Long non-coding RNA-mediated transcriptional interference of a permease gene confers drug tolerance in fission yeast

Nature Communications

Volumn 5, Issue , 2014, Pages

  Ard, Ryan ^a   Tong, Pin ^a   Allshire, Robin C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; PERMEASE; TRANSPORTER FOR GLYCEROPHOSPHODIESTER 1; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; CARRIER PROTEIN; FUNGAL RNA; SCHIZOSACCHAROMYCES POMBE PROTEIN; SPBC1271.09 PROTEIN, S POMBE; SPNCRNA.1343 LONG NONCODING RNA, S POMBE;

DRUG RESISTANCE; EUKARYOTE; GENE EXPRESSION; PHENOTYPE; RNA; YEAST;

ARTICLE; DNA DAMAGE; DRUG TOLERANCE; EXOSOME; FUNGAL GENOME; GENE LOCUS; GENE REPRESSION; HETEROCHROMATIN; LOXP SITE; NONHUMAN; NUCLEOSOME; OXIDATIVE STRESS; PHENOTYPE; PROMOTER REGION; PROTEIN BINDING; RNA DEGRADATION; RNA INTERFERENCE; RNA TRANSCRIPTION; SCHIZOSACCHAROMYCES POMBE; UPREGULATION; ANTIFUNGAL RESISTANCE; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

ANTIFUNGAL AGENTS; DRUG RESISTANCE, FUNGAL; MEMBRANE TRANSPORT PROTEINS; RNA INTERFERENCE; RNA, FUNGAL; RNA, LONG NONCODING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84923356606     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6576     Document Type: Article

References (57)

1. Guttman et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227 (2009).
2. Ponting, C. P., Oliver, P. L. & Reik, W. Evolution and functions of long noncoding RNAs. Cell 136, 629-641 (2009).
3. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. & Tollervey, D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 30-50 exoribonucleases. Cell 91, 457-466 (1997).
4. Struhl, K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat. Struct. Mol. Biol. 14, 103-105 (2007).
5. Wilusz, J. E., Sunwoo, H. & Spector, D. L. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23, 1494-1504 (2009).
6. Li, B., Carey, M. & Workman, J. L. The role of chromatin during transcription. Cell 128, 707-719 (2007).
7. Hirota, K. et al. Stepwise chromatin remodeling by a cascade of transcription intiation of non-coding RNAs. Nature 456, 130-134 (2008).
8. Hainer, S. J., Pruneski, J. A., Michell, R. D., Monteverde, R. M. & Martens, J. A. Intergenic transcription causes repression by directing nucleosome assembly. Genes Dev. 25, 29-40 (2011).
9. Martens, J. A., Laprade, L. & Winston, F. Inter Thebault genic transcription is required to repress Saccharomyces cerevisiae SER3 gene. Nature 429, 571-574 (2004).
10. Thebault, P. et al. Transcription regulation by the noncoding RNA SRG1 requires Spt2-dependent chromatin deposition in the wake of RNA polymerase II. Mol. Cell Biol. 31, 1288-1300 (2011).
11. Fejes-Toth, K. et al. Post-transcriptional processing generates a diversity of 50-modified long and short RNAs. Nature 457, 1028-1032 (2009).
12. Bayne, E. H. et al. Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140, 666-677 (2010).
13. Motamedi, M. R. et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789-802 (2004).
14. Verdel, A. et al. RNAi-mediated targeting of heterochromatin by the RITS comples. Science 303, 672-676 (2004).
15. Volpe, T. A. et al. Regulation of heterochromatin silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837 (2002).
16. Rinn, J. L. et al. Functional demarcation of active and silent chromatin domains in human HOX loci by non-coding RNAs. Cell 129, 1311-1323 (2007).
17. ∅rom, U. A. et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 143, 46-58 (2010).
18. Camblong, J., Iglesias, N., Fickentscher, C., Dieppois, G. & Stutz, F. Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell 131, 706-717 (2007).
19. Houseley, J., Rubbi, L., Grunstein, M., Tollervey, D. & Vogelauer, M. A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol. Cell 32, 685-695 (2008).
20. van Werven, F. J. et al. Transcription of two long non-coding RNAs mediates mating-type control of gametogenesis in budding yeast. Cell 150, 1170-1181 (2012).
21. Heo, J. B. & Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79 (2011).
22. Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120-124 (2011).
23. Hiriart, E. et al. Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast. EMBO J. 31, 2296-2308 (2012).
24. Yamanaka, S. et al. RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493, 557-560 (2013).
25. Zofall, M. et al. RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335, 96-100 (2012).
26. Harigaya, Y. et al. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45-50 (2006).
27. Lee, N. N. et al. Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155, 1061-1074 (2013).
28. Shah, S., Wittmann, S., Kilchert, C. & Vasilieva, L. lncRNA recruits RNAi and the exosome to dynamically regulate pho1 expression in response to phosphate levels in fission yeast. Genes Dev. 28, 213-244 (2014).
29. Pang, K. C., Frith, M. C. & Mattick, J. S. Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet. 22, 1-5 (2006).
30. Ulitsky, I., Shkumatava, A., Jan, C. H., Sive, H. & Bartel, D. P. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147, 1537-1550 (2011).
31. Rhind, N. et al. Comparative functional genomics of the fission yeasts. Science 332, 930-936 (2011).
32. Wilhelm, B. T. et al. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453, 1239-1243 (2008).
33. Leong, H. S. et al. A global non-coding RNA system modulates fission yeast protein levels in response to stress. Nat. Commun. 5, 3947 (2014).
34. Almaguer, C., Mantella, D., Perez, E. & Patton-Vogt, J. P. Inositol and phosphate regulate GIT1 transcription and glycerophophoinositol incorporation in Saccharomyces cerevisiae. Eukaryot. Cell 2, 729-736 (2003).
35. Carter-O'Connell, I., Peel, M. T., Wykoff, D. D. & O'Shea, E. Genome-wide characterization of the phosphate starvation response in Schizosaccharomyces pombe. BMC Genomics 13, 697 (2012).
36. Henry, T. C. et al. Systematic screen of Schizosaccharomyces pombe deletion collection uncovers parallel evolution of the phosphate signal transduction pathway in yeasts. Eukaryot. Cell 10, 198-206 (2011).
37. Yuan, G. C. et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626-630 (2005).
38. Bitton, D. A. et al. Programmed fluctuations in sense/antisense transcript ratios drive sexual differentiation in S. pombe. Mol. Syst. Biol. 7, 559 (2011).
39. Reyes-Turcu, F. E., Zhang, K., Zofall, M., Chen, E. & Grewal, S. I. Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat. Struct. Mol. Biol. 18, 1132-1138 (2011).
40. Hansen, K. R. et al. Global effects on gene expression in fission yeast by silencing and RNA interference machineries. Mol. Cell Biol. 25, 590-601 (2005).
41. Zafar, M. A., Carabetta, V. J., Mandel, M. J. & Silhavy, T. J. Transcriptional occlusion caused by overlapping promoters. Proc. Natl Acad. Sci. USA 111, 1557-1561 (2014).
42. Greger, I. H., Aranda, A. & Proudfoot, N. Balancing transcription interference and initation on the GAL7 promoter of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 97, 8415-8420 (2000).
43. Bumgarner, S. L. et al. Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proc. Natl Acad. Sci. USA 106, 18321-18326 (2009).
44. Petruk, S. et al. Transcriptional elongations of non-coding bxd RNAs promoted by the Trithorax TAC1 complex represses Ubx by a transcriptional interference mechanism. Cell 127, 1209-1221 (2006).
45. Martianov, I., Ramadass, A., Barros, A. S., Chow, N. & Akoulitchev, A. Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666-670 (2007).
46. Latos, P. A. et al. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Science 338, 1469-1472 (2012).
47. Lee, J. T. & Bartolomei, M. S. X-activation, imprinting, and long non-coding RNAs in health and disease. Cell 152, 1308-1323 (2013).
48. Ei-mann, M. et al. Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development. RNA Biol. 9, 1076-1087 (2012).
49. Korostowski, L., Sedlak, N. & Engel, N. The Kcnq1ot1 long non-coding RNA affects chromatin and expression of Kcnq1, but does not regulate its imprinting in the developing heart. PLOS Genet. 8, e1002956 (2012).
50. Nakagawa, S. et al. Malat1 is not an essential component of nuclear speckles in mice. RNA 18, 1487-1499 (2012).
51. Schorderet, P. & Duboule, D. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLOS Genet. 7, e1002071 (2011).
52. Zhang, B. et al. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2, 111-123 (2012).
53. Nakagawa, S., Naganuma, T., Shioi, G. & Hirose, T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 193, 31-39 (2011).
54. Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of fission yeast Schizosaccharomyces Pombe. Methods Enzymol. 194, 795-823 (1991).
55. Guarente, L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 101, 181-191 (1983).
56. Nakagawachi, T. et al. Silencing effect of CpG island hypermethylation and histone modifications on O6-methylguanine-DNA methyltransferase (MGMT) gene expression in human caner. Oncogene 22, 8835-8844 (2003).
57. Buscaino, A. et al. Raf1 is a DCAF for the Rik1 DDB1-like protein and has separable roles in siRNA generation and chromatin modification. PLOS Genet. 8, e1002499 (2012).