SUS1 introns are required for efficient mRNA nuclear export in yeast

Nucleic Acids Research

Volumn 39, Issue 19, 2011, Pages 8599-8611

  Cuenca Bono, Bernardo ^a   García Molinero, Varinia ^a   Pascual García, Pau ^a,d   Dopazo, Hernan ^a   Llopis, Ana ^a   Vilardell, Josep ^b,c   Rodríguez Navarro, Susana ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; ISOPROTEIN; MESSENGER RNA; SUS1 PROTEIN; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL GROWTH; CONTROLLED STUDY; EXON; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; INTRON; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; RNA SYNTHESIS; RNA TRANSLATION; WESTERN BLOTTING; YEAST;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; EVOLUTION, MOLECULAR; EXONS; GENE EXPRESSION REGULATION, FUNGAL; INTRONS; NONSENSE MEDIATED MRNA DECAY; NUCLEAR PROTEINS; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 80455168362     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr496     Document Type: Article

References (44)

1. Perales, R. and Bentley, D. (2009) "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell, 36, 178-191.
2. Moore, M.J. and Proudfoot, N.J. (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell, 136, 688-700.
3. Pascual-Garcia, P. and Rodriguez-Navarro, S. (2009) A tale of coupling, Sus1 function in transcription and mRNA export. RNA Biol., 6, 141-144.
4. Kopytova, D.V., Krasnov, A.N., Orlova, A.V., Gurskiy, D.Y., Nabirochkina, E.N., Georgieva, S.G. and Shidlovskii, Y.V. (2010) ENY2: couple, triple. . .more? Cell Cycle, 9, 479-481.
5. Kohler, A., Pascual-Garcia, P., Llopis, A., Zapater, M., Posas, F., Hurt, E. and Rodriguez-Navarro, S. (2006) The mRNA export factor Sus1 is involved in Spt/Ada/Gcn5 acetyltransferase-mediated H2B deubiquitinylation through its interaction with Ubp8 and Sgf11. Mol. Biol. Cell, 17, 4228-4236.
6. Kohler, A., Schneider, M., Cabal, G.G., Nehrbass, U. and Hurt, E. (2008) Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat. Cell. Biol., 10, 707-715.
7. Samara, N.L., Datta, A.B., Berndsen, C.E., Zhang, X., Yao, T., Cohen, R.E. and Wolberger, C. (2010) Structural insights into the assembly and function of the SAGA deubiquitinating module. Science, 328, 1025-1029.
8. Kohler, A., Zimmerman, E., Schneider, M., Hurt, E. and Zheng, N. (2010) Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module. Cell, 141, 606-617.
9. Pascual-Garcia, P., Govind, C.K., Queralt, E., Cuenca-Bono, B., Llopis, A., Chavez, S., Hinnebusch, A.G. and Rodriguez-Navarro, S. (2008) Sus1 is recruited to coding regions and functions during transcription elongation in association with SAGA and TREX2. Genes Dev., 22, 2811-2822.
10. Rodriguez-Navarro, S., Fischer, T., Luo, M.J., Antunez, O., Brettschneider, S., Lechner, J., Perez-Ortin, J.E., Reed, R. and Hurt, E. (2004) Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell, 116, 75-86.
11. Faza, M.B., Kemmler, S., Jimeno, S., Gonzalez-Aguilera, C., Aguilera, A., Hurt, E. and Panse, V.G. (2009) Sem1 is a functional component of the nuclear pore complex-associated messenger RNA export machinery. J. Cell. Biol., 184, 833-846.
12. Luna, R., Gonzalez-Aguilera, C. and Aguilera, A. (2009) Transcription at the proximity of the nuclear pore: a role for the THP1-SAC3-SUS1-CDC31 (THSC) complex. RNA Biol., 6, 145-148.
13. Cabal, G.G., Genovesio, A., Rodriguez-Navarro, S., Zimmer, C., Gadal, O., Lesne, A., Buc, H., Feuerbach-Fournier, F., Olivo-Marin, J.C., Hurt, E.C. et al. (2006) SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature, 441, 770-773.
14. Cuenca-Bono, B., Garcia-Molinero, V., Pascual-Garcia, P., Garcia-Oliver, E., Llopis, A. and Rodriguez-Navarro, S. (2010) A novel link between Sus1 and the cytoplasmic mRNA decay machinery suggests a broad role in mRNA metabolism. BMC Cell. Biol., 11, 19.
15. Hossain, M.A., Rodriguez, C.M. and Johnson, T.L. (2011) Key features of the two-intron Saccharomyces cerevisiae gene SUS1 contribute to its alternative splicing. Nuc. Acids Res., this issue.
16. Meyer, M. and Vilardell, J. (2009) The quest for a message: budding yeast, a model organism to study the control of pre-mRNA splicing. Brief. Funct. Genomic Proteomic, 8, 60-67.
17. Parenteau, J., Durand, M., Veronneau, S., Lacombe, A.A., Morin, G., Guerin, V., Cecez, B., Gervais-Bird, J., Koh, C.S., Brunelle, D. et al. (2008) Deletion of many yeast introns reveals a minority of genes that require splicing for function. Mol. Biol. Cell, 19, 1932-1941.
18. Juneau, K., Nislow, C. and Davis, R.W. (2009) Alternative splicing of PTC7 in Saccharomyces cerevisiae determines protein localization. Genetics, 183, 185-194.
19. Grund, S.E., Fischer, T., Cabal, G.G., Antunez, O., Perez-Ortin, J.E. and Hurt, E. (2008) The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J. Cell. Biol., 182, 897-910.
20. Rodriguez-Navarro, S., Strasser, K. and Hurt, E. (2002) An intron in the YRA1 gene is required to control Yra1 protein expression and mRNA export in yeast. EMBO Rep., 3, 438-442.
21. Preker, P.J. and Guthrie, C. (2006) Autoregulation of the mRNA export factor Yra1p requires inefficient splicing of its pre-mRNA. RNA, 12, 994-1006.
22. Preker, P.J., Kim, K.S. and Guthrie, C. (2002) Expression of the essential mRNA export factor Yra1p is autoregulated by a splicing-dependent mechanism. RNA, 8, 969-980.
23. Dong, S., Jacobson, A. and He, F. (2010) Degradation of YRA1 Pre-mRNA in the cytoplasm requires translational repression, multiple modular intronic elements, Edc3p, and Mex67p. PLoS Biol., 8, e1000360.
24. Dong, S., Li, C., Zenklusen, D., Singer, R.H., Jacobson, A. and He, F. (2007) YRA1 autoregulation requires nuclear export and cytoplasmic Edc3p-mediated degradation of its pre-mRNA. Mol. Cell, 25, 559-573.
25. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
26. Lopez, R., Silventoinen, V., Robinson, S., Kibria, A. and Gish, W. (2003) WU-Blast2 server at the European Bioinformatics Institute. Nucleic Acids Res., 31, 3795-3798.
27. Marcet-Houben, M. and Gabaldon, T. (2009) The tree versus the forest: the fungal tree of life and the topological diversity within the yeast phylome. PLoS One, 4, e4357.
28. Cracraft, J. and Donoghue, M.J. (2004) Assembling The Tree of Life. Oxford University Press, Oxford, UK.
29. Maddison, D.R. and Maddison, W.P. (2000), MacClade. Versio'n 4. Sinauer Associates, Sunderland, MA.
30. Gietz, R.D. and Schiestl, R.H. (2007) Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc., 2, 35-37.
31. Lesser, C.F. and Guthrie, C. (1993) Mutational analysis of pre-mRNA splicing in Saccharomyces cerevisiae using a sensitive new reporter gene, CUP1. Genetics, 133, 851-863.
32. Schmitt, M.E., Brown, T.A. and Trumpower, B.L. (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res., 18, 3091-3092.
33. Macias, S., Bragulat, M., Tardiff, D.F. and Vilardell, J. (2008) L30 binds the nascent RPL30 transcript to repress U2 snRNP recruitment. Mol. Cell, 30, 732-742.
34. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M. and Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320, 1344-1349.
35. Zhang, Z., Hesselberth, J.R. and Fields, S. (2007) Genome-wide identification of spliced introns using a tiling microarray. Genome Res., 17, 503-509.
36. Juneau, K., Palm, C., Miranda, M. and Davis, R.W. (2007) High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc. Natl Acad. Sci. USA, 104, 1522-1527.
37. Miura, F., Kawaguchi, N., Sese, J., Toyoda, A., Hattori, M., Morishita, S. and Ito, T. (2006) A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc. Natl Acad. Sci. USA, 103, 17846-17851.
38. Yassour, M., Kaplan, T., Fraser, H.B., Levin, J.Z., Pfiffner, J., Adiconis, X., Schroth, G., Luo, S., Khrebtukova, I., Gnirke, A. et al. (2009) Ab initio construction of a eukaryotic transcriptome by massively parallel mRNA sequencing. Proc. Natl Acad. Sci. USA, 106, 3264-3269.
39. Clark, T.A., Sugnet, C.W. and Ares, M. Jr (2002) Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science, 296, 907-910.
40. Wang, Q., Zhang, L., Lynn, B. and Rymond, B.C. (2008) A BBP-Mud2p heterodimer mediates branchpoint recognition and influences splicing substrate abundance in budding yeast. Nucleic Acids Res., 36, 2787-2798.
41. Johansson, M.J., He, F., Spatrick, P., Li, C. and Jacobson, A. (2007) Association of yeast Upf1p with direct substrates of the NMD pathway. Proc. Natl Acad. Sci. USA, 104, 20872-20877.
42. Bartel, P.L. and Fields, S. (1995) Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol., 254, 241-263.
43. Muhlrad, D. and Parker, R. (1999) Aberrant mRNAs with extended 30 UTRs are substrates for rapid degradation by mRNA surveillance. RNA, 5, 1299-1307.
44. Ast, G. (2004) How did alternative splicing evolve? Nat. Rev. Genet., 5, 773-782.