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LncRNA expression profiles of Schizosaccharomyces pombe in DNA damage inducing environments

  • Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230027, China

Cite this:
https://doi.org/10.52396/JUST-2021-0074
  • Received Date: 15 March 2021
  • Rev Recd Date: 02 May 2021
  • Publish Date: 31 August 2021
    Abstract

  • Abstract

    LncRNAs are pervasively transcribed in eukaryotic cells and dynamically regulated in response to environmental changes. Compared to mRNAs, roles of lncRNAs in DNA damage responses are poorly understood. The lncRNA expression profiles of Schizosaccharomyces pombe under the treatment of four kinds of DNA damage generating drugs (camptothecin, hydroxyurea, methyl methanesulfonate and phleomycin) were systematically characterized by RNA-seq. Similar to mRNAs, lncRNA repertoires underwent drastic changes in response to DNA damage inducing environments. A Core DNA Damage Response lncRNA set of 161 commonly induced and 194 commonly repressed lncRNAs was identified. The differences between lncRNA and mRNA transcription profiles suggested that lncRNAs might conduct critical functions in DNA damage responses independent from their associated mRNAs. This profiling on lncRNA expressions provided data and resources for further functional studies of the fission yeast lncRNAs.

    Abstract

    LncRNAs are pervasively transcribed in eukaryotic cells and dynamically regulated in response to environmental changes. Compared to mRNAs, roles of lncRNAs in DNA damage responses are poorly understood. The lncRNA expression profiles of Schizosaccharomyces pombe under the treatment of four kinds of DNA damage generating drugs (camptothecin, hydroxyurea, methyl methanesulfonate and phleomycin) were systematically characterized by RNA-seq. Similar to mRNAs, lncRNA repertoires underwent drastic changes in response to DNA damage inducing environments. A Core DNA Damage Response lncRNA set of 161 commonly induced and 194 commonly repressed lncRNAs was identified. The differences between lncRNA and mRNA transcription profiles suggested that lncRNAs might conduct critical functions in DNA damage responses independent from their associated mRNAs. This profiling on lncRNA expressions provided data and resources for further functional studies of the fission yeast lncRNAs.
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    • References(50)
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    Hylton H M, Lucas B E, Petreaca R C. Schizosaccharomyces pombe assays to study mitotic recombination outcomes. Genes (Basel), 2020, 11(1): 79.
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    Thomas A, Pommier Y. Targeting topoisomerase i in the era of precision medicine. Clin. Cancer Res., 2019, 25(22): 6581-6589.
    [31]
    Singh A, Xu Y J. The cell killing mechanisms of hydroxyurea. Genes (Basel), 2016, 7(11): 99.
    [32]
    Zheng F, Chen H, Chen Y, et al. Comparative analysis of ADR on China's national essential medicines list (2015 edition) and WHO model list of essential medicines (19th edition). BioMed Res. Int., 2018, 2018: 7862306.
    [33]
    Lundin C, North M, Erixon K, et al. Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res., 2005, 33(12): 3799-3811.
    [34]
    Murray V, Chen J K, Chung L H. The interaction of the metallo-glycopeptide anti-tumour drug Bleomycin with DNA. Int. J. Mol. Sci., 2018, 19(5): 1372.
    [35]
    Rather G A, Sharma A, Jeelani S M, et al. Metabolic and transcriptional analyses in response to potent inhibitors establish MEP pathway as major route for camptothecin biosynthesis in Nothapodytes nimmoniana (Graham) Mabb. BMC Plant Biol., 2019, 19(1): 301.
    [36]
    Pu X, Zhang C R, Zhu L, et al. Possible clues for camptothecin biosynthesis from the metabolites in camptothecin-producing plants. Fitoterapia, 2019, 134: 113-128.
    [37]
    Chen F, Li W, Jiang L, et al. Functional characterization of a geraniol synthase-encoding gene from Camptotheca acuminata and its application in production of geraniol in Escherichia coli. J. Ind. Microbiol. Biotechnol., 2016, 43(9): 1281-1292.
    [38]
    Camici M, Garcia-Gil M, Pesi R, et al. Purine-metabolising enzymes and apoptosis in cancer. Cancers (Basel), 2019, 11(9): 1354.
    [39]
    Osman F, Bjoras M, Alseth I, et al. A new Schizosaccharomyces pombe base excision repair mutant, nth1, reveals overlapping pathways for repair of DNA base damage. Mol. Microbiol., 2003, 48(2): 465-480.
    [40]
    Yang Y, Gordenin D A, Resnick M A. A single-strand specific lesion drives MMS-induced hyper-mutability at a double-strand break in yeast. DNA Repair (Amst), 2010, 9(8): 914-921.
    [41]
    Pommier Y. Topoisomerase I inhibitors: Camptothecins and beyond. Nat. Rev. Cancer, 2006, 6(10): 789-802.
    [42]
    Veloso A, Biewen B, Paulsen M T, et al. Genome-wide transcriptional effects of the anti-cancer agent camptothecin. PLoS One, 2013, 8(10): e78190.
    [43]
    Ulitsky I, Bartel D P. lincRNAs: Genomics, evolution, and mechanisms. Cell, 2013, 154(1): 26-46.
    [44]
    Schlackow M, Nojima T, Gomes T, et al. Distinctive patterns of transcription and RNA processing for human lincRNAs . Mol. Cell, 2017, 65(1): 25--8.
    [45]
    Wei S, Chen H, Dzakah E E, et al. Systematic evaluation of C. elegans lincRNAs with CRISPR knockout mutants. Genome Biol., 2019, 20(1): 7.
    [46]
    Chen D, Toone W M, Mata J, et al. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell, 2003, 14(1): 214-229.
    [47]
    Brown A J P, Larcombe D E, Pradhan A. Thoughts on the evolution of Core Environmental Responses in yeasts. Fungal Biol., 2020, 124(5): 475-481.
    [48]
    Hallsworth J E. Stress-free microbes lack vitality. Fungal Biol., 2018, 122(6): 379-385.
    [49]
    Mellor J, Woloszczuk R, Howe F S. The interleaved genome. Trends Genet., 2016, 32(1): 57-71.
    [50]
    Jensen T H, Jacquier A, Libri D. Dealing with pervasive transcription. Mol. Cell, 2013, 52(4): 473-484.
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    [1]
    Djebali S, Davis C A, Merkel A, et al. Landscape of transcription in human cells. Nature, 2012, 489(7414): 101-108.
    [2]
    Hangauer M J, Vaughn I W, Mcmanus M T. Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet., 2013, 9(6): e1003569.
    [3]
    Wilhelm B T, Marguerat S, Watt S, et al. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature, 2008, 453(7199): 1239-1243.
    [4]
    Statello L, Guo C J, Chen L L, et al. Gene regulation by long non-coding RNAs and its biological functions. Nat. Rev. Mol. Cell Biol., 2021, 22(2): 96-118.
    [5]
    Hon C C, Ramilowski J A, Harshbarger J, et al. An atlas of human long non-coding RNAs with accurate 5' ends. Nature, 2017, 543(7644): 199-204.
    [6]
    Marguerat S, Schmidt A, Codlin S, et al. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell, 2012, 151(3): 671-683.
    [7]
    Derrien T, Johnson R, Bussotti G, et al. The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res., 2012, 22(9): 1775-1789.
    [8]
    Pauli A, Valen E, Lin M F, et al. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res., 2012, 22(3): 577-591.
    [9]
    Kopp F, Mendell J T. Functional classification and experimental dissection of long noncoding RNAs. Cell, 2018, 172(3): 393-407.
    [10]
    Wang X, Arai S, Song X, et al. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature, 2008, 454(7200): 126-130.
    [11]
    Wan G, Hu X, Liu Y, et al. A novel non-coding RNA lncRNA-JADE connects DNA damage signalling to histone H4 acetylation. EMBO J., 2013, 32(21): 2833-2847.
    [12]
    Sharma V, Khurana S, Kubben N, et al. A BRCA1-interacting lncRNA regulates homologous recombination. EMBO Rep., 2015, 16(11): 1520-1534.
    [13]
    Huarte M. The emerging role of lncRNAs in cancer. Nat. Med., 2015, 21(11): 1253-1261.
    [14]
    Wei L, Sun J, Zhang N, et al. Noncoding RNAs in gastric cancer: implications for drug resistance. Mol. Cancer, 2020, 19(1): 62.
    [15]
    Zhou H, Feng B, Abudoureyimu M, et al. The functional role of long non-coding RNAs and their underlying mechanisms in drug resistance of non-small cell lung cancer. Life Sci., 2020, 261: 118362.
    [16]
    Hylton H M, Lucas B E, Petreaca R C. Schizosaccharomyces pombe assays to study mitotic recombination outcomes. Genes (Basel), 2020, 11(1): 79.
    [17]
    Martienssen R, Moazed D. RNAi and heterochromatin assembly. Cold Spring Harb. Perspect. Biol., 2015, 7(8): a019323.
    [18]
    Liu X, Hoque M, Larochelle M, et al. Comparative analysis of alternative polyadenylation in S. cerevisiae and S. pombe. Genome Res., 2017, 27(10): 1685-1695.
    [19]
    Chung C Z, Jaramillo J E, Ellis M J, et al. RNA surveillance by uridylation-dependent RNA decay in Schizosaccharomyces pombe. Nucleic Acids Res., 2019, 47(6): 3045-3057.
    [20]
    Mcdowall M D, Harris M A, Lock A, et al. PomBase 2015: Updates to the fission yeast database. Nucleic Acids Res., 2015, 43(D1): D656-D661.
    [21]
    Atkinson S R, Marguerat S, Bitton D A, et al. Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast. RNA, 2018, 24(9): 1195-1213.
    [22]
    Ding D Q, Okamasa K, Yamane M, et al. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science, 2012, 336(6082): 732-736.
    [23]
    Ehrensberger K M, Mason C, Corkins M E, et al. Zinc-dependent regulation of the Adh1 antisense transcript in fission yeast. J. Biol. Chem., 2013, 288(2): 759-769.
    [24]
    Leong H S, Dawson K, Wirth C, et al. A global non-coding RNA system modulates fission yeast protein levels in response to stress. Nat. Commun., 2014, 5: 3947.
    [25]
    Hirota K, Miyoshi T, Kugou K, et al. Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature, 2008, 456(7218): 130-134.
    [26]
    Ren B, Tan H L, Nguyen T T T, et al. Regulation of transcriptional silencing and chromodomain protein localization at centromeric heterochromatin by histone H3 tyrosine 41 phosphorylation in fission yeast. Nucleic Acids Res., 2018, 46(1): 189-202.
    [27]
    Lock A, Rutherford K, Harris M A, et al. PomBase 2018: User-driven reimplementation of the fission yeast database provides rapid and intuitive access to diverse, interconnected information. Nucleic Acids Res., 2019, 47(D1): D821-D827.
    [28]
    Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun., 2019, 10(1): 1523.
    [29]
    Pommier Y, Sun Y, Huang S N, et al. Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat. Rev. Mol. Cell Biol., 2016, 17(11): 703-721.
    [30]
    Thomas A, Pommier Y. Targeting topoisomerase i in the era of precision medicine. Clin. Cancer Res., 2019, 25(22): 6581-6589.
    [31]
    Singh A, Xu Y J. The cell killing mechanisms of hydroxyurea. Genes (Basel), 2016, 7(11): 99.
    [32]
    Zheng F, Chen H, Chen Y, et al. Comparative analysis of ADR on China's national essential medicines list (2015 edition) and WHO model list of essential medicines (19th edition). BioMed Res. Int., 2018, 2018: 7862306.
    [33]
    Lundin C, North M, Erixon K, et al. Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res., 2005, 33(12): 3799-3811.
    [34]
    Murray V, Chen J K, Chung L H. The interaction of the metallo-glycopeptide anti-tumour drug Bleomycin with DNA. Int. J. Mol. Sci., 2018, 19(5): 1372.
    [35]
    Rather G A, Sharma A, Jeelani S M, et al. Metabolic and transcriptional analyses in response to potent inhibitors establish MEP pathway as major route for camptothecin biosynthesis in Nothapodytes nimmoniana (Graham) Mabb. BMC Plant Biol., 2019, 19(1): 301.
    [36]
    Pu X, Zhang C R, Zhu L, et al. Possible clues for camptothecin biosynthesis from the metabolites in camptothecin-producing plants. Fitoterapia, 2019, 134: 113-128.
    [37]
    Chen F, Li W, Jiang L, et al. Functional characterization of a geraniol synthase-encoding gene from Camptotheca acuminata and its application in production of geraniol in Escherichia coli. J. Ind. Microbiol. Biotechnol., 2016, 43(9): 1281-1292.
    [38]
    Camici M, Garcia-Gil M, Pesi R, et al. Purine-metabolising enzymes and apoptosis in cancer. Cancers (Basel), 2019, 11(9): 1354.
    [39]
    Osman F, Bjoras M, Alseth I, et al. A new Schizosaccharomyces pombe base excision repair mutant, nth1, reveals overlapping pathways for repair of DNA base damage. Mol. Microbiol., 2003, 48(2): 465-480.
    [40]
    Yang Y, Gordenin D A, Resnick M A. A single-strand specific lesion drives MMS-induced hyper-mutability at a double-strand break in yeast. DNA Repair (Amst), 2010, 9(8): 914-921.
    [41]
    Pommier Y. Topoisomerase I inhibitors: Camptothecins and beyond. Nat. Rev. Cancer, 2006, 6(10): 789-802.
    [42]
    Veloso A, Biewen B, Paulsen M T, et al. Genome-wide transcriptional effects of the anti-cancer agent camptothecin. PLoS One, 2013, 8(10): e78190.
    [43]
    Ulitsky I, Bartel D P. lincRNAs: Genomics, evolution, and mechanisms. Cell, 2013, 154(1): 26-46.
    [44]
    Schlackow M, Nojima T, Gomes T, et al. Distinctive patterns of transcription and RNA processing for human lincRNAs . Mol. Cell, 2017, 65(1): 25--8.
    [45]
    Wei S, Chen H, Dzakah E E, et al. Systematic evaluation of C. elegans lincRNAs with CRISPR knockout mutants. Genome Biol., 2019, 20(1): 7.
    [46]
    Chen D, Toone W M, Mata J, et al. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell, 2003, 14(1): 214-229.
    [47]
    Brown A J P, Larcombe D E, Pradhan A. Thoughts on the evolution of Core Environmental Responses in yeasts. Fungal Biol., 2020, 124(5): 475-481.
    [48]
    Hallsworth J E. Stress-free microbes lack vitality. Fungal Biol., 2018, 122(6): 379-385.
    [49]
    Mellor J, Woloszczuk R, Howe F S. The interleaved genome. Trends Genet., 2016, 32(1): 57-71.
    [50]
    Jensen T H, Jacquier A, Libri D. Dealing with pervasive transcription. Mol. Cell, 2013, 52(4): 473-484.
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