RNA virus can operate in trans and requires viral polymerase actively engaging in transcription","volume":"287","author":"Fujimura","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1111\/mmi.13446","article-title":"Diphosphates at the 5\u2032 end of the positive strand of yeast L-A double-stranded RNA virus as a molecular self-identity tag","volume":"102","author":"Fujimura","year":"2016","journal-title":"Mol. Microbiol."},{"key":"ref_62","first-page":"3390","article-title":"The coat protein of the yeast double-stranded RNA virus L-A attaches covalently to the cap structure of eukaryotic mRNA","volume":"12","author":"Blanc","year":"1992","journal-title":"Mol. Cell. Biol."},{"key":"ref_63","first-page":"2664","article-title":"His154 is involved in the linkage of the Saccharomyces cerevisiae L-A double-stranded RNA virus gag protein to the cap structure of mRNAs and is essential for M1 satellite virus expression","volume":"14","author":"Blanc","year":"1994","journal-title":"Mol. Cell. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1002\/(SICI)1097-0061(19970330)13:4<391::AID-YEA92>3.0.CO;2-Q","article-title":"Identification of gene encoding a putative RNA-helicase, homologous to SKI2, in chromosome VII of Saccharomyces cerevisiae","volume":"13","author":"Martegani","year":"1997","journal-title":"Yeast"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1017\/S1355838200991787","article-title":"The yeast antiviral proteins Ski2p, Ski3p and Ski8p exist as a complex in vivo","volume":"6","author":"Brown","year":"2000","journal-title":"RNA"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1126\/science.aaf7520","article-title":"The cryo-EM structure of a ribosome-Ski2-Ski3-Ski8 helicase complex","volume":"354","author":"Schmidt","year":"2016","journal-title":"Science"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1016\/j.molcel.2020.01.011","article-title":"Extraction of mRNA from stalled ribosomes by the Ski complex","volume":"77","author":"Zinoviev","year":"2020","journal-title":"Molec. Cell"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1002\/wrna.1124","article-title":"Degradation of mRNAs that lack a stop codon: A decade of nonstop progress","volume":"3","author":"Klauer","year":"2012","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/s41467-017-00188-1","article-title":"Ubiquitination of stalled ribosome triggers ribosome-associated quality control","volume":"8","author":"Matsuo","year":"2017","journal-title":"Nat. Comm."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2846","DOI":"10.1073\/pnas.69.10.2846","article-title":"Curing of a killer factor in Saccharomyces cerevisiae","volume":"69","author":"Fink","year":"1972","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4706","DOI":"10.1073\/pnas.79.15.4706","article-title":"Ribosomal protein L3 is involved in replication or maintenance of the killer double-stranded RNA genome of Saccharomyces cerevisiae","volume":"79","author":"Wickner","year":"1982","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2887","DOI":"10.1128\/jb.177.10.2887-2891.1995","article-title":"Translation and M1 dsRNA propagation: MAK18 = RPL41B and cycloheximide curing","volume":"177","author":"Carroll","year":"1995","journal-title":"J. Bacteriol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1128\/jb.140.1.154-160.1979","article-title":"Mak mutants of yeast: Mapping and characterization","volume":"140","author":"Wickner","year":"1979","journal-title":"J. Bacteriol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2772","DOI":"10.1128\/MCB.15.5.2772","article-title":"Yeast virus propagation depends critically on free 60S ribosomal subunit concentration","volume":"15","author":"Ohtake","year":"1995","journal-title":"Mol. Cell. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/0378-1119(90)90082-3","article-title":"Tales of poly(A): A review","volume":"91","author":"Munroe","year":"1990","journal-title":"Gene"},{"key":"ref_76","first-page":"3441","article-title":"mRNA poly(A) tail, a 3\u2032 enhancer of translation initiation","volume":"10","author":"Munroe","year":"1990","journal-title":"Mol. Cell. Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1128\/jvi.65.1.155-161.1991","article-title":"Expression of yeast L-A double-stranded RNA virus proteins produces derepressed replication: A ski- phenocopy","volume":"65","author":"Wickner","year":"1991","journal-title":"J. Virol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"28912","DOI":"10.1074\/jbc.273.44.28912","article-title":"Mak21p of Saccharomyces cerevisiae, a homolog of human CAATT-binding protein, is essential for 60S ribosomal subunit biogenesis","volume":"273","author":"Edskes","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1073\/pnas.77.1.527","article-title":"\u201cSuperkiller\u201d mutations suppress chromosomal mutations affecting double-stranded RNA killer plasmid replication in Saccharomyces cerevisiae","volume":"77","author":"Wickner","year":"1980","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1038\/35002118","article-title":"The ribosomal subunit joining reaction in eukaryotes requires eIF5B","volume":"403","author":"Pestova","year":"2000","journal-title":"Nature"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"16689","DOI":"10.1073\/pnas.262569399","article-title":"Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation","volume":"99","author":"Lee","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1038\/s41586-022-04858-z","article-title":"eIF5B and eIF1A reorient tRNA to allow ribosomal subunit joining","volume":"607","author":"Lapointe","year":"2022","journal-title":"Nature"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"4900","DOI":"10.1128\/MCB.21.15.4900-4908.2001","article-title":"Linking the 3\u2032 poly(A) Tail to the Subunit Joining Step of Translation Initiation: Relations of Pab1p, eIF5B (Fun12p) and Ski2p-Slh1p","volume":"21","author":"Searfoss","year":"2001","journal-title":"Mol. Biol. Cell."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1093\/genetics\/76.3.423","article-title":"Chromosomal and nonchromosomal mutations affecting the \u201ckiller character: Of Saccharomyces cerevisiae","volume":"76","author":"Wickner","year":"1974","journal-title":"Genetics"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2061","DOI":"10.1073\/pnas.73.6.2061","article-title":"A chromosomal gene required for killer plasmid expression, mating, and spore maturation in Saccharomyces cerevisiae","volume":"73","author":"Leibowitz","year":"1976","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1073\/pnas.86.5.1434","article-title":"Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2+-dependent serine protease","volume":"86","author":"Fuller","year":"1989","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/0092-8674(87)90030-4","article-title":"Yeast KEX1 gene encodes a putative protease with a carboxypeptidase B-like function involved in killer toxin and alpha factor proecursor processing","volume":"50","author":"Dmochowska","year":"1987","journal-title":"Cell"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/S0079-6123(08)61179-6","article-title":"The biosynthesis and processing of neuroendocrine peptides: Identification of proprotein convertases involved in intravesicular processing","volume":"92","author":"Smeekens","year":"1992","journal-title":"Prog. Brain Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"7269","DOI":"10.1093\/nar\/12.18.7269","article-title":"Primary structural comparison of RNA-dependent polymerase from plant, animal and bacterial viruses","volume":"12","author":"Kamer","year":"1984","journal-title":"Nucleic Acids Res."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/0092-8674(88)90031-1","article-title":"Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region","volume":"55","author":"Jacks","year":"1988","journal-title":"Cell"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1073\/pnas.88.1.174","article-title":"A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein","volume":"88","author":"Dinman","year":"1991","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1093\/genetics\/136.1.75","article-title":"Translational maintenance of frame: Mutants of Saccharomyces cerevisiae with altered -1 ribosomal frameshfiting efficiencies","volume":"136","author":"Dinman","year":"1994","journal-title":"Genetics"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1093\/genetics\/141.1.95","article-title":"5S rRNA is involved in fidelity of translational reading frame","volume":"141","author":"Dinman","year":"1995","journal-title":"Genetics"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1002\/bies.201500131","article-title":"Reprogramming the genetic code: The emerging role of ribosomal frameshifting in regulating cellular gene expression","volume":"38","author":"Advani","year":"2016","journal-title":"Bioessays"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1016\/0022-2836(91)90361-9","article-title":"Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal","volume":"220","author":"Brierley","year":"1991","journal-title":"J. Mol. Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1825","DOI":"10.1093\/nar\/gki329","article-title":"Torsional restraint: A new twist on frameshifting pseudoknots","volume":"30","author":"Plant","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/0022-2836(76)90102-9","article-title":"Chromosomal genes essential for replication of a double-stranded RNA plasmid of Saccharomyces cerevisiae: The killer character of yeast","volume":"105","author":"Wickner","year":"1976","journal-title":"J. Mol. Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/yea.320010204","article-title":"The PET18 locus of Saccharomyces cerevisiae: A complex locus containing multiple genes","volume":"1","author":"Sahashi","year":"1985","journal-title":"Yeast"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"20270","DOI":"10.1016\/S0021-9258(19)88696-9","article-title":"Localized mutagenesis and evidence for post-transcriptional regulation of MAK3, a putative N-acetyltransferase required for dsRNA virus propagation in Saccharomyces cerevisiae","volume":"267","author":"Tercero","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"20277","DOI":"10.1016\/S0021-9258(19)88697-0","article-title":"MAK3 encodes an N-acetyltransferase whose modification of the L-A gag N-terminus is necessary for virus particle assembly","volume":"267","author":"Tercero","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"3192","DOI":"10.1128\/jb.175.10.3192-3194.1993","article-title":"Yeast MAK3 N-acetyltransferase recognizes the N-terminal four amino acids of the major coat protein (gag) of the L-A double-stranded RNA virus","volume":"175","author":"Tercero","year":"1993","journal-title":"J. Bacteriol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1038\/13732","article-title":"A generic protein purification method for protein complex characterization and proteome exploration","volume":"17","author":"Rigaut","year":"1999","journal-title":"Nat. Biotech."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"20154","DOI":"10.1074\/jbc.M011440200","article-title":"NatC Nalpha-terminal acetyltransferase of yeast contains three subunits, Mak3p, Mak10p and Mak31p","volume":"276","author":"Polevoda","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1038\/nrmicro1347","article-title":"Yeast viral killer toxins: Lethality and self-protection","volume":"4","author":"Schmitt","year":"2006","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Creagh, J.W., Reetz, D.C., Givens, L.L., Cross, S.A., Bizarria, R., Patel, J.S., Rodrigues, A., Ytreberg, F.M., and Rowley, P.A. (2026). A comprehensive structural and functional analysis of Saccharomyces cerevisiae killer toxins. Toxins, 18.","DOI":"10.3390\/toxins18050235"},{"key":"ref_106","first-page":"140","article-title":"Comparative genetics of yeast. XIII. Comparative study of killer strains of Saccharomyces from different collections","volume":"9","author":"Naumov","year":"1973","journal-title":"Genetika"},{"key":"ref_107","first-page":"4807","article-title":"K28, a unique double-stranded RNA killer virus of Saccharomyces cerevisiae","volume":"10","author":"Schmitt","year":"1990","journal-title":"Mol. Cell. Biol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1822","DOI":"10.1128\/AEM.02501-10","article-title":"A new wine Saccharomyces cerevisiae killer toxin (Klus), encoded by a double-stranded RNA virus, with broad antifungal activity is evolutionarily related to a chromosomal host gene","volume":"77","author":"Maqueda","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0092-8674(80)90129-4","article-title":"Plasmids controlling exclusion of the K2 killer double-stranded RNA plasmid of yeast","volume":"21","author":"Wickner","year":"1980","journal-title":"Cell"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1093\/genetics\/100.2.159","article-title":"[HOK], a new yeast non-Mendelian trait, enables a replication-defective killer plasmid to be maintained","volume":"100","author":"Wickner","year":"1982","journal-title":"Genetics"},{"key":"ref_111","first-page":"654","article-title":"Killer systems in Saccharomyces cerevisiae: Three distinct modes of exclusion of M2 double-stranded RNA by three species of double-stranded RNA, M1, L-A-E, and L-A-HN","volume":"3","author":"Wickner","year":"1983","journal-title":"Mol. Cell. Biol."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"4941","DOI":"10.1128\/jb.169.11.4941-4945.1987","article-title":"MKT1, a nonessential Saccharomyces cerevisiae gene with a temperature-dependent effect on replication of M2 double-stranded RNA","volume":"169","author":"Wickner","year":"1987","journal-title":"J. Bacteriol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"3670","DOI":"10.1128\/MCB.24.9.3670-3681.2004","article-title":"Posttranscriptional regulation of HO expression by the Mkt1-Pbp1 complex","volume":"24","author":"Tadauchi","year":"2004","journal-title":"Mol. Cell. Biol."},{"key":"ref_114","first-page":"938","article-title":"Suppression of chromosomal mutations affecting M1 virus replication in Saccharomyces cerevisiae by a variant of a viral RNA segment (L-A) that encodes coat protein","volume":"8","author":"Uemura","year":"1988","journal-title":"Mol. Cell. Biol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1093\/genetics\/117.3.399","article-title":"A new non-mendelian genetic element of yeast that increases cytopathology produced by M1 double-stranded RNA in ski strains","volume":"117","author":"Esteban","year":"1987","journal-title":"Genetics"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"4293","DOI":"10.1073\/pnas.84.12.4293","article-title":"Viruses in fungi: Infection of yeast with the K1 and K2 killer virus","volume":"84","author":"Bostian","year":"1987","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/18\/8\/920\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T11:43:27Z","timestamp":1787312607000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/18\/8\/920"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,21]]},"references-count":116,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["v18080920"],"URL":"https:\/\/doi.org\/10.3390\/v18080920","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,21]]}}}