Mutational analysis of the yeast RNA helicase Sub2p reveals conserved domains required for growth, mRNA export, and genomic stability

RNA

Volumn 19, Issue 10, 2013, Pages 1363-1371

  Saguez, Cyril ^a   Gonzales, Fernando A ^a,c   Schmid, Manfred ^a   Bøggild, Andreas ^a   Latrick, Chrysa M ^a,d   Malagon, Francisco ^a,e   Putnam, Andrea ^b   Sanderson, Lee ^a   Jankowsky, Eckhard ^b   Brodersen, Ditlev E ^a   Jensen, Torben Heick ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^e NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Genome stability; RNA; RNA export; RNA helicase

Indexed keywords

ADENOSINE TRIPHOSPHATE; MESSENGER RNA; POLYADENYLATED RNA; PROTEIN SUB2P; RNA HELICASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS; CHROMATIN; DNA RECOMBINATION; FUNGUS GROWTH; GENE; GENE LOCUS; GENE MUTATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; MUTANT; NONHUMAN; NUCLEAR EXPORT SIGNAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; SUB2 GENE; WILD TYPE;

GENOME STABILITY; RNA; RNA EXPORT; RNA HELICASE;

ADENOSINE TRIPHOSPHATASES; BLOTTING, WESTERN; CELL NUCLEUS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENOMIC INSTABILITY; MUTATION; RNA TRANSPORT; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 84884681783     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.040048.113     Document Type: Article

References (47)

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. (Pubitemid 38988233)
2. Aguilera A, Klein HL. 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119: 779-790.
3. Aguilera A, Klein HL. 1990. HPR1, a novel yeast gene that prevents intrachromosomal excision recombination, shows carboxy-terminal homology to the Saccharomyces cerevisiae TOP1 gene. Mol Cell Biol 10: 1439-1451.
4. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H. 2008. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7: 1389-1396. (Pubitemid 352038280)
5. Andersen CB, Ballut L, Johansen JS, Chamieh H, Nielsen KH, Oliveira CL, Pedersen JS, Seraphin B, Le Hir H, Andersen GR. 2006. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313: 1968-1972. (Pubitemid 44498005)
6. Boeke JD, LaCroute F, Fink GR. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197: 345-346.
7. Cariani L, Thomas L, Brito J, del Castillo JR. 2004. Bismuth citrate in the quantification of inorganic phosphate and its utility in the determination of membrane-bound phosphatases. Anal Biochem 324: 79-83. (Pubitemid 37491126)
8. 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.
9. Cordin O, Banroques J, Tanner NK, Linder P. 2006. The DEAD-box protein family of RNA helicases. Gene 367: 17-37. (Pubitemid 43286737)
10. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: A sequence logo generator. Genome Res 14: 1188-1190. (Pubitemid 38811555)
11. Dufu K, Livingstone MJ, Seebacher J, Gygi SP, Wilson SA, Reed R. 2010. ATP is required for interactions between UAP56 and two conserved mRNA export proteins, Aly and CIP29, to assemble the TREX complex. Genes Dev 24: 2043-2053.
12. Fairman-Williams ME, Guenther UP, Jankowsky E. 2010. SF1 and SF2 helicases: Family matters. Curr Opin Struct Biol 20: 313-324.
13. Fan HY, Merker RJ, Klein HL. 2001. High-copy-number expression of Sub2p, a member of the RNA helicase superfamily, suppresses hpr1- mediated genomic instability. Mol Cell Biol 21: 5459-5470. (Pubitemid 32702450)
14. Folco EG, Lee CS, Dufu K, Yamazaki T, Reed R. 2012. The proteins PDIP3 and ZC11A associate with the human TREX complex in an ATP-dependent manner and function in mRNA export. PloS one 7: e43804.
15. Gomez-Gonzalez B, Garcia-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marin A, Foiani M, Aguilera A. 2011. Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J 30: 3106-3119.
16. Heckman KL, Pease LR. 2007. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932. (Pubitemid 46758810)
17. Henn A, Bradley MJ, De La Cruz EM. 2012. ATP utilization and RNA conformational rearrangement by DEAD-box proteins. Annu Rev Biophys 41: 247-267.
18. Huertas P, Aguilera A. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription- associated recombination. Mol Cell 12: 711-721. (Pubitemid 37222491)
19. Jensen TH, Boulay J, Rosbash M, Libri D. 2001a. The DECD box putative ATPase Sub2p is an early mRNA export factor. Curr Biol 11: 1711-1715. (Pubitemid 33037785)
20. Jensen TH, Patricio K, McCarthy T, Rosbash M. 2001b. 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. (Pubitemid 32436448)
21. Jensen MM, Christensen MS, Bonven B, Jensen TH. 2008. Requirements for chromatin reassembly during transcriptional downregulation of a heat shock gene in Saccharomyces cerevisiae. FEBS J 275: 2956-2964. (Pubitemid 351678682)
22. 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. (Pubitemid 34760582)
23. Jimeno-Gonzalez S, Haaning LL, Malagon F, Jensen TH. 2010. The yeast 5′-3′ exonuclease Rat1p functions during transcription elongation by RNA polymerase II. Mol Cell 37: 580-587.
24. Johnson SA, Cubberley G, Bentley DL. 2009. Cotranscriptional recruitment of the mRNA export factor Yra1 by direct interaction with the 3′ end processing factor Pcf11. Mol Cell 33: 215-226.
25. Kistler AL, Guthrie C. 2001. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase. Genes Dev 15: 42-49. (Pubitemid 32060681)
26. Libri D, Graziani N, Saguez C, Boulay J. 2001. Multiple roles for the yeast SUB2/yUAP56 gene in splicing. Genes Dev 15: 36-41. (Pubitemid 32060680)
27. Mohr G, Del Campo M, Mohr S, Yang Q, Jia H, Jankowsky E, Lambowitz AM. 2008. Function of the C-terminal domain of the DEAD-box protein Mss116p analyzed in vivo and in vitro. J Mol Biol 375: 1344-1364.
28. Pagni M, Ioannidis V, Cerutti L, Zahn-Zabal M, Jongeneel CV, Falquet L. 2004. MyHits: A new interactive resource for protein annotation and domain identification. Nucleic Acids Res 32: W332-W335. (Pubitemid 38997353)
29. Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N. 1994. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J 13: 1205-1215. (Pubitemid 24074727)
30. Peña A, Gewartowski K, Mroczek S, Cuéllar J, Szykowska A, Prokop A, Czarnocki-Cieciura M, Piwowarski J, Tous C, Aguilera A, et al. 2012. Architecture and nucleic acids recognition mechanism of the THO complex, an mRNP assembly factor. EMBO J 31: 1605-1616.
31. Piruat JI, Aguilera A. 1998. A novel yeast gene, THO2, is involved in RNA pol II transcription and provides new evidence for transcriptional elongation-associated recombination. EMBO J 17: 4859-4872. (Pubitemid 28377186)
32. Prado F, Aguilera A. 1995. Role of reciprocal exchange, one-ended invasion crossover and single-strand annealing on inverted and direct repeat recombination in yeast: Different requirements for the RAD1, RAD10, and RAD52 genes. Genetics 139: 109-123.
33. Rougemaille M, Gudipati RK, Olesen JR, Thomsen R, Seraphin B, Libri D, Jensen TH. 2007. Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J 26: 2317-2326. (Pubitemid 46685852)
34. 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. (Pubitemid 351905924)
35. Schmid M, Rougemaille M, Libri D, Jensen TH. 2008. Chapter 10. Estimating nuclear mRNA decay in Saccharomyces cerevisiae. Methods Enzymol 449: 205-219.
36. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S. 2006. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125: 287-300.
37. Shen J, Zhang L, Zhao R. 2007. Biochemical characterization of the ATPase and helicase activity of UAP56, an essential pre-mRNA splicing and mRNA export factor. J Biol Chem 282: 22544-22550. (Pubitemid 47267313)
38. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
39. Strasser K, Hurt E. 2001. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature 413: 648-652. (Pubitemid 32964066)
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. (Pubitemid 34534714)
41. Sun X, Perlick HA, Dietz HC, Maquat LE. 1998. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc Natl Acad Sci 95: 10009-10014. (Pubitemid 28415285)
42. Taniguchi I, Ohno M. 2008. ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol Cell Biol 28: 601-608.
43. Thomsen R, Libri D, Boulay J, Rosbash M, Jensen TH. 2003. Localization of nuclear retained mRNAs in Saccharomyces cerevisiae. RNA 9: 1049-1057. (Pubitemid 37093615)
44. Tutucci E, Stutz F. 2011. Keeping mRNPs in check during assembly and nuclear export. Nat Rev Mol Cell Biol 12: 377-384.
45. Yang Q, Jankowsky E. 2005. ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 44: 13591-13601. (Pubitemid 41443687)
46. 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. (Pubitemid 35304057)
47. Zhao R, Shen J, Green MR, MacMorris M, Blumenthal T. 2004. Crystal structure of UAP56, a DExD/H-box protein involved in pre-mRNA splicing and mRNA export. Structure 8: 1373-1381. (Pubitemid 39092082)