Repression of meiotic genes by antisense transcription and by Fkh2 transcription factor in Schizosaccharomyces pombe

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Chen, Huei Mei ^a,c   Rosebrock, Adam P ^a,b   Khan, Sohail R ^a   Futcher, Bruce ^a   Leatherwood, Janet K ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKH2; TRANSCRIPTION FACTOR MEI4; UNCLASSIFIED DRUG; ANTISENSE OLIGODEOXYNUCLEOTIDE; FKH2 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ANTISENSE TRANSCRIPTION; ARTICLE; FUNGAL CELL; FUNGAL GENE; GENE CONTROL; GENE DELETION; GENE REPRESSION; GENETIC TRANSCRIPTION; MEIOSIS; MEIOTIC GENE; NONHUMAN; RNA INTERFERENCE; RNA SPLICING; SCHIZOSACCHAROMYCES POMBE; CLUSTER ANALYSIS; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCES POMBE;

BASE SEQUENCE; CLUSTER ANALYSIS; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; MEIOSIS; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84855417071     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029917     Document Type: Article

References (72)

1. Huber W, Toedling J, Steinmetz LM, (2006) Transcript mapping with high-density oligonucleotide tiling arrays. Bioinformatics 22: 1963-1970.
2. Numata K, Okada Y, Saito R, Kiyosawa H, Kanai A, et al. (2007) Comparative analysis of cis-encoded antisense RNAs in eukaryotes. Gene 392: 134-141.
3. Ge X, Rubinstein WS, Jung YC, Wu Q, (2008) Genome-wide analysis of antisense transcription with Affymetrix exon array. BMC Genomics 9: 27.
4. Jia H, Osak M, Bogu GK, Stanton LW, Johnson R, et al. (2010) Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA 16: 1478-1487.
5. Yassour M, Pfiffner J, Levin JZ, Adiconis X, Gnirke A, et al. (2010) Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biol 11: R87.
6. Dutrow N, Nix DA, Holt D, Milash B, Dalley B, et al. (2008) Dynamic transcriptome of Schizosaccharomyces pombe shown by RNA-DNA hybrid mapping. Nat Genet 40: 977-986.
7. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243.
8. Ni T, Tu K, Wang Z, Song S, Wu H, et al. (2010) The Prevalence and Regulation of Antisense Transcripts in Schizosaccharomyces pombe. PLoS One 5: e15271.
9. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332: 930-936.
10. Hongay CF, Grisafi PL, Galitski T, Fink GR, (2006) Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 127: 735-745.
11. Gelfand B, Mead J, Bruning A, Apostolopoulos N, Tadigotla V, et al. (2011) Regulated antisense transcription controls expression of cell-type specific genes in yeast. Mol Cell Biol 31: 1071-1079.
12. Camblong J, Iglesias N, Fickentscher C, Dieppois G, Stutz F, (2007) Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell 131: 706-717.
13. Bun-Ya M, Nishimura M, Harashima S, Oshima Y, (1991) The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol Cell Biol 11: 3229-3238.
14. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, et al. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538.
15. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
16. Kishida M, Nagai T, Nakaseko Y, Shimoda C, (1994) Meiosis-dependent mRNA splicing of the fission yeast Schizosaccharomyces pombe mes1+ gene. Curr Genet 25: 497-503.
17. Averbeck N, Sunder S, Sample N, Wise JA, Leatherwood J, (2005) Negative control contributes to an extensive program of meiotic splicing in fission yeast. Mol Cell 18: 491-498.
18. Moldon A, Malapeira J, Gabrielli N, Gogol M, Gomez-Escoda B, et al. (2008) Promoter-driven splicing regulation in fission yeast. Nature 455: 997-1000.
19. McPheeters DS, Cremona N, Sunder S, Chen HM, Averbeck N, et al. (2009) A complex gene regulatory mechanism that operates at the nexus of multiple RNA processing decisions. Nat Struct Mol Biol 16: 255-264.
20. Cremona N, Potter K, Wise JA, (2011) A meiotic gene regulatory cascade driven by alternative fates for newly synthesized transcripts. Mol Biol Cell 22: 66-77.
21. Spiegelman S, Burny A, Das MR, Keydar J, Schlom J, et al. (1970) DNA-directed DNA polymerase activity in oncogenic RNA viruses. Nature 227: 1029-1031.
22. Muller WE, Zahn RK, Seidel HJ, (1971) Inhibitors acting on nucleic acid synthesis in an oncogenic RNA virus. Nature: New biology 232: 143-145.
23. Perocchi F, Xu Z, Clauder-Munster S, Steinmetz LM, (2007) Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D. Nucleic Acids Res 35: e128.
24. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. (2004) GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
25. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, et al. (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119: 789-802.
26. Mata J, Lyne R, Burns G, Bahler J, (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32: 143-147.
27. Mata J, Wilbrey A, Bahler J, (2007) Transcriptional regulatory network for sexual differentiation in fission yeast. Genome biology 8: R217.
28. Nakamura T, Nakamura-Kubo M, Shimoda C, (2002) Novel fission yeast Cdc7-Dbf4-like kinase complex required for the initiation and progression of meiotic second division. Mol Cell Biol 22: 309-320.
29. Amorim MJ, Cotobal C, Duncan C, Mata J, (2010) Global coordination of transcriptional control and mRNA decay during cellular differentiation. Mol Syst Biol 6: 380.
30. Aranda A, Proudfoot NJ, (1999) Definition of transcriptional pause elements in fission yeast. Mol Cell Biol 19: 1251-1261.
31. Nakamura T, Kishida M, Shimoda C, (2000) The Schizosaccharomyces pombe spo6+ gene encoding a nuclear protein with sequence similarity to budding yeast Dbf4 is required for meiotic second division and sporulation. Genes Cells 5: 463-479.
32. Almeida R, Allshire RC, (2005) RNA silencing and genome regulation. Trends Cell Biol 15: 251-258.
33. Buhler M, Spies N, Bartel DP, Moazed D, (2008) TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat Struct Mol Biol 15: 1015-1023.
34. Grewal SI, Elgin SC, (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447: 399-406.
35. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, et al. (2005) Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37: 809-819.
36. Harigaya Y, Tanaka H, Yamanaka S, Tanaka K, Watanabe Y, et al. (2006) Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442: 45-50.
37. Chen HM, Futcher B, Leatherwood J, (2011) The fission yeast RNA binding protein mmi1 regulates meiotic genes by controlling intron specific splicing and polyadenylation coupled RNA turnover. PLoS One 6: e26804.
38. Horie S, Watanabe Y, Tanaka K, Nishiwaki S, Fujioka H, et al. (1998) The Schizosaccharomyces pombe mei4+ gene encodes a meiosis-specific transcription factor containing a forkhead DNA-binding domain. Mol Cell Biol 18: 2118-2129.
39. Oliva A, Rosebrock A, Ferrezuelo F, Pyne S, Chen H, et al. (2005) The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biol 3: e225.
40. Kaufmann E, Hoch M, Jackle H, (1994) The interaction of DNA with the DNA-binding domain encoded by the Drosophila gene fork head. Eur J Biochem 223: 329-337.
41. Gaudet J, Mango SE, (2002) Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295: 821-825.
42. Pierrou S, Hellqvist M, Samuelsson L, Enerback S, Carlsson P, (1994) Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J 13: 5002-5012.
43. Darieva Z, Clancy A, Bulmer R, Williams E, Pic-Taylor A, et al. (2010) A competitive transcription factor binding mechanism determines the timing of late cell cycle-dependent gene expression. Mol Cell 38: 29-40.
44. Wade JT, Hall DB, Struhl K, (2004) The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature 432: 1054-1058.
45. Rudra D, Zhao Y, Warner JR, (2005) Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. EMBO J 24: 533-542.
46. Rustici G, Mata J, Kivinen K, Lio P, Penkett CJ, et al. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat Genet 36: 809-817.
47. Abe H, Shimoda C, (2000) Autoregulated expression of Schizosaccharomyces pombe meiosis-specific transcription factor Mei4 and a genome-wide search for its target genes. Genetics 154: 1497-1508.
48. Koranda M, Schleiffer A, Endler L, Ammerer G, (2000) Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters. Nature 406: 94-98.
49. Reynolds D, Shi BJ, McLean C, Katsis F, Kemp B, et al. (2003) Recruitment of Thr 319-phosphorylated Ndd1p to the FHA domain of Fkh2p requires Clb kinase activity: a mechanism for CLB cluster gene activation. Genes Dev 17: 1789-1802.
50. Darieva Z, Bulmer R, Pic-Taylor A, Doris KS, Geymonat M, et al. (2006) Polo kinase controls cell-cycle-dependent transcription by targeting a coactivator protein. Nature 444: 494-498.
51. Liu J, Tang X, Wang H, Balasubramanian M, (2000) Bgs2p, a 1,3-beta-glucan synthase subunit, is essential for maturation of ascospore wall in Schizosaccharomyces pombe. FEBS Lett 478: 105-108.
52. Martin V, Ribas JC, Carnero E, Duran A, Sanchez Y, (2000) bgs2+, a sporulation-specific glucan synthase homologue is required for proper ascospore wall maturation in fission yeast. Mol Microbiol 38: 308-321.
53. Garcia I, Tajadura V, Martin V, Toda T, Sanchez Y, (2006) Synthesis of alpha-glucans in fission yeast spores is carried out by three alpha-glucan synthase paralogues, Mok12p, Mok13p and Mok14p. Mol Microbiol 59: 836-853.
54. Bailey TL, Elkan C, (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
55. Buske FA, Boden M, Bauer DC, Bailey TL, (2010) Assigning roles to DNA regulatory motifs using comparative genomics. Bioinformatics 26: 860-866.
56. Werner A, Sayer JA, (2009) Naturally occurring antisense RNA: function and mechanisms of action. Curr Opin Nephrol Hypertens 18: 343-349.
57. Buhler M, Spies N, Bartel DP, Moazed D, (2008) TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat Struct Mol Biol 15: 1015-1023.
58. Adhya S, Gottesman M, (1982) Promoter occlusion: transcription through a promoter may inhibit its activity. Cell 29: 939-944.
59. Prescott EM, Proudfoot NJ, (2002) Transcriptional collision between convergent genes in budding yeast. Proc Natl Acad Sci U S A 99: 8796-8801.
60. Xu Z, Wei W, Gagneur J, Clauder-Munster S, Smolik M, et al. (2011) Antisense expression increases gene expression variability and locus interdependency. Mol Syst Biol 7: 468.
61. Lardenois A, Liu Y, Walther T, Chalmel F, Evrard B, et al. (2011) Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proc Natl Acad Sci U S A 108: 1058-1063.
62. Zhang L, Ma H, Pugh BF, (2011) Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res 21: 875-884.
63. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, et al. (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123.
64. Juneau K, Palm C, Miranda M, Davis RW, (2007) High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci U S A 104: 1522-1527.
65. Mahajan A, Yuan C, Lee H, Chen ES, Wu PY, et al. (2008) Structure and function of the phosphothreonine-specific FHA domain. Science signaling 1: re12.
66. Leatherwood J, Futcher B, (2010) King of the castle: competition between repressors and activators on the Mcm1 platform. Mol Cell 38: 1-2.
67. Yamanaka S, Yamashita A, Harigaya Y, Iwata R, Yamamoto M, (2010) Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO J 29: 2173-2181.
68. St-Andre O, Lemieux C, Perreault A, Lackner DH, Bahler J, et al. (2010) Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J Biol Chem 285: 27859-27868.
69. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.
70. Cervantes MD, Farah JA, Smith GR, (2000) Meiotic DNA breaks associated with recombination in S. pombe. Mol Cell 5: 883-888.
71. Ruprecht RM, Goodman NC, Spiegelman S, (1973) Conditions for the selective synthesis of DNA complementary to template RNA. Biochim Biophys Acta 294: 192-203.
72. Li W, Carroll JS, Brown M, Liu S, (2008) xMAN: extreme MApping of OligoNucleotides. BMC Genomics 9 Suppl 1: S20.