Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast

Nucleic Acids Research

Volumn 41, Issue 13, 2013, Pages 6674-6686

  Sugiyama, Tomoyasu ^a   Wanatabe, Nobuyoshi ^b   Kitahata, Eri ^b   Tani, Tokio ^b   Sugioka Sugiyama, Rie ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MESSENGER RNA; RED5 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MUTANT; CELL NUCLEUS; FLUORESCENCE IN SITU HYBRIDIZATION; FUNGUS GROWTH; GENE INTERACTION; GENE REPRESSION; MEIOSIS; NONHUMAN; NORTHERN BLOTTING; NUCLEAR PORE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RNA DEGRADATION; RNA STRUCTURE; SCHIZOSACCHAROMYCES POMBE; UPREGULATION; VEGETATIVE GROWTH; ZINC FINGER MOTIF;

CARRIER PROTEINS; CELL NUCLEOLUS; CELL NUCLEUS; DNA DAMAGE; MEIOSIS; MITOSIS; MUTATION; NUCLEAR PORE COMPLEX PROTEINS; PHEROMONES; POLY(A)-BINDING PROTEINS; PROTEIN STRUCTURE, TERTIARY; RNA STABILITY; RNA, MESSENGER; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SPORES, FUNGAL; TUBULIN MODULATORS; ZINC FINGERS;

EID: 84880521782     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt363     Document Type: Article

References (55)

1. Gamsjaeger, R., Liew, C.K., Loughlin, F.E., Crossley, M. and Mackay, J.P. (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem. Sci., 32, 63-70. (Pubitemid 46199196)
2. Le Provost, F., Lillico, S., Passet, B., Young, R., Whitelaw, B. and Vilotte, J.L. (2010) Zinc finger nuclease technology heralds a new era in mammalian transgenesis. Trends Biotechnol., 28, 134-141.
3. Yamamoto, M. (1996) Regulation of meiosis in fission yeast. Cell Struct. Funct., 21, 431-436. (Pubitemid 27068331)
4. Mata, J., Lyne, R., Burns, G. and Bahler, J. (2002) The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet., 32, 143-147. (Pubitemid 34977209)
5. Chikashige, Y., Tsutsumi, C., Yamane, M., Okamasa, K., Haraguchi, T. and Hiraoka, Y. (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell, 125, 59-69.
6. Harigaya, Y., Tanaka, H., Yamanaka, S., Tanaka, K., Watanabe, Y., Tsutsumi, C., Chikashige, Y., Hiraoka, Y., Yamashita, A. and Yamamoto, M. (2006) Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature, 442, 45-50. (Pubitemid 44064204)
7. McPheeters, D.S., Cremona, N., Sunder, S., Chen, H.M., Averbeck, N., Leatherwood, J. and Wise, J.A. (2009) A complex gene regulatory mechanism that operates at the nexus of multiple RNA processing decisions. Nat. Struct. Mol. Biol., 16, 255-264.
8. Chen, H.M., Futcher, B. and 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.
9. Yamanaka, S., Yamashita, A., Harigaya, Y., Iwata, R. and Yamamoto, M. (2010) Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO J., 29, 2173-2181.
10. St-Andre, O., Lemieux, C., Perreault, A., Lackner, D.H., Bahler, J. and Bachand, F. (2010) Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J. Biol. Chem., 285, 27859-27868.
11. Sugiyama, T. and Sugioka-Sugiyama, R. (2011) Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO J., 30, 1027-1039.
12. Yamashita, A., Shichino, Y., Tanaka, H., Hiriart, E., Touat-Todeschini, L., Vavasseur, A., Ding, D.Q., Hiraoka, Y., Verdel, A. and Yamamoto, M. (2012) Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes. Open Biol., 2, 120014.
13. Strambio-De-Castillia, C., Niepel, M. and Rout, M.P. (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell Biol., 11, 490-501.
14. Ryan, K.J. and Wente, S.R. (2000) The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr. Opin. Cell Biol., 12, 361-371. (Pubitemid 30265068)
15. Dieppois, G. and Stutz, F. (2010) Connecting the transcription site to the nuclear pore: a multi-tether process that regulates gene expression. J. Cell Sci., 123, 1989-1999.
16. Fasken, M.B. and Corbett, A.H. (2009) Mechanisms of nuclear mRNA quality control. RNA Biol., 6, 237-241.
17. Dauer, W.T. and Worman, H.J. (2009) The nuclear envelope as a signaling node in development and disease. Dev. Cell, 17, 626-638.
18. D'Angelo, M.A., Gomez-Cavazos, J.S., Mei, A., Lackner, D.H. and Hetzer, M.W. (2012) A change in nuclear pore complex composition regulates cell differentiation. Dev. Cell, 22, 446-458.
19. Lupu, F., Alves, A., Anderson, K., Doye, V. and Lacy, E. (2008) Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Dev. Cell, 14, 831-842. (Pubitemid 351757198)
20. Sugiyama, T., Sugioka-Sugiyama, R., Hada, K. and Niwa, R. (2012) Rhn1, a nuclear protein, is required for suppression of meiotic mRNAs in mitotically dividing fission yeast. PLoS One, 7, e42962.
21. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795-823.
22. Allshire, R.C., Javerzat, J.P., Redhead, N.J. and Cranston, G. (1994) Position effect variegation at fission yeast centromeres. Cell, 76, 157-169. (Pubitemid 24035289)
23. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. and Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol., 22, 1567-1572. (Pubitemid 40039460)
24. Ogawa, H., Yu, R.T., Haraguchi, T., Hiraoka, Y., Nakatani, Y., Morohashi, K. and Umesono, K. (2004) Nuclear structure-associated TIF2 recruits glucocorticoid receptor and its target DNA. Biochem. Biophys. Res. Commun., 320, 218-225. (Pubitemid 38786481)
25. Bahler, J., Wu, J.Q., Longtine, M.S., Shah, N.G., McKenzie, A. 3rd, Steever, A.B., Wach, A., Philippsen, P. and Pringle, J.R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14, 943-951. (Pubitemid 28328000)
26. Williams, J.S., Hayashi, T., Yanagida, M. and Russell, P. (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol. Cell, 33, 287-298.
27. Sugioka-Sugiyama, R. and Sugiyama, T. (2011) Sde2: a novel nuclear protein essential for telomeric silencing and genomic stability in Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun., 406, 444-448.
28. Sugiyama, T., Cam, H.P., Sugiyama, R., Noma, K., Zofall, M., Kobayashi, R. and Grewal, S.I. (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell, 128, 491-504. (Pubitemid 46198892)
29. Azad, A.K., Tani, T., Shiki, N., Tsuneyoshi, S., Urushiyama, S. and Ohshima, Y. (1997) Isolation and molecular characterization of mRNA transport mutants in Schizosaccharomyces pombe. Mol. Biol. Cell., 8, 825-841. (Pubitemid 27255025)
30. Gulli, M.P., Girard, J.P., Zabetakis, D., Lapeyre, B., Melese, T. and Caizergues-Ferrer, M. (1995) gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res., 23, 1912-1918.
31. Mandel, C.R., Bai, Y. and Tong, L. (2008) Protein factors in pre-mRNA 3'-end processing. Cell Mol. Life Sci., 65, 1099-1122.
32. Hurt, J.A., Obar, R.A., Zhai, B., Farny, N.G., Gygi, S.P. and Silver, P.A. (2009) A conserved CCCH-type zinc finger protein regulates mRNA nuclear adenylation and export. J. Cell. Biol., 185, 265-277.
33. Kim, D.U., Hayles, J., Kim, D., Wood, V., Park, H.O., Won, M., Yoo, H.S., Duhig, T., Nam, M., Palmer, G. et al. (2010) Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol., 28, 617-623.
34. Chinen, M., Morita, M., Fukumura, K. and Tani, T. (2010) Involvement of the spliceosomal U4 small nuclear RNA in heterochromatic gene silencing at fission yeast centromeres. J. Biol. Chem., 285, 5630-5638.
35. Goldar, M.M., Jeong, H.T., Tanaka, K., Matsuda, H. and Kawamukai, M. (2005) Moc3, a novel Zn finger type protein involved in sexual development, ascus formation, and stress response of Schizosaccharomyces pombe. Curr. Genet., 48, 345-355. (Pubitemid 43008715)
36. Wang, S.W., Asakawa, K., Win, T.Z., Toda, T. and Norbury, C.J. (2005) Inactivation of the pre-mRNA cleavage and polyadenylation factor Pfs2 in fission yeast causes lethal cell cycle defects. Mol. Cell Biol., 25, 2288-2296. (Pubitemid 40354625)
37. Thakurta, A.G., Gopal, G., Yoon, J.H., Kozak, L. and Dhar, R. (2005) Homolog of BRCA2-interacting Dss1p and Uap56p link Mlo3p and Rae1p for mRNA export in fission yeast. EMBO J., 24, 2512-2523. (Pubitemid 41076308)
38. Selvanathan, S.P., Thakurta, A.G., Dhakshnamoorthy, J., Zhou, M., Veenstra, T.D. and Dhar, R. (2010) Schizosaccharomyces pombe Dss1p is a DNA damage checkpoint protein that recruits Rad24p, Cdc25p, and Rae1p to DNA double-strand breaks. J. Biol. Chem., 285, 14122-14133.
39. Okuzaki, D., Kasama, T., Hirata, A., Ohtaka, A., Kakegawa, R. and Nojima, H. (2010) Spo5 phosphorylation is essential for its own timely degradation and for successful meiosis in Schizosaccharomyces pombe. Cell Cycle, 9, 3751-3760.
40. Amorim, M.J., Cotobal, C., Duncan, C. and Mata, J. (2010) Global coordination of transcriptional control and mRNA decay during cellular differentiation. Mol. Syst. Biol., 6, 380.
41. Watanabe, Y. and 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. (Pubitemid 24250812)
42. Yamamoto, M. (2010) The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 86, 788-797.
43. Yamamoto, A. and Hiraoka, Y. (2003) Monopolar spindle attachment of sister chromatids is ensured by two distinct mechanisms at the first meiotic division in fission yeast. EMBO J., 22, 2284-2296. (Pubitemid 36565551)
44. Andoh, T., Azad, A.K., Shigematsu, A., Ohshima, Y. and Tani, T. (2004) The fission yeast ptr1+ gene involved in nuclear mRNA export encodes a putative ubiquitin ligase. Biochem. Biophys. Res. Commun., 317, 1138-1143. (Pubitemid 38496428)
45. Brown, J.A., Bharathi, A., Ghosh, A., Whalen, W., Fitzgerald, E. and Dhar, R. (1995) A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J. Biol. Chem., 270, 7411-7419.
46. Tatebayashi, K., Tani, T. and Ikeda, H. (2001) Fission yeast Mog1p homologue, which interacts with the small GTPase Ran, is required for mitosis-to-interphase transition and poly(A)(+) RNA metabolism. Genetics, 157, 1513-1522. (Pubitemid 32298821)
47. Murphy, R., Watkins, J.L. and Wente, S.R. (1996) GLE2, a Saccharomyces cerevisiae homologue of the Schizosaccharomyces pombe export factor RAE1, is required for nuclear pore complex structure and function. Mol. Biol. Cell, 7, 1921-1937. (Pubitemid 26415000)
48. Singer, S., Zhao, R., Barsotti, A.M., Ouwehand, A., Fazollahi, M., Coutavas, E., Breuhahn, K., Neumann, O., Longerich, T., Pusterla, T. et al. (2012) Nuclear pore component Nup98 is a potential tumor suppressor and regulates posttranscriptional expression of select p53 target genes. Mol. Cell, 48, 799-810.
49. Schmid, M., Poulsen, M.B., Olszewski, P., Pelechano, V., Saguez, C., Gupta, I., Steinmetz, L.M., Moore, C. and Jensen, T.H. (2012) Rrp6p controls mRNA poly(A) tail length and its decoration with poly(A) binding proteins. Mol. Cell, 47, 267-280.
50. Mannen, T., Andoh, T. and Tani, T. (2008) Dss1 associating with the proteasome functions in selective nuclear mRNA export in yeast. Biochem. Biophys. Res. Commun., 365, 664-671. (Pubitemid 350234842)
51. Zhang, K., Fischer, T., Porter, R.L., Dhakshnamoorthy, J., Zofall, M., Zhou, M., Veenstra, T. and Grewal, S.I. (2011) Clr4/Suv39 and RNA quality control factors cooperate to trigger RNAi and suppress antisense RNA. Science, 331, 1624-1627.
52. Vanacova, S. and Stefl, R. (2007) The exosome and RNA quality control in the nucleus. EMBO Rep., 8, 651-657. (Pubitemid 47033796)
53. Bai, S.W., Rouquette, J., Umeda, M., Faigle, W., Loew, D., Sazer, S. and Doye, V. (2004) The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Mol. Cell Biol., 24, 6379-6392. (Pubitemid 38891137)
54. Yoon, J.H., Whalen, W.A., Bharathi, A., Shen, R. and Dhar, R. (1997) Npp106p, a Schizosaccharomyces pombe nucleoporin similar to Saccharomyces cerevisiae Nic96p, functionally interacts with Rae1p in mRNA export. Mol. Cell Biol., 17, 7047-7060. (Pubitemid 27505934)
55. Hessle, V., von Euler, A., Gonzalez de Valdivia, E. and Visa, N. (2012) Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore. RNA, 18, 1466-1474.