Quantitative proteomic analysis reveals concurrent RNA-protein interactions and identifies new RNA-binding proteins in Saccharomyces cerevisiae

Genome Research

Volumn 23, Issue 6, 2013, Pages 1028-1038

  Klass, Daniel M ^a   Scheibe, Marion ^b   Butter, Falk ^b   Hogan, Gregory J ^a   Mann, Matthias ^b   Brown, Patrick O ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN NAB2; PROTEIN PAB1; PROTEIN PUF3; RIBONUCLEASE; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DNA BINDING MOTIF; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; PROTEOMICS; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE;

CLUSTER ANALYSIS; MODELS, BIOLOGICAL; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTEIN BINDING; PROTEOMICS; REPRODUCIBILITY OF RESULTS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS;

SACCHAROMYCES CEREVISIAE;

EID: 84878708955     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.153031.112     Document Type: Article

References (68)

1. Balagopal V, Parker R. 2011. Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. RNA 17: 835-842.
2. Baltz AG, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K,Milek M, et al. 2012. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 46: 674-690.
3. Bertrand E, Fromont-Racine M, Pictet R, Grange T. 1993. Visualization of the interaction of a regulatory protein with RNA in vivo. Proc Natl Acad Sci 90: 3496-3500. (Pubitemid 23111393)
4. Bohnsack MT, Martin R, Granneman S, Ruprecht M, Schleiff E, Tollervey D. 2009. Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol Cell 36: 583-592.
5. Bregman A, Avraham-Kelbert M, Barkai O, Duek L, Guterman A, Choder M. 2011. Promoter elements regulate cytoplasmic mRNA decay. Cell 147: 1473-1483.
6. Brune C, Munchel SE, Fischer N, Podtelejnikov AV, Weis K. 2005. Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA 11: 517-531. (Pubitemid 40397185)
7. Butter F, Scheibe M, Morl M, Mann M. 2009. Unbiased RNA-protein interaction screen by quantitative proteomics. Proc Natl Acad Sci 106: 10626-10631.
8. Casey JL, HentzeMW, KoellerDM, Caughman SW, Rouault TA, Klausner RD, Harford JB. 1988. Iron-responsive elements: Regulatory RNA sequences that control mRNA levels and translation. Science 240: 924-928.
9. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM, et al. 2012. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149: 1393-1406.
10. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, Chan ET, Christie KR, Costanzo MC, Dwight SS, Engel SR, et al. 2012. Saccharomyces Genome Database: The genomics resource of budding yeast. Nucleic Acids Res 40: D700-D705.
11. Choder M. 2011. mRNA imprinting: Additional level in the regulation of gene expression. Cell Logist 1: 37-40.
12. Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, Holstege FC, Weissman JS, Krogan NJ. 2007. Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics 6: 439-450. (Pubitemid 46554539)
13. Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372.
14. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR. 1997. Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci 94: 11456-11460. (Pubitemid 27451020)
15. de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, Walther TC, Mann M. 2008. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254.
16. Dunn EF, Hammell CM, Hodge CA, Cole CN. 2005. Yeast poly(A)-binding protein, Pab1, and PAN, a poly(A) nuclease complex recruited by Pab1, connect mRNA biogenesis to export. Genes Dev 19: 90-103. (Pubitemid 40095819)
17. Falcon S, Gentleman R. 2007. Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258. (Pubitemid 46189622)
18. Fasken MB, Stewart M, Corbett AH. 2008. Functional significance of the interaction between the mRNA-binding protein, Nab2, and the nuclear pore-associated protein, Mlp1, in mRNA export. J Biol Chem 283: 27130-27143.
19. Fontana A, de Laureto PP, Spolaore B, Frare E. 2012. Identifying disordered regions in proteins by limited proteolysis. Methods Mol Biol 896: 297-318.
20. Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
21. Gebauer F, Hentze MW. 2004. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835. (Pubitemid 39336276)
22. Gerber AP, Herschlag D, Brown PO. 2004. Extensive association of functionally and cytotopically related mRNAs with Puf family RNAbinding proteins in yeast. PLoS Biol 2: e79.
23. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK,Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425: 737-741. (Pubitemid 37314318)
24. Granneman S, Kudla G, Petfalski E, Tollervey D. 2009. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and highthroughput analysis of cDNAs. Proc Natl Acad Sci 106: 9613-9618.
25. Granneman S, Petfalski E, Swiatkowska A, Tollervey D. 2010. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J 29: 2026-2036.
26. Green DM, Marfatia KA, Crafton EB, Zhang X, Cheng X, Corbett AH. 2002. Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by argininemethylation via Hmt1p. J Biol Chem 277: 7752-7760. (Pubitemid 34968221)
27. Greenberg Jr. 1979. Ultraviolet light-induced crosslinking of mRNA to proteins. Nucleic Acids Res 6: 715-732.
28. Greenberg Jr. 1980. Proteins crosslinked to messenger RNA by irradiating polyribosomes with ultraviolet light. Nucleic Acids Res 8: 5685-5701.
29. Guisbert K, Duncan K, Li H, Guthrie C. 2005. Functional specificity of shuttling hnRNPs revealed by genome-wide analysis of their RNA binding profiles. RNA 11: 383-393. (Pubitemid 40397172)
30. Harel-Sharvit L, Eldad N, Haimovich G, Barkai O, Duek L, Choder M. 2010. RNA polymerase II subunits link transcription and mRNA decay to translation. Cell 143: 552-563.
31. Hector RE, Nykamp KR, Dheur S, Anderson JT, Non PJ, Urbinati CR,Wilson SM,Minvielle-Sebastia L, SwansonMS. 2002. Dual requirement for yeast hnRNP Nab2p in mRNA poly(A) tail length control and nuclear export. EMBO J 21: 1800-1810. (Pubitemid 34614636)
32. Hentze MW, Caughman SW, Rouault TA, Barriocanal JG,Dancis A, Harford JB, Klausner RD. 1987a. Identification of the iron-responsive element for the translational regulation of human ferritinmRNA. Science 238: 1570-1573. (Pubitemid 18032473)
33. Hentze MW, Rouault TA, Caughman SW, Dancis A, Harford JB, Klausner RD. 1987b. A cis-acting element is necessary and sufficient for translational regulation of human ferritin expression in response to iron. Proc Natl Acad Sci 84: 6730-6734.
34. Hieronymus H, Silver PA. 2003. Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat Genet 33: 155-161. (Pubitemid 36177066)
35. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO. 2008. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6: e255.
36. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, Hyman A, Mann M. 2010. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189: 739-754.
37. Iglesias N, Stutz F. 2008. Regulation of mRNP dynamics along the export pathway. FEBS Lett 582: 1987-1996.
38. Jansen JM, Wanless AG, Seidel CW, Weiss EL. 2009. Cbk1 regulation of the RNA-binding protein Ssd1 integrates cell fate with translational control. Curr Biol 19: 2114-2120.
39. Keene JD. 2007a. Biological clocks and the coordination theory of RNA operons and regulons. Cold Spring Harb Symp Quant Biol 72: 157-165.
40. Keene JD. 2007b. RNA regulons: Coordination of post-transcriptional events. Nat Rev Genet 8: 533-543. (Pubitemid 46955210)
41. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
42. Kurischko C, Kim HK, Kuravi VK, Pratzka J, Luca FC. 2011. The yeast Cbk1 kinase regulates mRNA localization via the mRNA-binding protein Ssd1. J Cell Biol 192: 583-598.
43. Lee DC, Aitchison JD. 1999. Kap104p-mediated nuclear import: Nuclear localization signals in mRNA-binding proteins and the role of Ran and RNA. J Biol Chem 274: 29031-29037.
44. Lee D, Ohn T, Chiang YC, Quigley G, Yao G, Liu Y, Denis CL. 2010. PUF3 acceleration of deadenylation in vivo can operate independently of CCR4 activity, possibly involving effects on the PAB1-mRNP structure. J Mol Biol 399: 562-575.
45. Leibold EA, Munro HN. 1988. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs. Proc Natl Acad Sci 85: 2171-2175. (Pubitemid 24315851)
46. Mann M. 2006. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 7: 952-958. (Pubitemid 44871421)
47. Marnef A, Standart N. 2010. Pat1 proteins: A life in translation, translation repression and mRNA decay. Biochem Soc Trans 38: 1602-1607.
48. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, Greenblatt J, Patterson SD, Wickens M, Bentley DL. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
49. Mittler G, Butter F, Mann M. 2009. A SILAC-based DNA-protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res 19: 284-293.
50. Ong SE, Mittler G, Mann M. 2004. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods 1: 119-126.
51. 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. (Pubitemid 46921005)
52. Pramanik SK, Bewley JD. 1996. Post-transcriptional regulation of protein synthesis during alfalfa embryogenesis: Proteins associated with the cytoplasmic polysomal and non-polysomal mRNAs (messenger ribonucleoprotein complex). J Exp Bot 45: 1871-1879.
53. Quenault T, Lithgow T, Traven A. 2011. PUF proteins: Repression, activation and mRNA localization. Trends Cell Biol 21: 104-112.
54. Rouault TA, HentzeMW, Haile DJ, Harford JB, Klausner RD. 1989. The ironresponsive element binding protein: A method for the affinity purification of a regulatory RNA-binding protein. Proc Natl Acad Sci 86: 5768-5772. (Pubitemid 19217535)
55. Saint-Georges Y, Garcia M, Delaveau T, Jourdren L, Le Crom S, Lemoine S, Tanty V, Devaux F, Jacq C. 2008. Yeast mitochondrial biogenesis: A role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS ONE 3: e2293.
56. Scheibe M, Butter F, Hafner M, Tuschl T, Mann M. 2012. Quantitative mass spectrometry and PAR-CLIP to identify RNA-protein interactions. Nucleic Acids Res 40: 9897-9902.
57. Schenk L, Meinel DM, Strasser K, Gerber AP. 2012. La-motif-dependent mRNA association with Slf1 promotes copper detoxification in yeast. RNA 18: 449-461.
58. Scherrer T, Mittal N, Janga SC, Gerber AP. 2010. A screen for RNA-binding proteins in yeast indicates dual functions for many enzymes. PLoS ONE 5: e15499.
59. Scherrer T, Femmer C, Schiess R, Aebersold R, Gerber AP. 2011. Defining potentially conserved RNA regulons of homologous zinc-finger RNAbinding proteins. Genome Biol 12: R3.
60. Schulze WX, Mann M. 2004. A novel proteomic screen for peptide-protein interactions. J Biol Chem 279: 10756-10764. (Pubitemid 38372689)
61. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. 2011. Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27: 431-432.
62. Tran EJ, Zhou Y, Corbett AH,Wente SR. 2007. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol Cell 28: 850-859. (Pubitemid 350217049)
63. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM, Vandermoere F, Morrice NA, Swift S, Rothbauer U, Leonhardt H, et al. 2008. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol 183: 223-239.
64. Tsvetanova NG, Klass DM, Salzman J, Brown PO. 2010. Proteome-wide search reveals unexpected RNA-binding proteins in Saccharomyces cerevisiae. PLoS ONE 5: e12671.
65. Tutucci E, Stutz F. 2011. Keeping mRNPs in check during assembly and nuclear export. Nat Rev Mol Cell Biol 12: 377-384.
66. Ule J, Jensen K, Mele A, Darnell RB. 2005. CLIP: A method for identifying protein-RNA interaction sites in living cells. Methods 37: 376-386. (Pubitemid 41682508)
67. Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, Brown PO. 2002. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci 99: 5860-5865. (Pubitemid 34493230)
68. Wolf JJ, Dowell RD, Mahony S, Rabani M, Gifford DK, Fink GR. 2010. Feedforward regulation of a cell fate determinant by an RNA-binding protein generates asymmetry in yeast. Genetics 185: 513-522.