The Yeast La Related Protein Slf1p Is a Key Activator of Translation during the Oxidative Stress Response

PLoS Genetics

Volumn 11, Issue 1, 2015, Pages

  Kershaw, Christopher J ^a   Costello, Joseph L ^a,b   Castelli, Lydia M ^a   Talavera, David ^a   Rowe, William ^a   Sims, Paul F G ^a   Ashe, Mark P ^a   Hubbard, Simon J ^a   Pavitt, Graham D ^a   Grant, Chris M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HYDROGEN PEROXIDE; MESSENGER RNA; PROTEIN SLF1P; PROTEIN SRO9P; PROTEOME; RNA BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; SACCHAROMYCES CEREVISIAE PROTEIN; SLF1 PROTEIN, S CEREVISIAE;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; FUNGUS GROWTH; GENE EXPRESSION; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN MOTIF; RIBOSOME; RNA BINDING; RNA TRANSLATION; SEQUENCE ANALYSIS; STEADY STATE; WILD TYPE; BIOSYNTHESIS; GENETICS; METABOLISM; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, RNA;

EID: 84924366667     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004903     Document Type: Article

References (43)

1. Vogel C, Marcotte EM, (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews Genetics 13: 227–232.
2. Schwanhaeusser B, Busse D, Li N, Dittmar G, Schuchhardt J, et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337–342.
3. Simpson CE, Ashe MP, (2012) Adaptation to stress in yeast: to translate or not? Biochemical Society Transactions 40: 794–799.
4. Jackson RJ, Hellen CUT, Pestova TV, (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nature Reviews Molecular Cell Biology 11: 113–127.
5. Tsvetanova NG, Klass DM, Salzman J, Brown PO (2010) Proteome-Wide Search Reveals Unexpected RNA-Binding Proteins in Saccharomyces cerevisiae. Plos One 5.
6. Bousquet-Antonelli C, Deragon J-M, (2009) A comprehensive analysis of the La-motif protein superfamily. Rna-a Publication of the Rna Society 15: 750–764.
7. Bayfield MA, Yang R, Maraia RJ, (2010) Conserved and divergent features of the structure and function of La and La-related proteins (LARPs). Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms 1799: 365–378.
8. Yang R, Gaidamakov SA, Xie J, Lee J, Martino L, et al. (2011) La-Related Protein 4 Binds Poly(A), Interacts with the Poly(A)-Binding Protein MLLE Domain via a Variant PAM2w Motif, and Can Promote mRNA Stability. Molecular and Cellular Biology 31: 542–556.
9. Aoki K, Adachi S, Homoto M, Kusano H, Koike K, et al. (2013) LARP1 specifically recognizes the 3 ′ terminus of poly(A) mRNA. Febs Letters 587: 2173–2178.
10. Sobel SG, Wolin SL, (1999) Two yeast La motif-containing proteins are RNA-binding proteins that associate with polyribosomes. Molecular Biology of the Cell 10: 3849–3862.
11. Schaeffler K, Schulz K, Hirmer A, Wiesner J, Grimm M, et al. (2010) A stimulatory role for the La-related protein 4B in translation. Rna-a Publication of the Rna Society 16: 1488–1499.
12. Schenk L, Meinel DM, Straesser K, Gerber AP, (2012) La-motif-dependent mRNA association with Slf1 promotes copper detoxification in yeast. Rna-a Publication of the Rna Society 18: 449–461.
13. Chatenay-Lapointe M, Shadel GS (2011) Repression of Mitochondrial Translation, Respiration and a Metabolic Cycle-Regulated Gene, SLF1, by the Yeast Pumilio-Family Protein Puf3p. Plos One 6.
14. Keene JD, (2007) RNA regulons: coordination of post-transcriptional events. Nature Reviews Genetics 8: 533–543.
15. Shenton D, Smirnova JB, Selley JN, Carroll K, Hubbard SJ, et al. (2006) Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. Journal of Biological Chemistry 281: 29011–29021.
16. Subtelny AO, Eichhorn SW, Chen GR, Sive H, Bartel DP, (2014) Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508: 66–71.
17. Yu W, Farrell RA, Stillman DJ, Winge DR, (1996) Identification of SLF1 as a new copper homeostasis gene involved in copper sulfide mineralization in Saccharomyces cerevisiae. Molecular and Cellular Biology 16: 2464–2472.
18. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell 11: 4241–4257.
19. Mascarenhas C, Edwards-Ingram LC, Zeef L, Shenton D, Ashe MP, et al. (2008) Gcn4 is required for the response to peroxide stress in the yeast Saccharomyces cerevisiae. Molecular Biology of the Cell 19: 2995–3007.
20. Wells SE, Hillner PE, Vale RD, Sachs AB, (1998) Circularization of mRNA by eukaryotic translation initiation factors. Molecular Cell 2: 135–140.
21. Richardson R, Denis CL, Zhang C, Nielsen MEO, Chiang Y-C, et al. (2012) Mass spectrometric identification of proteins that interact through specific domains of the poly(A) binding protein. Molecular Genetics and Genomics 287: 711–730.
22. David A, Netzer N, Strader MB, Das SR, Chen CY, et al. (2011) RNA Binding Targets Aminoacyl-tRNA Synthetases to Translating Ribosomes. Journal of Biological Chemistry 286: 20688–20700.
23. Lui J, Castelli LM, Pizzinga M, Simpson CE, Hoyle NP, et al. (2014) Granules harboring translationally active mRNAs provide a platform for P-body formation following stress (In Press). Cell Reports.
24. Dong G, Chakshusmathi G, Wolin SL, Reinisch KM, (2004) Structure of the La motif: a winged helix domain mediates RNA binding via a conserved aromatic patch. Embo Journal 23: 1000–1007.
25. Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, et al. (2012) PaxDb, a Database of Protein Abundance Averages Across All Three Domains of Life. Molecular & Cellular Proteomics 11: 492–500.
26. Cridge AG, Castelli LM, Smirnova JB, Selley JN, Rowe W, et al. (2010) Identifying eIF4E-binding protein translationally-controlled transcripts reveals links to mRNAs bound by specific PUF proteins. Nucleic Acids Research 38: 8039–8050.
27. Altmann M, Sonenberg N, Trachsel H, (1989) TRANSLATION IN SACCHAROMYCES-CEREVISIAE - INITIATION-FACTOR 4E-DEPENDENT CELL-FREE SYSTEM. Molecular and Cellular Biology 9: 4467–4472.
28. Armache J-P, Jarasch A, Anger AM, Villa E, Becker T, et al. (2010) Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-angstrom resolution. Proceedings of the National Academy of Sciences of the United States of America 107: 19748–19753.
29. Armache J-P, Jarasch A, Anger AM, Villa E, Becker T, et al. (2010) Localization of eukaryote-specific ribosomal proteins in a 5.5-angstrom cryo-EM map of the 80S eukaryotic ribosome. Proceedings of the National Academy of Sciences of the United States of America 107: 19754–19759.
30. Baum S, Bittins M, Frey S, Seedorf M, (2004) Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochemical Journal 380: 823–830.
31. Sezen B, Seedorf M, Schiebel E, (2009) The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes & Development 23: 1559–1570.
32. Gerashchenko MV, Lobanov AV, Gladyshev VN, (2012) Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 109: 17394–17399.
33. Tcherkezian J, Cargnello M, Romeo Y, Huttlin EL, Lavoie G, et al. (2014) Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5 ′ TOP mRNA translation. Genes & Development 28: 357–371.
34. Sengupta J, Agrawal RK, Frank J, (2001) Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proceedings of the National Academy of Sciences of the United States of America 98: 11991–11996.
35. Duttagupta R, Tian B, Wilusz CJ, Khounh DT, Soteropoulos P, et al. (2005) Global analysis of Pup1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Molecular and Cellular Biology 25: 5499–5513.
36. Hogan D, Riordan D, Gerber A, Herschlag D, Brown P, (2008) Diverse RNA-Binding Proteins Interact with Functionally Related Sets of RNAs, Suggesting an Extensive Regulatory System. Plos Biology 6: 2297–2313.
37. Kunkel TA, (1985) RAPID AND EFFICIENT SITE-SPECIFIC MUTAGENESIS WITHOUT PHENOTYPIC SELECTION. Proceedings of the National Academy of Sciences of the United States of America 82: 488–492.
38. Taylor EJ, Campbell SG, Griffiths CD, Reid PJ, Slaven JW, et al. (2010) Fusel Alcohols Regulate Translation Initiation by Inhibiting eIF2B to Reduce Ternary Complex in a Mechanism That May Involve Altering the Integrity and Dynamics of the eIF2B Body. Molecular Biology of the Cell 21: 2202–2216.
39. Trotter EW, Rand JD, Vickerstaff J, Grant CM, (2008) The yeast Tsa1 peroxiredoxin is a ribosome-associated antioxidant. Biochemical Journal 412: 73–80.
40. Rowe W, Kershaw CJ, Castelli LM, Costello JL, Ashe MP, et al. (2014) Puf3p induces translational repression of genes linked to oxidative stress. Nucleic Acids Research 42: 1026–1041.
41. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.
42. McCarthy DJ, Chen Y, Smyth GK, (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research 40: 4288–4297.
43. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37: W202–W208.