Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes

Open Biology

Volumn 2, Issue MARCH, 2012, Pages

  Yamashita, Akira ^a   Shichino, Yuichi ^a   Tanaka, Hirotsugu ^a   Hiriart, Edwige ^b   Touat Todeschini, Leila ^b   Vavasseur, Aurélia ^b   Ding, Da Qiao ^c   Hiraoka, Yasushi ^c,d   Verdel, André ^b   Yamamoto, Masayuki ^a,e  

^a UNIVERSITY OF TOKYO   (Japan)

^b INSERM   (France)

^c NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Exosome; Meiosis; Mmi1; mRNA degradation; RNA binding protein

Indexed keywords

SCHIZOSACCHAROMYCETACEAE;

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; FUNGAL RNA; MMI1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CHEMISTRY; CYTOLOGY; EXOSOME; FUNGAL GENE; GENE SILENCING; GENETICS; MEIOSIS; METABOLISM; MMI1; MRNA DEGRADATION; MUTAGENESIS; NUCLEOTIDE SEQUENCE; RNA-BINDING PROTEIN; SCHIZOSACCHAROMYCES; TANDEM REPEAT;

EXOSOME; MEIOSIS; MMI1; MRNA DEGRADATION; RNA-BINDING PROTEIN;

BASE SEQUENCE; EXOSOMES; GENE SILENCING; GENES, FUNGAL; MEIOSIS; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTAGENESIS; RNA, FUNGAL; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TANDEM REPEAT SEQUENCES;

EID: 84860794279     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.120014     Document Type: Article

References (32)

1. Mata J, Lyne R, Burns G, Bahler J. 2002 The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32, 143-147. (doi:10.1038/ng951) (Pubitemid 34977209)
2. Surosky RT, Esposito RE. 1992 Early meiotic transcripts are highly unstable in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 3948-3958.
3. Harigaya Y et al. 2006 Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45-50. (doi:10.1038/ nature04881) (Pubitemid 44064204)
4. Moldon A, Malapeira J, Gabrielli N, Gogol M, Gomez-Escoda B, Ivanova T, Seidel C, Ayte J. 2008 Promoter-driven splicing regulation in fission yeast. Nature 455, 997-1000. (doi:10.1038/nature07325)
5. McPheeters DS, Cremona N, Sunder S, Chen HM, Averbeck N, Leatherwood J, Wise JA. 2009 A complex gene regulatory mechanism that operates at the nexus of multiple RNA processing decisions. Nat. Struct. Mol. Biol. 16, 255-264. (doi:10.1038/nsmb.1556)
6. Stoilov P, Rafalska I, Stamm S. 2002 YTH: a new domain in nuclear proteins. Trends Biochem. Sci. 27, 495-497. (doi:10.1016/S0968-0004(02)02189-8) (Pubitemid 35279588)
7. Harigaya Y, Yamamoto M. 2007 Molecular mechanisms underlying the mitosis-meiosis decision. Chromosome Res. 15, 523-537. (doi:10. 1007/s10577-007-1151-0) (Pubitemid 47221378)
8. 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. (doi:10.1038/emboj.2010.108)
9. Watanabe Y, Yabana S, Chikashige Y, Hiraoka Y, Yamamoto M. 1997 Phosphorylation of RNAbinding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature 386, 187-190. (doi:10.1038/386187a0) (Pubitemid 27131447)
10. Yamashita A, Watanabe Y, Nukina N, Yamamoto M. 1998 RNA-assisted nuclear transport of the meiotic regulator Mei2p in fission yeast. Cell 95, 115-123. (doi:10.1016/S0092-8674(00)81787-0) (Pubitemid 28458029)
11. Shimada T, Yamashita A, Yamamoto M. 2003 The fission yeast meiotic regulator Mei2p forms a dot structure in the horse-tail nucleus in association with the sme2 locus on chromosome II. Mol. Biol. Cell 14, 2461-2469. (doi:10.1091/mbc.E02-11-0738) (Pubitemid 36724334)
12. Imai Y, Matsuo N, Ogawa S, Tohyama M, Takagi T. 1998 Cloning of a gene, YT521, for a novel RNA splicing-related protein induced by hypoxia/ reoxygenation. Brain Res. Mol. Brain Res. 53, 33-40. (doi:10.1016/S0169-328X(97) 00262-3) (Pubitemid 28085440)
13. Hartmann AM, Nayler O, Schwaiger FW, Obermeier A, Stamm S. 1999 The interaction and colocalization of Sam68 with the splicing-associated factor YT521-B in nuclear dots is regulated by the Src family kinase p59(fyn). Mol. Biol. Cell 10, 3909-3926. (Pubitemid 29534034)
14. Zhang Z et al. 2010 The YTH domain is a novel RNA binding domain. J. Biol. Chem. 285, 14 701-14 710. (doi:10.1074/jbc.M110.104711)
15. Thijs G, Marchal K, Lescot M, Rombauts S, De Moor B, Rouze P, Moreau Y. 2002 A Gibbs sampling method to detect overrepresented motifs in the upstream regions of coexpressed genes. J. Comput. Biol. 9, 447-464. (doi:10.1089/ 10665270252935566) (Pubitemid 34548275)
16. Horie S, Watanabe Y, Tanaka K, Nishiwaki S, Fujioka H, Abe H, Yamamoto M, Shimoda C. 1998 The Schizosaccharomyces pombe mei4+ gene encodes a meiosis-specific transcription factor containing a forkhead DNA-binding domain. Mol. Cell Biol. 18, 2118-2129. (Pubitemid 28152661)
17. Mata J, Wilbrey A, Bahler J. 2007 Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 8, R217. (doi:10.1186/ gb-2007-8-10-r217)
18. Watanabe Y, Yamamoto M. 1994 S. pombe mei2 encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78, 487-498. (doi:10.1016/0092-8674(94)90426-X) (Pubitemid 24250812)
19. Zofall M, Yamanaka S, Reyes-Turcu FE, Zhang K, Rubin C, Grewal SI. 2012 RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335, 96-100. (doi:10.1126/science.1211651)
20. Sugiyama T, Sugioka-Sugiyama R. 2011 Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO J. 30, 1027-1039. (doi:10.1038/emboj.2011.32).
21. St-Andre O, Lemieux C, Perreault A, Lackner DH, Bahler J, Bachand F. 2010 Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J. Biol. Chem. 285, 27 859-27 868. (doi:10.1074/jbc.M110. 150748).
22. Gutz H, Heslot H, Leupold U, Loprieno N. 1974 Schizosaccharomyces pombe. In Handbook of genetics (ed. R. D. King), pp. 395-446. New York: Plenum Publishing Corporation.
23. Okazaki K, Okazaki N, Kume K, Jinno S, Tanaka K, Okayama H. 1990 High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by transcomplementation of Schizosaccharomyces pombe. Nucleic Acids Res. 18, 6485-6489. (doi:10.1093/ nar/18.22.6485)
24. Moreno S, Klar A, Nurse P. 1991 Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823. (doi:10.1016/ 0076-6879(91)94059-L)
25. Egel R, Egel-Mitani M. 1974 Premeiotic DNA synthesis in fission yeast. Exp. Cell Res. 88, 127-134. (doi:10.1016/0014-4827(74)90626-0)
26. Maundrell K. 1993 Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123, 127-130. (doi:10.1016/0378-1119(93)90551-D) (Pubitemid 23035804)
27. Kunkel TA. 1985 Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA 82, 488-492. (doi:10.1073/ pnas.82.2.488) (Pubitemid 15128292)
28. Yamashita A, Watanabe Y, Yamamoto M. 1997 Microtubule-associated coiled-coil protein Ssm4 is involved in the meiotic development in fission yeast. Genes Cells 2, 155-166. (doi:10.1046/j. 1365-2443.1997.1100307.x) (Pubitemid 127688566)
29. Hiriart E et al. Submitted. Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast.
30. Lao K, Xu NL, Yeung V, Chen C, Livak KJ, Straus NA. 2006 Multiplexing RT-PCR for the detection of multiple miRNA species in small samples. Biochem. Biophys. Res. Commun. 343, 85-89. (doi:10.1016/j.bbrc.2006.02.106)
31. Smith MJ, Pascal CE, Grauvogel Z, Habicht C, Seeb JE, Seeb LW. 2011 Multiplex preamplification PCR and microsatellite validation enables accurate single nucleotide polymorphism genotyping of historical fish scales. Mol. Ecol. Resourc. 11(Suppl. 1), 268-277. (doi:10.1111/j.1755-0998. 2010.02965.x)
32. Chen H-M, Futcher B, Leatherwood J. 2011 The fission yeast RNA binding protein MMi1 regulates meiotic genes by controlling intron specific splicing and polydenylation coupled RNA turnover. PLoS ONE 6, e26804. (doi:10.1371/pone. 0026804)