We employed virus-like elements (VLEs) pGKL1,2 from Kluyveromyces lactis as a model to investigate the previously neglected transcriptome of the broader group of yeast cytoplasmic linear dsDNA VLEs. We performed 5' and 3' RACE analyses of all pGKL1,2 mRNAs and found them not 3' polyadenylated and containing frequently uncapped 5' poly(A) leaders that are not complementary to VLE genomic DNA. The degree of 5' capping and/or 5' mRNA polyadenylation is specific to each gene and is controlled by the corresponding promoter region. The expression of pGKL1,2 transcripts is independent of eIF4E and Pab1 and is enhanced in lsm1Δ and pab1Δ strains. We suggest a model of primitive pGKL1,2 gene expression regulation in which the degree of 5' mRNA capping and 5' non-template polyadenylation, together with the presence of negative regulators such as Pab1 and Lsm1, play important roles. Our data also support a hypothesis of a close relationship between yeast linear VLEs and poxviruses.

Laboratory of RNA Biochemistry Department of Genetics and Microbiology Faculty of Science Charles University Prague Czechia

Zobrazit více v PubMed

Ahn B. Y., Moss B. (1989). Capped poly(A) leaders of variable lengths at the 5′ ends of vaccinia virus late mRNAs. PubMed PMC

Altmann M., Handschin C., Trachsel H. (1987). mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from PubMed DOI PMC

Altmann M., Sonenberg N., Trachsel H. (1989). Translation in PubMed DOI PMC

Altmann M., Trachsel H. (1989). Altered mRNA cap recognition activity of initiation factor 4E in the yeast cell cycle division mutant cdc33. PubMed DOI PMC

Bergman N., Moraes K. C., Anderson J. R., Zaric B., Kambach C., Schneider R. J., et al. (2007). Lsm proteins bind and stabilize RNAs containing 5′ poly(A) tracts. PubMed DOI

Bernstein P., Peltz S. W., Ross J. (1989). The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. PubMed DOI PMC

Boone R. F., Moss B. (1977). Methylated 5′-terminal sequences of vaccinia virus mRNA species made in vivo at early and late times after infection. PubMed DOI

Brenner C., Nakayama N., Goebl M., Tanaka K., Toh-e A., Matsumoto K. (1988). CDC33 encodes mRNA cap-binding protein eIF-4E of PubMed DOI PMC

Butler A. R., White J. H., Stark M. J. (1991). Analysis of the response of PubMed DOI

Costello J., Castelli L. M., Rowe W., Kershaw C. J., Talavera D., Mohammad-Qureshi S. S., et al. (2015). Global mRNA selection mechanisms for translation initiation. PubMed DOI PMC

Davison A. J., Moss B. (1989a). Structure of vaccinia virus early promoters. PubMed DOI

Davison A. J., Moss B. (1989b). Structure of vaccinia virus late promoters. PubMed DOI

de Magistris L., Stunnenberg H. G. (1988). Cis-acting sequences affecting the length of the poly(A) head of vaccinia virus late transcripts. PubMed DOI PMC

Dhungel P., Cao S., Yang Z. (2017). The 5′-poly(A) leader of poxvirus mRNA confers a translational advantage that can be achieved in cells with impaired cap-dependent translation. PubMed DOI PMC

Feketova Z., Masek T., Vopalensky V., Pospisek M. (2010). Ambiguous decoding of the CUG codon alters the functionality of the PubMed DOI

Fukuhara H. (1987). The RF1 gene of the killer DNA of yeast may encode a DNA polymerase. PubMed DOI PMC

Fukuhara H. (1995). Linear DNA plasmids of yeasts. PubMed DOI

Gallie D. R. (1991). The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. PubMed DOI

Giaever G., Chu A. M., Ni L., Connelly C., Riles L., Veronneau S., et al. (2002). Functional profiling of the PubMed DOI

Gietz R. D., Woods R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. PubMed DOI

Gilbert W. V., Zhou K., Butler T. K., Doudna J. A. (2007). Cap-independent translation is required for starvation-induced differentiation in yeast. PubMed DOI

Gowda M., Li H., Alessi J., Chen F., Pratt R., Wang G. L. (2006). Robust analysis of 5′-transcript ends (5′-RATE): a novel technique for transcriptome analysis and genome annotation. PubMed DOI PMC

Gudkov A. T., Ozerova M. V., Shiryaev V. M., Spirin A. S. (2005). 5′-poly(A) sequence as an effective leader for translation in eukaryotic cell-free systems. PubMed DOI

Gueldener U., Heinisch J., Koehler G. J., Voss D., Hegemann J. H. (2002). A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. PubMed PMC

Guldener U., Heck S., Fielder T., Beinhauer J., Hegemann J. H. (1996). A new efficient gene disruption cassette for repeated use in budding yeast. PubMed DOI PMC

Gunge N. (1983). Yeast DNA plasmids. PubMed

Gunge N., Sakaguchi K. (1981). Intergeneric transfer of deoxyribonucleic acid killer plasmids, pGKl1 and pGKl2, from PubMed PMC

Gunge N., Tamaru A., Ozawa F., Sakaguchi K. (1981). Isolation and characterization of linear deoxyribonucleic acid plasmids from PubMed PMC

Gunge N., Tokunaga M. (2004). “Linear DNA plasmids and killer system of DOI

Gunge N., Yamane C. (1984). Incompatibility of linear DNA killer plasmids pGKL1 and pGKL2 from PubMed PMC

Hishinuma F., Nakamura K., Hirai K., Nishizawa R., Gunge N., Maeda T. (1984). Cloning and nucleotide sequences of the linear DNA killer plasmids from yeast. PubMed DOI PMC

Huang B., Johansson M. J., Bystrom A. S. (2005). An early step in wobble uridine tRNA modification requires the Elongator complex. PubMed DOI PMC

Jablonowski D., Zink S., Mehlgarten C., Daum G., Schaffrath R. (2006). tRNAGlu wobble uridine methylation by Trm9 identifies Elongator’s key role for zymocin-induced cell death in yeast. PubMed DOI

Jeske S., Meinhardt F., Klassen R. (2007). “Extranuclear inheritance: virus-like DNA-elements in yeast,” in DOI

Jeske S., Tiggemann M., Meinhardt F. (2006). Yeast autonomous linear plasmid pGKL2: ORF9 is an actively transcribed essential gene with multiple transcription start points. PubMed DOI

Jiao X., Xiang S., Oh C., Martin C. E., Tong L., Kiledjian M. (2010). Identification of a quality-control mechanism for mRNA 5′-end capping. PubMed DOI PMC

Jung G. H., Leavitt M. C., Ito J. (1987). Yeast killer plasmid pGKL1 encodes a DNA polymerase belonging to the family B DNA polymerases. PubMed DOI PMC

Jungfleisch J., Blasco-Moreno B., Diez J. (2016). Use of cellular decapping activators by positive-strand RNA viruses. PubMed DOI PMC

Kahvejian A., Svitkin Y. V., Sukarieh R., M’Boutchou M. N., Sonenberg N. (2005). Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. PubMed DOI PMC

Kamper J., Meinhardt F., Gunge N., Esser K. (1989). New recombinant linear DNA-elements derived from PubMed DOI PMC

Kast A., Klassen R., Meinhardt F. (2014). rRNA fragmentation induced by a yeast killer toxin. PubMed DOI

Kates J., Beeson J. (1970). Ribonucleic acid synthesis in vaccinia virus. I. The mechanism of synthesis and release of RNA in vaccinia cores. PubMed DOI

Klassen R., Meinhardt F. (2007). “Linear protein-primed replicating plasmids in eukaryotic microbes,” in DOI

Kobayashi M., Arias C., Garabedian A., Palmenberg A. C., Mohr I. (2012). Site-specific cleavage of the host poly(A) binding protein by the encephalomyocarditis virus 3C proteinase stimulates viral replication. PubMed DOI PMC

Larsen M., Gunge N., Meinhardt F. (1998). PubMed DOI

Lin R. J., Kim D. H., Castanotto D., Westaway S., Rossi J. J. (1996). “RNA preparation from yeast cells,” in

Lu J., Huang B., Esberg A., Johansson M. J., Bystrom A. S. (2005). The PubMed DOI PMC

Mangus D. A., Amrani N., Jacobson A. (1998). Pbp1p, a factor interacting with PubMed DOI PMC

Maruyama K., Sugano S. (1994). Oligo-capping: a simple method to replace the cap structure of eukaryotic mRNAs with oligoribonucleotides. PubMed DOI

Masek T., Valasek L., Pospisek M. (2011). Polysome analysis and RNA purification from sucrose gradients. PubMed DOI

Masek T., Vopalensky V., Suchomelova P., Pospisek M. (2005). Denaturing RNA electrophoresis in TAE agarose gels. PubMed DOI

Mayes A. E., Verdone L., Legrain P., Beggs J. D. (1999). Characterization of Sm-like proteins in yeast and their association with U6 snRNA. PubMed DOI PMC

McNeel D. G., Tamanoi F. (1991). Terminal region recognition factor 1, a DNA-binding protein recognizing the inverted terminal repeats of the pGKl linear DNA plasmids. PubMed DOI PMC

Meineke B., Kast A., Schwer B., Meinhardt F., Shuman S., Klassen R. (2012). A fungal anticodon nuclease ribotoxin exploits a secondary cleavage site to evade tRNA repair. PubMed DOI PMC

Meinhardt F., Wodara C., Larsen M., Schickel J. (1994). A novel-approach to express a heterologous gene on PubMed DOI

Melo E. O., de Melo Neto O. P., Martins de Sa C. (2003). Adenosine-rich elements present in the 5′-untranslated region of PABP mRNA can selectively reduce the abundance and translation of CAT mRNAs in vivo. PubMed DOI

Mokrejs M., Masek T., Vopalensky V., Hlubucek P., Delbos P., Pospisek M. (2010). IRESite—a tool for the examination of viral and cellular internal ribosome entry sites. PubMed DOI PMC

Mukherjee C., Patil D. P., Kennedy B. A., Bakthavachalu B., Bundschuh R., Schoenberg D. R. (2012). Identification of cytoplasmic capping targets reveals a role for cap homeostasis in translation and mRNA stability. PubMed DOI PMC

Mulder J., Robertson M. E., Seamons R. A., Belsham G. J. (1998). Vaccinia virus protein synthesis has a low requirement for the intact translation initiation factor eIF4F, the cap-binding complex, within infected cells. PubMed PMC

Munroe D., Jacobson A. (1990). mRNA poly(A) tail, a 3′ enhancer of translational initiation. PubMed DOI PMC

Novák J. (2012).

Palfree R. G., Bussey H. (1979). Yeast killer toxin: purification and characterisation of the protein toxin from PubMed DOI

Parker R. (2012). RNA degradation in PubMed DOI PMC

Partow S., Siewers V., Bjorn S., Nielsen J., Maury J. (2010). Characterization of different promoters for designing a new expression vector in PubMed DOI

Patel D. D., Pickup D. J. (1987). Messenger RNAs of a strongly-expressed late gene of cowpox virus contain 5′-terminal poly(A) sequences. PubMed DOI PMC

Patel G. P., Ma S., Bag J. (2005). The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex. PubMed DOI PMC

Pospisek M., Palkova Z. (1991). Microisolation of yeast nucleic-acids on the microtitre plate without using lytic enzymes. PubMed DOI PMC

Pospisek M., Valasek L. (2013). Polysome profile analysis–yeast. PubMed DOI

Ramanathan A., Robb G. B., Chan S. H. (2016). mRNA capping: biological functions and applications. PubMed DOI PMC

Riback J. A., Katanski C. D., Kear-Scott J. L., Pilipenko E. V., Rojek A. E., Sosnick T. R., et al. (2017). Stress-triggered phase separation is an adaptive, evolutionarily tuned response. PubMed DOI PMC

Romanos M. A., Boyd A. (1988). A transcriptional barrier to expression of cloned toxin genes of the linear plasmid k1 of PubMed DOI PMC

Ross J. (1995). mRNA stability in mammalian cells. PubMed PMC

Sachs A. B., Bond M. W., Kornberg R. D. (1986). A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. PubMed DOI

Sachs A. B., Davis R. W., Kornberg R. D. (1987). A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. PubMed DOI PMC

Santiago T. C., Bettany A. J., Purvis I. J., Brown A. J. (1987). Messenger RNA stability in PubMed DOI PMC

Schaffrath R., Meacock P. A. (1995). PubMed DOI

Schaffrath R., Meacock P. A. (2001). An SSB encoded by and operating on linear killer plasmids from PubMed DOI

Schaffrath R., Meinhardt F., Meacock P. A. (1997). ORF7 of yeast plasmid pGKL2: analysis of gene expression in vivo. PubMed DOI

Schaffrath R., Meinhardt F., Meacock P. A. (1999). Genetic manipulation of PubMed DOI

Schickel J., Helmig C., Meinhardt F. (1996). PubMed DOI PMC

Schmidt W. M., Mueller M. W. (1999). CapSelect: a highly sensitive method for 5′ CAP-dependent enrichment of full-length cDNA in PCR-mediated analysis of mRNAs. PubMed PMC

Schrunder J., Gunge N., Meinhardt F. (1996). Extranuclear expression of the bacterial xylose isomerase (xylA) and the UDP-glucose dehydrogenase (hasB) genes in yeast with PubMed

Schrunder J., Meinhardt F. (1995). An extranuclear expression system for analysis of cytoplasmic promoters of yeast linear killer plasmids. PubMed

Schwer B., Mao X., Shuman S. (1998). Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. PubMed DOI PMC

Schwer B., Stunnenberg H. G. (1988). Vaccinia virus late transcripts generated in vitro have a poly(A) head. PubMed PMC

Schwer B., Visca P., Vos J. C., Stunnenberg H. G. (1987). Discontinuous transcription or RNA processing of vaccinia virus late messengers results in a 5′ poly(A) leader. PubMed PMC

Shirokikh N. E., Spirin A. S. (2008). Poly(A) leader of eukaryotic mRNA bypasses the dependence of translation on initiation factors. PubMed DOI PMC

Smith R. W., Gray N. K. (2010). Poly(A)-binding protein (PABP): a common viral target. PubMed DOI

Song M. G., Bail S., Kiledjian M. (2013). Multiple Nudix family proteins possess mRNA decapping activity. PubMed DOI PMC

Sor F., Fukuhara H. (1985). Structure of a linear plasmid of the yeast DOI

Stam J. C., Kwakman J., Meijer M., Stuitje A. R. (1986). Efficient isolation of the linear DNA killer plasmid of PubMed PMC

Stark M. J., Boyd A. (1986). The killer toxin of PubMed PMC

Stark M. J., Mileham A. J., Romanos M. A., Boyd A. (1984). Nucleotide sequence and transcription analysis of a linear DNA plasmid associated with the killer character of the yeast PubMed PMC

Stark M. J. R., Boyd A., Mileham A. J., Romanos M. A. (1990). The plasmid-encoded killer system of PubMed DOI

Sugisaki Y., Gunge N., Sakaguchi K., Yamasaki M., Tamura G. (1984). Characterization of a novel killer toxin encoded by a double-stranded linear DNA plasmid of PubMed DOI

Sýkora M., Pospíšek M., Novák J., Mrvová S., Krásný L., Vopálenský V. (2018). Transcription apparatus of the yeast virus-like elements: architecture, function, and evolutionary origin. PubMed DOI PMC

Tahiri-Alaoui A., Zhao Y., Sadigh Y., Popplestone J., Kgosana L., Smith L. P., et al. (2014). Poly(A) binding protein 1 enhances cap-independent translation initiation of neurovirulence factor from avian herpesvirus. PubMed DOI PMC

Takeda M., Hiraishi H., Takesako T., Tanase S., Gunge N. (1996). The terminal protein of the linear DNA plasmid pGKL2 shares an N-terminal domain of the plasmid-encoded DNA polymerase. PubMed

Tamarkin-Ben-Harush A., Vasseur J. J., Debart F., Ulitsky I., Dikstein R. (2017). Cap-proximal nucleotides via differential eIF4E binding and alternative promoter usage mediate translational response to energy stress. PubMed DOI PMC

Tanguay R. L., Gallie D. R. (1996). Translational efficiency is regulated by the length of the 3′ untranslated region. PubMed PMC

Tarun S. Z., Jr., Sachs A. B. (1995). A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. PubMed

Tiggemann M., Jeske S., Larsen M., Meinhardt F. (2001). PubMed

Tokunaga M., Kawamura A., Hishinuma F. (1989). Expression of pGKL killer 28K subunit in PubMed PMC

Tokunaga M., Wada N., Hishinuma F. (1987). Expression and identification of immunity determinants on linear DNA killer plasmids pGKL1 and pGKL2 in PubMed PMC

Tommasino M. (1991). Killer SYSTEM of PubMed DOI

Tommasino M., Ricci S., Galeotti C. L. (1988). Genome organization of the killer plasmid pGK12 from PubMed PMC

Valis K., Masek T., Novotna D., Pospisek M., Janderova B. (2006). Immunity to killer toxin K1 is connected with the Golgi-to-vacuole protein degradation pathway. PubMed

van Dijk E., Cougot N., Meyer S., Babajko S., Wahle E., Seraphin B. (2002). Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. PubMed PMC

Wang Z., Jiao X., Carr-Schmid A., Kiledjian M. (2002). The hDcp2 protein is a mammalian mRNA decapping enzyme. PubMed PMC

Wei C. M., Moss B. (1974). Methylation of newly synthesized viral messenger RNA by an enzyme in vaccinia virus. PubMed PMC

Wei C. M., Moss B. (1975). Methylated nucleotides block 5′-terminus of vaccinia virus messenger RNA. PubMed PMC

Wieczorek Z., Niedzwiecka-Kornas A., Chlebicka L., Jankowska M., Kiraga K., Stepinski J., et al. (1999). Fluorescence studies on association of human translation initiation factor eIF4E with mRNA cap-analogues. PubMed

Wilson D. W., Meacock P. A. (1988). Extranuclear gene expression in yeast: evidence for a plasmid-encoded RNA polymerase of unique structure. PubMed PMC

Xia X., MacKay V., Yao X., Wu J., Miura F., Ito T., et al. (2011). Translation initiation: a regulatory role for poly(A) tracts in front of the AUG codon in PubMed DOI PMC

Xiang S., Cooper-Morgan A., Jiao X., Kiledjian M., Manley J. L., Tong L. (2009). Structure and function of the 5′→3′ exoribonuclease Rat1 and its activating partner Rai1. PubMed DOI PMC

Yang Z., Martens C. A., Bruno D. P., Porcella S. F., Moss B. (2012). Pervasive initiation and 3′-end formation of poxvirus postreplicative RNAs. PubMed DOI PMC

Yoshikawa K., Tanaka T., Ida Y., Furusawa C., Hirasawa T., Shimizu H. (2011). Comprehensive phenotypic analysis of single-gene deletion and overexpression strains of PubMed DOI

Zakharov J. A., Yurchenko L. V., Yarovot B. F. (1969). Cytoduction: the autonomous transfer of cytoplasmic hereditary factors during pairing of yeast cells.

Zhong Z., Ravikumar A., Liu C. C. (2018). Tunable expression systems for orthogonal DNA replication. PubMed DOI PMC

Zubko E. I., Zubko M. K. (2014). Deficiencies in mitochondrial DNA compromise the survival of yeast cells at critically high temperatures. PubMed DOI

Vaccinia virus mRNAs containing long 5'-poly(A)-leaders lack a canonical 5'-methylguanosine cap