A nucleoporin, Nup60p, affects the nuclear and cytoplasmic localization of ASH1 mRNA in S. cerevisiae

RNA

Volumn 17, Issue 1, 2011, Pages 134-144

  Powrie, Erin A ^a,b   Zenklusen, Daniel ^a,c   Singer, Robert H ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

ASH1; In situ hybridization; mRNA export; NUP60; RNA localization

Indexed keywords

MESSENGER RNA; NUCLEOPORIN; NUCLEOPORIN 60P; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; BUD; CELL BUDDING; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; FLUORESCENCE IN SITU HYBRIDIZATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

CELL NUCLEUS; CYTOPLASM; GENE DELETION; IN SITU HYBRIDIZATION, FLUORESCENCE; NUCLEAR PORE COMPLEX PROTEINS; POLY A; REPRESSOR PROTEINS; RNA TRANSPORT; RNA, FUNGAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

SACCHAROMYCETALES;

EID: 78650424316     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1210411     Document Type: Article

References (65)

1. Abruzzi KC, Belostotsky DA, Chekanova JA, Dower K, Rosbash M. 2006. 39-End formation signals modulate the association of genes with the nuclear periphery as well as mRNP dot formation. EMBO J 25: 4253-4262.
2. Barta I, Iggo R. 1995. Autoregulation of expression of the yeast Dbp2p 'DEAD-box' protein is mediated by sequences in the conserved DBP2 intron. EMBO J 14: 3800-3808.
3. Beach DL, Salmon ED, Bloom K. 1999. Localization and anchoring of mRNA in budding yeast. Curr Biol 9: 569-578.
4. Brickner JH, Walter P. 2004. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol 2: e342. doi: 10.1371/ journal.pbio.0020342. (Pubitemid 40280482)
5. Brodsky AS, Silver PA. 2000. Pre-mRNA processing factors are required for nuclear export. RNA 6: 1737-1749.
6. Bystricky K, Van Attikum H, Montiel M-D, Dion V, Gehlen L, Gasser SM. 2009. Regulation of nuclear positioning and dynamics of the silent mating type loci by the yeast Ku70/Ku80 complex. Mol Cell Biol 29: 835-848.
7. Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin JC, Hurt EC, et al. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441: 770-773.
8. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA. 2004. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117: 427-439.
9. Chartrand P, Meng XH, Huttelmaier S, Donato D, Singer RH. 2002. Asymmetric sorting of Ash1p in yeast results from inhibition of translation by localization elements in the mRNA. Mol Cell 10: 1319-1330.
10. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ, et al. 1998. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2: 65-73.
11. Deng Y, Singer RH, Gu W. 2008. Translation of ASH1 mRNA is repressed by Puf6p-Fun12p/eIF5B interaction and released by CK2 phosphorylation. Genes Dev 22: 1037-1050.
12. Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A. 2006. Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci 103: 2172-2177.
13. Dieppois G, 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.
14. Dilworth DJ, Suprapto A, Padovan JC, Chait BT, Wozniak RW, Rout MP, Aitchison JD. 2001. Nup2p dynamically associates with the distal regions of the yeast nuclear pore complex. J Cell Biol 153: 1465-1478.
15. Dilworth DJ, Tackett AJ, Rogers RS, Yi EC, Christmas RH, Smith JJ, Siegel AF, Chait BT, Wozniak RW, Aitchison JD. 2005. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J Cell Biol 171: 955-965.
16. Dockendorff TC, Heath CV, Goldstein AL, Snay CA, Cole CN. 1997. C-terminal truncations of the yeast nucleoporin Nup145p produce a rapid temperature-conditional mRNA export defect and alterations to nuclear structure. Mol Cell Biol 17: 906-920.
17. Dong S, Li C, Zenklusen D, Singer RH, Jacobson A, He F. 2007. YRA1 autoregulation requires nuclear export and cytoplasmic Edc3pmediated degradation of its pre-mRNA. Mol Cell 25: 559-573.
18. Du T-G, Schmid M, Jansen R-P. 2007. Why cells move messages: The biological functions of mRNA localization. Semin Cell Dev Biol 18: 171-177.
19. Farina KL and Singer RH. 2002. The nuclear connection in RNA transport and localization. Trends Cell Biol 12: 466-472.
20. Fischer T, Strasser K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P, Lechner J, Hurt E. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21: 5843-5852.
21. Galy V, Gadal O, Fromont-Racine M, Romano A, Jacquier A, Nehrbass U. 2004. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 116: 63-73.
22. Gerber AP, Herschlag D, Brown PO. 2004. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2: e79. doi: 10.1371/ journal.pbio.0020079. (Pubitemid 39234531)
23. Gorsch LC, Dockendorff TC, Cole CN. 1995. A conditional allele of the novel repeat-containing yeast nucleoporin RAT7/NUP159 causes both rapid cessation of mRNA export and reversible clustering of nuclear pore complexes. J Cell Biol 129: 939-955.
24. Gu W, Pan F, Zhang H, Bassell GJ, Singer RH. 2002. A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J Cell Biol 156: 41-51.
25. Gu W, Deng Y, Zenklusen D, Singer RH. 2004. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev 18: 1452-1465.
26. Heath CV, Copeland CS, Amberg DC, Del Priore V, Snyder M, Cole CN. 1995. Nuclear pore complex clustering and nuclear accumulation of poly(A)+ RNA associated with mutation of the Saccharomyces cerevisiae RAT2/NUP120 gene. J Cell Biol 131: 1677-1697.
27. Hediger F, Neumann FR, Van Houwe G, Dubrana K, Gasser SM. 2002. Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr Biol 12: 2076-2089.
28. Hieronymus H, Silver PA. 2003. Genome-wide analysis of RNAprotein interactions illustrates specificity of the mRNA export machinery. Nat Genet 33: 155-161.
29. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717-728.
30. Hood JK, Casolari JM, Silver PA. 2000. Nup2p is located on the nuclear side of the nuclear pore complex and coordinates Srp1p/ importin-a export. J Cell Sci 113: 1471-1480.
31. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exosome. Natl Rev 7: 529-539.
32. Huisinga KL, Pugh BF. 2004. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 13: 573-585.
33. Irie K, Tadauchi T, Takizawa PA, Vale RD, Matsumoto K, Herskowitz I. 2002. The Khd1 protein, which has three KH RNA-binding motifs, is required for proper localization of ASH1 mRNA in yeast. EMBO J 21: 1158-1167.
34. Jansen RP, Dowzer C, Michaelis C, Galova M, Nasmyth K. 1996. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Cell 84: 687-697.
35. Jensen TH, Patricio K, McCarthy T, Rosbash M. 2001. A block to mRNA nuclear export in S. cerevisiae leads to hyperadenylation of transcripts that accumulate at the site of transcription. Mol Cell 7: 887-898.
36. Keene JD. 2007. RNA regulons: Coordination of post-transcriptional events. Nat Rev Genet 8: 533-543.
37. Kruse C, Jaedicke A, Beaudouin J, Bohl F, Ferring D, Guttler T, Ellenberg J, Jansen RP. 2002. Ribonucleoprotein-dependent localization of the yeast class V myosin Myo4p. J Cell Biol 159: 971-982.
38. Larson DR, Singer RH, Zenklusen D. 2009. A single molecule view of gene expression. Trends Cell Biol 19: 630-637
39. Li O, Heath CV, Amberg DC, Dockendorff TC, Copeland CS, Snyder M, Cole CN. 1995. Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes. Mol Biol Cell 6: 401-417.
40. Libri D, Dower K, Boulay J, Thomsen R, Rosbash M, Jensen TH. 2002. Interactions between mRNA export commitment, 39-end quality control, and nuclear degradation. Mol Cell Biol 22: 8254-8266.
41. Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen RP. 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science (New York, NY) 277: 383-387.
42. Long RM, Gu W, Meng X, Gonsalvez G, Singer RH, Chartrand P. 2001. An exclusively nuclear RNA-binding protein affects asymmetric localization of ASH1 mRNA and Ash1p in yeast. J Cell Biol 153: 307-318.
43. Niessing D, Hüttelmaier S, Zenklusen D, Singer RH, Burley SK. 2004. She2p is a novel RNA binding protein with a basic helical hairpin motif. Cell 119: 491-502.
44. Palancade B, Zuccolo M, Loeillet S, Nicolas A, Doye V. 2005. Pml39, a novel protein of the nuclear periphery required for nuclear retention of improper messenger ribonucleoparticles. Mol Biol Cell 16: 5258-5268.
45. Paquin N, Menade M, Poirier G, Donato D, Drouet E, Chartrand P. 2007. Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p. Mol Cell 26: 795-809.
46. Pemberton LF, Rout MP, Blobel G. 1995. Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc Natl Acad Sci 92: 1187-1191.
47. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. 2000. The yeast nuclear pore complex: Composition, architecture, and transport mechanism. J Cell Biol 148: 635-651.
48. Saavedra C, Tung KS, Amberg DC, Hopper AK, Cole CN. 1996. Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev 10: 1608-1620.
49. Saavedra CA, Hammell CM, Heath CV, Cole CN. 1997. Yeast heat shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev 11: 2845-2856.
50. Sarma NJ, Haley TM, Barbara KE, Buford TD, Willis KA, Santangelo GM. 2007. Glucose-responsive regulators of gene expression in Saccharomyces cerevisiae function at the nuclear periphery via a reverse recruitment mechanism. Genetics 175: 1127-1135.
51. Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli UK. 2006. Nup-PI: The nucleopore-promoter interaction of genes in yeast. Mol Cell 21: 379-391.
52. Segref A, Sharma K, Doye V, Hellwig A, Huber J, Luhrmann R, Hurt E. 1997. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J 16: 3256-3271.
53. Shen Z, Paquin N, Forget A, Chartrand P. 2009. Nuclear shuttling of She2p couples ASH1 mRNA localization to its translational repression by recruiting Loc1p and Puf6p. Mol Biol Cell 20: 2265-2275.
54. Shen Z, St-Denis A, Chartrand P. 2010. Cotranscriptional recruitment of She2p by RNA pol II elongation factor Spt4-Spt5/DSIF promotes mRNA localization to the yeast bud. Genes Dev 24: 1914-1926.
55. Shepard KA, Gerber AP, Jambhekar A, Takizawa PA, Brown PO, Herschlag D, DeRisi JL, Vale RD. 2003. Widespread cytoplasmic mRNA transport in yeast: Identification of 22 bud-localized transcripts using DNA microarray analysis. Proc Natl Acad Sci 100: 11429-11434.
56. Skružný M, Schneider C, Rácz A, Weng J, Tollervey D, Hurt E. 2009. An endoribonuclease functionally linked to perinuclear mRNP quality control associates with the nuclear pore complexes. PLoS Biol 7: e8. doi: 10.1371/journal.pbio.1000008.
57. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9: 3273-3297.
58. Strasser K, Hurt E. 2000. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 19: 410-420.
59. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM. 2006. Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441: 774-778.
60. Takizawa PA, Sil A, Swedlow JR, Herskowitz I, Vale RD. 1997. Actindependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389: 90-93.
61. Thomsen R, Libri D, Boulay J, Rosbash M, Jensen TH. 2003. Localization of nuclear retained mRNAs in Saccharomyces cerevisiae. RNA 9: 1049-1057.
62. Tran EJ, Wente SR. 2006. Dynamic nuclear pore complexes: Life on the edge. Cell 125: 1041-1053.
63. Zenklusen D, Singer RH. 2010. Analyzing mRNA expression using single mRNA resolution fluorescent in situ hybridization. In Methods in enzymology (ed. W Jonathan, G Christine, and RF Gerald), Vol. 470, pp. 641-659. Academic, New York.
64. Zenklusen D, Larson DR, Singer RH. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat Struct Mol Biol 15: 1263-1271.
65. Zhao X, Wu CY, Blobel G. 2004. Mlp-dependent anchorage and stabilization of a desumoylating enzyme is required to prevent clonal lethality. J Cell Biol 167: 605-611.