Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
29765496
PubMed Central
PMC5889882
DOI
10.1155/2018/4950591
Knihovny.cz E-zdroje
- MeSH
- biofilmy růst a vývoj MeSH
- buněčná diferenciace MeSH
- lidé MeSH
- RNA dlouhá nekódující metabolismus MeSH
- Saccharomyces cerevisiae patogenita MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- RNA dlouhá nekódující MeSH
We summarize current knowledge regarding regulatory functions of long noncoding RNAs (lncRNAs) in yeast, with emphasis on lncRNAs identified recently in yeast colonies and biofilms. Potential regulatory functions of these lncRNAs in differentiated cells of domesticated colonies adapted to plentiful conditions versus yeast colony biofilms are discussed. We show that specific cell types differ in their complements of lncRNA, that this complement changes over time in differentiating upper cells, and that these lncRNAs target diverse functional categories of genes in different cell subpopulations and specific colony types.
Department Medical Genetics Oslo University Hospital and University of Oslo 0450 Oslo Norway
Faculty of Science Charles University BIOCEV 252 50 Vestec Czech Republic
Institute of Microbiology of the Czech Academy of Sciences BIOCEV 252 50 Vestec Czech Republic
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Palkova Z., Vachova L. Life within a community: benefit to yeast long-term survival. FEMS Microbiology Reviews. 2006;30(5):806–824. doi: 10.1111/j.1574-6976.2006.00034.x. PubMed DOI
Brückner S., Mösch H. U. Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiology Reviews. 2012;36(1):25–58. doi: 10.1111/j.1574-6976.2011.00275.x. PubMed DOI
Honigberg S. M. Cell signals, cell contacts, and the organization of yeast communities. Eukaryotic Cell. 2011;10(4):466–473. doi: 10.1128/EC.00313-10. PubMed DOI PMC
Palkova Z., Vachova L. Yeast cell differentiation: lessons from pathogenic and non-pathogenic yeasts. Seminars in Cell & Developmental Biology. 2016;57:110–119. doi: 10.1016/j.semcdb.2016.04.006. PubMed DOI
Palkova Z., Wilkinson D., Vachova L. Aging and differentiation in yeast populations: elders with different properties and functions. FEMS Yeast Research. 2014;14(1):96–108. doi: 10.1111/1567-1364.12103. PubMed DOI
Podholová K., Plocek V., Rešetárová S., et al. Divergent branches of mitochondrial signaling regulate specific genes and the viability of specialized cell types of differentiated yeast colonies. Oncotarget. 2016;7(13):15299–15314. doi: 10.18632/oncotarget.8084. PubMed DOI PMC
Tan Z., Hays M., Cromie G. A., et al. Aneuploidy underlies a multicellular phenotypic switch. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(30):12367–12372. doi: 10.1073/pnas.1301047110. PubMed DOI PMC
Fatica A., Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nature Reviews Genetics. 2014;15(1):7–21. doi: 10.1038/nrg3606. PubMed DOI
Burroughs A. M., Ando Y., Aravind L. New perspectives on the diversification of the RNA interference system: insights from comparative genomics and small RNA sequencing. Wiley Interdisciplinary Reviews: RNA. 2014;5(2):141–181. doi: 10.1002/wrna.1210. PubMed DOI PMC
David L., Huber W., Granovskaia M., et al. A high-resolution map of transcription in the yeast genome. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(14):5320–5325. doi: 10.1073/pnas.0601091103. PubMed DOI PMC
Davis C. A., Ares M. Accumulation of unstable promoter-associated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(9):3262–3267. doi: 10.1073/pnas.0507783103. PubMed DOI PMC
Wyers F., Rougemaille M., Badis G., et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell. 2005;121(5):725–737. doi: 10.1016/j.cell.2005.04.030. PubMed DOI
Alcid E. A., Tsukiyama T. Expansion of antisense lncRNA transcriptomes in budding yeast species since the loss of RNAi. Nature Structural & Molecular Biology. 2016;23(5):450–455. doi: 10.1038/nsmb.3192. PubMed DOI PMC
Neil H., Malabat C., d’Aubenton-Carafa Y., Xu Z., Steinmetz L. M., Jacquier A. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature. 2009;457(7232):1038–1042. doi: 10.1038/nature07747. PubMed DOI
Xu Z., Wei W., Gagneur J., et al. Bidirectional promoters generate pervasive transcription in yeast. Nature. 2009;457(7232):1033–1037. doi: 10.1038/nature07728. PubMed DOI PMC
Maršíková J., Wilkinson D., Hlaváček O., et al. Metabolic differentiation of surface and invasive cells of yeast colony biofilms revealed by gene expression profiling. BMC Genomics. 2017;18(1):p. 814. doi: 10.1186/s12864-017-4214-4. PubMed DOI PMC
Wilkinson D., Maršíková J., Hlaváček O., et al. Transcriptome remodeling of differentiated cells during chronological ageing of yeast colonies: new insights into metabolic differentiation. Oxidative Medicine and Cellular Longevity. 2018;2018:17. doi: 10.1155/2018/4932905.4932905 PubMed DOI PMC
Váchová L., Stovícek V., Hlavácek O., et al. Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. The Journal of Cell Biology. 2011;194(5):679–687. doi: 10.1083/jcb.201103129. PubMed DOI PMC
Cap M., Stepanek L., Harant K., Vachova L., Palkova Z. Cell differentiation within a yeast colony: metabolic and regulatory parallels with a tumor-affected organism. Molecular Cell. 2012;46(4):436–448. doi: 10.1016/j.molcel.2012.04.001. PubMed DOI
Costa F. F. Non-coding RNAs: meet thy masters. BioEssays. 2010;32(7):599–608. doi: 10.1002/bies.200900112. PubMed DOI
Mavrich T. N., Ioshikhes I. P., Venters B. J., et al. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Research. 2008;18(7):1073–1083. doi: 10.1101/gr.078261.108. PubMed DOI PMC
Schulz D., Schwalb B., Kiesel A., et al. Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell. 2013;155(5):1075–1087. doi: 10.1016/j.cell.2013.10.024. PubMed DOI
Wu J., Delneri D., O'Keefe R. T. Non-coding RNAs in Saccharomyces cerevisiae: what is the function? Biochemical Society Transactions. 2012;40(4):907–911. doi: 10.1042/BST20120042. PubMed DOI PMC
Tisseur M., Kwapisz M., Morillon A. Pervasive transcription—lessons from yeast. Biochimie. 2011;93(11):1889–1896. doi: 10.1016/j.biochi.2011.07.001. PubMed DOI
Vera J. M., Dowell R. D. Survey of cryptic unstable transcripts in yeast. BMC Genomics. 2016;17(1):p. 305. doi: 10.1186/s12864-016-2622-5. PubMed DOI PMC
Yassour M., Pfiffner J., Levin J. Z., et al. Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biology. 2010;11(8, article R87) doi: 10.1186/gb-2010-11-8-r87. PubMed DOI PMC
Gelfand B., Mead J., Bruning A., et al. Regulated antisense transcription controls expression of cell-type-specific genes in yeast. Molecular and Cellular Biology. 2011;31(8):1701–1709. doi: 10.1128/MCB.01071-10. PubMed DOI PMC
Lardenois A., Liu Y., Walther T., et al. Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(3):1058–1063. doi: 10.1073/pnas.1016459108. PubMed DOI PMC
van Werven F. J., Neuert G., Hendrick N., et al. Transcription of two long noncoding RNAs mediates mating-type control of gametogenesis in budding yeast. Cell. 2012;150(6):1170–1181. doi: 10.1016/j.cell.2012.06.049. PubMed DOI PMC
Kim T., Xu Z., Clauder-Munster S., Steinmetz L. M., Buratowski S. Set3 HDAC mediates effects of overlapping noncoding transcription on gene induction kinetics. Cell. 2012;150(6):1158–1169. doi: 10.1016/j.cell.2012.08.016. PubMed DOI PMC
Toesca I., Nery C. R., Fernandez C. F., Sayani S., Chanfreau G. F. Cryptic transcription mediates repression of subtelomeric metal homeostasis genes. PLoS Genetics. 2011;7(6, article e1002163) doi: 10.1371/journal.pgen.1002163. PubMed DOI PMC
Nadal-Ribelles M., Solé C., Xu Z., Steinmetz L. M., de Nadal E., Posas F. Control of Cdc28 CDK1 by a stress-induced lncRNA. Molecular Cell. 2014;53(4):549–561. doi: 10.1016/j.molcel.2014.01.006. PubMed DOI PMC
Vaškovičová K., Awadová T., Veselá P., Balážová M., Opekarová M., Malinsky J. mRNA decay is regulated via sequestration of the conserved 5′-3′ exoribonuclease Xrn1 at eisosome in yeast. European Journal of Cell Biology. 2017;96(6):591–599. doi: 10.1016/j.ejcb.2017.05.001. PubMed DOI
van Dijk E. L., Chen C. L., d’Aubenton-Carafa Y., et al. XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature. 2011;475(7354):114–117. doi: 10.1038/nature10118. PubMed DOI
Luke B., Panza A., Redon S., Iglesias N., Li Z., Lingner J. The Rat1p 5′ to 3′ exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Molecular Cell. 2008;32(4):465–477. doi: 10.1016/j.molcel.2008.10.019. PubMed DOI
Cakiroglu S. A., Zaugg J. B., Luscombe N. M. Backmasking in the yeast genome: encoding overlapping information for protein-coding and RNA degradation. Nucleic Acids Research. 2016;44(17):8065–8072. doi: 10.1093/nar/gkw683. PubMed DOI PMC
Arigo J. T., Eyler D. E., Carroll K. L., Corden J. L. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Molecular Cell. 2006;23(6):841–851. doi: 10.1016/j.molcel.2006.07.024. PubMed DOI
Darby M. M., Serebreni L., Pan X., Boeke J. D., Corden J. L. The Saccharomyces cerevisiae Nrd1-Nab3 transcription termination pathway acts in opposition to Ras signaling and mediates response to nutrient depletion. Molecular and Cellular Biology. 2012;32(10):1762–1775. doi: 10.1128/MCB.00050-12. PubMed DOI PMC
Houseley J. Form and function of eukaryotic unstable non-coding RNAs. Biochemical Society Transactions. 2012;40(4):836–841. doi: 10.1042/BST20120040. PubMed DOI
Wery M., Descrimes M., Vogt N., Dallongeville A. S., Gautheret D., Morillon A. Nonsense-mediated decay restricts LncRNA levels in yeast unless blocked by double-stranded RNA structure. Molecular Cell. 2016;61(3):379–392. doi: 10.1016/j.molcel.2015.12.020. PubMed DOI PMC
Bumgarner S. L., Dowell R. D., Grisafi P., Gifford D. K., Fink G. R. Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(43):18321–18326. doi: 10.1073/pnas.0909641106. PubMed DOI PMC
Mostovoy Y., Thiemicke A., Hsu T. Y., Brem R. B. The role of transcription factors at antisense-expressing gene pairs in yeast. Genome Biology and Evolution. 2016;8(6):1748–1761. doi: 10.1093/gbe/evw104. PubMed DOI PMC
Bumgarner S. L., Neuert G., Voight B. F., et al. Single-cell analysis reveals that noncoding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment. Molecular Cell. 2012;45(4):470–482. doi: 10.1016/j.molcel.2011.11.029. PubMed DOI PMC
Cassone A., Cauda R. Candida and candidiasis in HIV-infected patients: where commensalism, opportunistic behavior and frank pathogenicity lose their borders. AIDS. 2012;26(12):1457–1472. doi: 10.1097/QAD.0b013e3283536ba8. PubMed DOI
Nobile C. J., Mitchell A. P. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Current Biology. 2005;15(12):1150–1155. doi: 10.1016/j.cub.2005.05.047. PubMed DOI
Ramage G., Rajendran R., Sherry L., Williams C. Fungal biofilm resistance. International Journal of Microbiology. 2012;2012:14. doi: 10.1155/2012/528521.528521 PubMed DOI PMC
Martens J. A., Laprade L., Winston F. Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature. 2004;429(6991):571–574. doi: 10.1038/nature02538. PubMed DOI
Martens J. A., Wu P. Y., Winston F. Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes & Development. 2005;19(22):2695–2704. doi: 10.1101/gad.1367605. PubMed DOI PMC
Prescott E. M., Proudfoot N. J. Transcriptional collision between convergent genes in budding yeast. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(13):8796–8801. doi: 10.1073/pnas.132270899. PubMed DOI PMC
Pinskaya M., Gourvennec S., Morillon A. H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. The EMBO Journal. 2009;28(12):1697–1707. doi: 10.1038/emboj.2009.108. PubMed DOI PMC
Geisler S., Lojek L., Khalil A. M., Baker K. E., Coller J. Decapping of long noncoding RNAs regulates inducible genes. Molecular Cell. 2012;45(3):279–291. doi: 10.1016/j.molcel.2011.11.025. PubMed DOI PMC
Lenstra T. L., Coulon A., Chow C. C., Larson D. R. Single-molecule imaging reveals a switch between spurious and functional ncRNA transcription. Molecular Cell. 2015;60(4):597–610. doi: 10.1016/j.molcel.2015.09.028. PubMed DOI PMC
Beck Z. T., Cloutier S. C., Schipma M. J., et al. Regulation of glucose-dependent gene expression by the RNA helicase Dbp2 in Saccharomyces cerevisiae. Genetics. 2014;198(3):1001–1014. doi: 10.1534/genetics.114.170019. PubMed DOI PMC
Cloutier S. C., Ma W. K., Nguyen L. T., Tran E. J. The DEAD-box RNA helicase Dbp2 connects RNA quality control with repression of aberrant transcription. The Journal of Biological Chemistry. 2012;287(31):26155–26166. doi: 10.1074/jbc.M112.383075. PubMed DOI PMC
Cloutier S. C., Wang S., Ma W. K., et al. Regulated formation of lncRNA-DNA hybrids enables faster transcriptional induction and environmental adaptation. Molecular Cell. 2016;61(3):393–404. doi: 10.1016/j.molcel.2015.12.024. PubMed DOI PMC
Cloutier S. C., Wang S., Ma W. K., Petell C. J., Tran E. J. Long noncoding RNAs promote transcriptional poising of inducible genes. PLoS Biology. 2013;11(11, article e1001715) doi: 10.1371/journal.pbio.1001715. PubMed DOI PMC
Zacharioudakis I., Tzamarias D. Bimodal expression of yeast GAL genes is controlled by a long non-coding RNA and a bifunctional galactokinase. Biochemical and Biophysical Research Communications. 2017;486(1):63–69. doi: 10.1016/j.bbrc.2017.02.127. PubMed DOI
Berretta J., Pinskaya M., Morillon A. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes & Development. 2008;22(5):615–626. doi: 10.1101/gad.458008. PubMed DOI PMC
Camblong J., Beyrouthy N., Guffanti E., Schlaepfer G., Steinmetz L. M., Stutz F. Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes & Development. 2009;23(13):1534–1545. doi: 10.1101/gad.522509. PubMed DOI PMC
Uhler J. P., Hertel C., Svejstrup J. Q. A role for noncoding transcription in activation of the yeast PHO5 gene. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(19):8011–8016. doi: 10.1073/pnas.0702431104. PubMed DOI PMC
Bunina D., Štefl M., Huber F., et al. Upregulation of SPS100 gene expression by an antisense RNA via a switch of mRNA isoforms with different stabilities. Nucleic Acids Research. 2017;45(19):11144–11158. doi: 10.1093/nar/gkx737. PubMed DOI PMC
Chia M., Tresenrider A., Chen J., Spedale G., Jorgensen V., et al. Transcription of a 5′ extended mRNA isoform directs dynamic chromatin changes and interference of a downstream promoter. eLife. 2017;6, article 27420 doi: 10.7554/eLife.27420. PubMed DOI PMC
Kim J. H., Lee B. B., Oh Y. M., et al. Modulation of mRNA and lncRNA expression dynamics by the Set2–Rpd3S pathway. Nature Communications. 2016;7, article 13534 doi: 10.1038/ncomms13534. PubMed DOI PMC
McDaniel S. L., Hepperla A. J., Huang J., et al. H3K36 methylation regulates nutrient stress response in Saccharomyces cerevisiae by enforcing transcriptional fidelity. Cell Reports. 2017;19(11):2371–2382. doi: 10.1016/j.celrep.2017.05.057. PubMed DOI PMC
Kwapisz M., Ruault M., van Dijk E., et al. Expression of subtelomeric lncRNAs links telomeres dynamics to RNA decay in S. cerevisiae. Non-Coding RNA. 2015;1(2):94–126. doi: 10.3390/ncrna1020094. PubMed DOI PMC
Traven A., Jänicke A., Harrison P., Swaminathan A., Seemann T., Beilharz T. H. Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities. PLoS One. 2012;7(9, article e46243) doi: 10.1371/journal.pone.0046243. PubMed DOI PMC
Vachova L., Hatakova L., Cap M., Pokorna M., Palkova Z. Rapidly developing yeast microcolonies differentiate in a similar way to aging giant colonies. Oxidative Medicine and Cellular Longevity. 2013;2013:9. doi: 10.1155/2013/102485.102485 PubMed DOI PMC
San Paolo S., Vanacova S., Schenk L., et al. Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genetics. 2009;5(7, article e1000555) doi: 10.1371/journal.pgen.1000555. PubMed DOI PMC
Houseley J., Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Reports. 2006;7(2):205–211. doi: 10.1038/sj.embor.7400612. PubMed DOI PMC
Cherry J. M. The Saccharomyces genome database: advanced searching methods and data mining. Cold Spring Harb Protoc. 2015;2015(12, article pdb.prot088906) doi: 10.1101/pdb.prot088906. PubMed DOI PMC
Khan A., Mathelier A. Intervene: a tool for intersection and visualization of multiple gene or genomic region sets. BMC Bioinformatics. 2017;18(1):p. 287. doi: 10.1186/s12859-017-1708-7. PubMed DOI PMC
Cap M., Vachova L., Palkova Z. Longevity of U cells of differentiated yeast colonies grown on respiratory medium depends on active glycolysis. Cell Cycle. 2015;14(21):3488–3497. doi: 10.1080/15384101.2015.1093706. PubMed DOI PMC
Sole C., Nadal-Ribelles M., de Nadal E., Posas F. A novel role for lncRNAs in cell cycle control during stress adaptation. Current Genetics. 2015;61(3):299–308. doi: 10.1007/s00294-014-0453-y. PubMed DOI PMC