Multifunctional factor ENY2 is associated with the THO complex and promotes its recruitment onto nascent mRNA

Genes and Development

Volumn 24, Issue 1, 2010, Pages 86-96

  Kopytova, Daria V ^a   Orlova, Anastasija V ^a   Krasnov, Alexey N ^a,b   Gurskiy, Dmitriy Ya ^a   Nikolenko, Julia V ^a   Nabirochkina, Elena N ^a   Shidlovskii, Yulii V ^a,b   Georgieva, Sofia G ^a,c  

^a INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^b UNIVERSITY OF OSLO   (Norway)

^c ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

ENY2; Gene expression; mRNA export; mRNP formation; Protein complex; THO

Indexed keywords

HEAT SHOCK PROTEIN 70; MESSENGER RNA; PROTEIN THO; REGULATOR PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AMEX; TRANSCRIPTION FACTOR ENY2; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

ANIMALS; CHROMOSOMES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE KNOCKDOWN TECHNIQUES; HSP70 HEAT-SHOCK PROTEINS; MUTATION; PHENOTYPE; PROTEIN BINDING; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

METAZOA;

EID: 73549090359     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.550010     Document Type: Article

References (44)

1. Abruzzi KC, Lacadie S, Rosbash M. 2004. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J 23: 2620-2631.
2. Baroni TE, Chittur SV, George AD, Tenenbaum SA. 2008. Advances in RIP-chip analysis: RNA-binding protein immunoprecipitation-microarray profiling. Methods Mol Biol 419:93-108.
3. Boehm AK, Saunders A, Werner J, Lis JT. 2003. Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock. Mol Cell Biol 23: 7628-7637.
4. Bruhn L, Munnerlyn A, Grosschedl R. 1997. ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRα enhancer function. Genes & Dev 11: 640-653.
5. 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.
6. Carre C, Szymczak D, Pidoux J, Antoniewski C. 2005. The histone H3 acetylase dGCN5 is a key player in Drosophila melanogaster metamorphosis. Mol Cell Biol 25: 8228-8238.
7. Chavez S, Beilharz T, Rondon AG, Erdjument-Bromage H, Tempst P, Svejstrup JQ, Lithgow T, Aguilera A. 2000. A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J 19: 5824-5834.
8. Chekanova JA, Abruzzi KC, Rosbash M, Belostotsky DA. 2008. Sus1, Sac3, and Thp1 mediate post-transcriptional tethering of active genes to the nuclear rim as well as to non-nascent mRNP. RNA 14: 66-77.
9. Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R. 2006. Human mRNA export machinery recruited to the 59 end of mRNA. Cell 127: 1389-1400.
10. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, Hemmings BA, Dixon JE. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci 97: 6499-6503.
11. Demeny MA, Soutoglou E, Nagy Z, Scheer E, Janoshazi A, Richardot M, Argentini M, Kessler P, Tora L. 2007. Identification of a small TAF complex and its role in the assembly of TAF-containing complexes. PLoS One 2: e316. doi: 10.1371/ journal.pone.0000316.
12. 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.
13. Georgiev PG, Gerasimova TI. 1989. Novel genes influencing the expression of the yellow locus and mdg4 (gypsy) in Drosophila melanogaster. Mol Gen Genet 220: 121-126.
14. Georgieva S, Kirschner DB, Jagla T, Nabirochkina E, Hanke S, Schenkel H, de Lorenzo C, Sinha P, Jagla K, Mechler B, et al. 2000. Two novel Drosophila TAF(II)s have homology with human TAF(II)30 and are differentially regulated during development. Mol Cell Biol 20: 1639-1648.
15. Georgieva S, Nabirochkina E, Dilworth FJ, Eickhoff H, Becker P, Tora L, Georgiev P, Soldatov A. 2001. The novel transcription factor e(y)2 interacts with TAF(II)40 and potentiates transcription activation on chromatin templates. Mol Cell Biol 21: 5223-5231.
16. Gonzalez-Aguilera C, Tous C, Gomez-Gonzalez B, Huertas P, Luna R, Aguilera A. 2008. The THP1-SAC3-SUS1-CDC31 complex works in transcription elongation-mRNA export preventing RNA-mediated genome instability. Mol Biol Cell 19: 4310-4318.
17. Huertas P, Aguilera A. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12: 711-721.
18. Iglesias N, Stutz F. 2008. Regulation of mRNP dynamics along the export pathway. FEBS Lett 582: 1987-1996.
19. Jani D, Lutz S, Marshall NJ, Fischer T, Kohler A, Ellisdon AM, Hurt E, Stewart M. 2009. Sus1, Cdc31, and the Sac3 CID region form a conserved interaction platform that promotes nuclear pore association and mRNA export. Mol Cell 33: 727-737.
20. Jimeno S, Rondon AG, Luna R, Aguilera A. 2002. The yeast THO complex and mRNA export factors link RNA metabolism with transcription and genome instability. EMBO J 21: 3526-3535.
21. Jimeno S, Luna R, Garcia-Rubio M, Aguilera A. 2006. Tho1, a novel hnRNP, and Sub2 provide alternative pathways for mRNP biogenesis in yeast THO mutants. Mol Cell Biol 26: 4387-4398.
22. Jimeno S, Garcia-Rubio M, Luna R, Aguilera A. 2008. A reduction in RNA polymerase II initiation rate suppresses hyper-recombination and transcription-elongation impairment of THO mutants. Mol Genet Genomics 280: 327-336.
23. Katahira J, Inoue H, Hurt E, Yoneda Y. 2009. Adaptor Aly and co-adaptor Thoc5 function in the Tap-p15-mediated nuclear export of HSP70 mRNA. EMBO J 28: 556-567.
24. Kim M, Ahn SH, Krogan NJ, Greenblatt JF, Buratowski S. 2004. Transitions in RNA polymerase II elongation complexes at the 3' ends of genes. EMBO J 23: 354-364.
25. Kohler A, Pascual-Garcia P, Llopis A, Zapater M, Posas F, Hurt E, 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.
26. Krasnov AN, Kurshakova MM, Ramensky VE, Mardanov PV, Nabirochkina EN, Georgieva SG. 2005. A retrocopy of a gene can functionally displace the source gene in evolution. Nucleic Acids Res 33: 6654-6661.
27. Kurshakova M, Maksimenko O, Golovnin A, Pulina M, Georgieva S, Georgiev P, Krasnov A. 2007. Evolutionarily conserved E(y)2/ Sus1 protein is essential for the barrier activity of Su(Hw)-dependent insulators in Drosophila. Mol Cell 27: 332-338.
28. Kurshakova MM, Krasnov AN, Kopytova DV, Shidlovskii YV, Nikolenko JV, Nabirochkina EN, Spehner D, Schultz P, Tora L, Georgieva SG. 2007. SAGA and a novel Drosophila export complex anchor efficient transcription and mRNA export to NPC. EMBO J 26: 4956-4965.
29. Kusch T, Guelman S, Abmayr SM, Workman JL. 2003. Two Drosophila Ada2 homologues function in different multi-protein complexes. Mol Cell Biol 23: 3305-3319.
30. Lebedeva LA, Nabirochkina EN, Kurshakova MM, Robert F, Krasnov AN, Evgen'ev MB, Kadonaga JT, Georgieva SG, Tora L. 2005. Occupancy of the Drosophila hsp70 promoter by a subset of basal transcription factors diminishes upon transcriptional activation. Proc Natl Acad Sci 102: 18087-18092.
31. Masuda S, Das R, Cheng H, Hurt E, Dorman N, Reed R. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes & Dev 19: 1512-1517.
32. Mohrmann L, Verrijzer CP. 2005. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta-Gene Struct. Exp. 1681: 59-73.
33. Pascual-Garcia P, Govind CK, Queralt E, Cuenca-Bono B, Llopis A, Chavez S, Hinnebusch AG, 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.
34. Rasmussen EB, Lis JT. 1993. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci 90: 7923-7927.
35. Rehwinkel J, Herold A, Gari K, Kocher T, Rode M, Ciccarelli FL, Wilm M, Izaurralde E. 2004. Genome-wide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat Struct Mol Biol 11: 558-566.
36. Rodriguez-Navarro S, Fischer T, Luo MJ, Antunez O, Brettschneider S, Lechner J, Perez-Ortin JE, Reed R, 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.
37. Rougemaille M, Dieppois G, Kisseleva-Romanova E, Gudipati RK, Lemoine S, Blugeon C, Boulay J, Jensen TH, Stutz F, Devaux F, et al. 2008. THO/Sub2p functions to coordinate 3'-end processing with gene-nuclear pore association. Cell 135: 308-321.
38. Saguez C, Schmid M, Olesen JR, Ghazy MA, Qu X, Poulsen MB, Nasser T, Moore C, Jensen TH. 2008. Nuclear mRNA surveillance in THO/sub2 mutants is triggered by inefficient polyadenylation. Mol Cell 31: 91-103.
39. Soldatov A, Nabirochkina E, Georgieva S, Belenkaja T, Georgiev P. 1999. TAFII40 protein is encoded by the e(y)1 gene: Biological consequences of mutations. Mol Cell Biol 19: 3769-3778.
40. Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez-Navarro S, Rondon AG, Aguilera A, Struhl K, Reed R, et al. 2002. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417: 304-308.
41. Tenenbaum SA, Carson CC, Lager PJ, Keene JD. 2000. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci 97: 14085-14090.
42. Vorobyeva NE, Soshnikova NV, Nikolenko JV, Kuzmina JL, Nabirochkina EN, Georgieva SG, Shidlovskii YV. 2009. Transcription coactivator SAYP combines chromatin remodeler Brahma and transcription initiation factor TFIID into a single supercomplex. Proc Natl Acad Sci 106: 11049-11054.
43. Zenklusen D, Vinciguerra P, Wyss JC, Stutz F. 2002. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol Cell Biol 22: 8241-8253.
44. Zhao Y, Lang G, Ito S, Bonnet J, Metzger E, Sawatsubashi S, Suzuki E, Le Guezennec X, Stunnenberg HG, Krasnov A, et al. 2008. A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol Cell 29: 92-101.