Interactions affected by arginine methylation in the yeast protein-protein interaction network

Molecular and Cellular Proteomics

Volumn 12, Issue 11, 2013, Pages 3184-3198

  Erce, Melissa A ^a   Abeygunawardena, Dhanushi ^b   Low, Jason K K ^a,c   Hart Smith, Gene ^a   Wilkins, Marc R ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AIR2 PROTEIN; ARGININE; DED1 PROTEIN; HMT1 METHYLTRANSFERASE; NPL3 PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN; SNP1 PROTEIN; UNCLASSIFIED DRUG; YRA1 PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SACCHAROMYCES CEREVISIAE; TANDEM MASS SPECTROMETRY; TWO HYBRID SYSTEM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ARGININE; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; DEAD-BOX RNA HELICASES; METHYLATION; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTEOME; PROTEOMICS; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TANDEM MASS SPECTROMETRY; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84887048938     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.031500     Document Type: Article

References (69)

1. de Lichtenberg, U., Jensen, L. J., Brunak, S., and Bork, P. (2005) Dynamic Complex Formation During the Yeast Cell Cycle. Science 307, 724-727. (Pubitemid 40194642)
2. Wu, X., Guo, J., Zhang, D. Y., and Lin, K. (2009) The properties of hub proteins in a yeast-aggregated cell cycle network and its phase subnetworks. Proteomics 9, 4812-4824.
3. Goel, A., and Wilkins, M. R. (2012) Dynamic Hubs Show Competitive and Static Hubs Non-Competitive Regulation of Their Interaction Partners. PLoS One 7, e48209.
4. Wilkins, M. R., and Kummerfeld, S. K. (2008) Sticking together? Falling apart? Exploring the dynamics of the interactome. Trends in Biochemical Sciences 33, 195-200.
5. Seet, B. T., Dikic, I., Zhou, M. M., and Pawson, T. (2006) Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 7, 473-483. (Pubitemid 44036453)
6. Yaffe, M. B. (2002) How do 14-3-3 proteins work? - Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57. (Pubitemid 34242978)
7. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45. (Pubitemid 30038513)
8. Low, J. K., and Wilkins, M. R. (2012) Protein arginine methylation in Saccharomyces cerevisiae. Febs J. 279, 4423-4443.
9. Erce, M. A., Pang, C. N., Hart-Smith, G., and Wilkins, M. R. (2012) The methylproteome and the intracellular methylation network. Proteomics 12, 564-586.
10. Bachand, F. (2007) Protein arginine methyltransferases: from unicellular eukaryotes to humans. Eukaryotic Cell 6, 889-898. (Pubitemid 46983289)
11. Côté, J., and Richard, S. (2005) Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280, 28476-28483. (Pubitemid 41105747)
12. Bedford, M. T., Frankel, A., Yaffe, M. B., Clarke, S., Leder, P., and Richard, S. (2000) Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains. J. Biol. Chem. 275, 16030-16036. (Pubitemid 30366909)
13. Yang, Y., and Bedford, M. T. (2013) Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50.
14. Erce, M. A., Low, J. K., Hart-Smith, G., and Wilkins, M. R. (2013) A conditional two-hybrid (C2H) system for the detection of protein-protein interactions that are mediated by post-translational modification. Proteomics 13, 1059-1064.
15. McBride, A. E., Cook, J. T., Stemmler, E. A., Rutledge, K. L., McGrath, K. A., and Rubens, J. A. (2005) Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions. Journal of Biological Chemistry 280, 30888-30898. (Pubitemid 41291820)
16. Chen, Y. C., Milliman, E. J., Goulet, I., Côté, J., Jackson, C. A., Vollbracht, J. A., and Yu, M. C. (2010) Protein arginine methylation facilitates cotranscriptional recruitment of pre-mRNA splicing factors. Mol. Cell. Biol. 30, 5245-5256.
17. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95, 5752-5756. (Pubitemid 28224168)
18. Battesti, A., and Bouveret, E. (2012) The bacterial two-hybrid system based on adenylate cyclase reconstitution in Escherichia coli. Methods 58, 325-334.
19. Erce, M. A., Low, J. K. K., March, P. E., Wilkins, M. R., and Takayama, K. M. (2009) Identification and functional analysis of RNase E of Vibrio angustum S14 and two-hybrid analysis of its interaction partners. Biochim. Biophys. Acta 1794, 1107-1114.
20. Hart-Smith, G., Low, J. K., Erce, M. A., and Wilkins, M. R. (2012) Enhanced methylarginine characterization by post-translational modification-specific targeted data acquisition and electron-transfer dissociation mass spectrometry. J. Am. Soc. Mass Spectrom. 23, 1376-1389.
21. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass Spectrometric Sequencing of Proteins from Silver-Stained Polyacrylamide Gels. Anal. Chem. 68, 850-858.
22. Hart-Smith, G., and Raftery, M. J. (2012) Detection and characterization of low abundance glycopeptides via higher-energy c-trap dissociation and orbitrap mass analysis. J. Am. Soc. Mass Spectrom. 23, 124-140.
23. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567. (Pubitemid 30007252)
24. Snijders, A. P., Hung, M. L., Wilson, S. A., and Dickman, M. J. (2010) Analysis of arginine and lysine methylation utilizing peptide separations at neutral pH and electron transfer dissociation mass spectrometry. J. Am. Soc. Mass Spectrom. 21, 88-96.
25. Acharya, A., Xu, X. J., Husain-Ponnampalam, R. D., Hoffmann-Benning, S., and Kuo, M. H. (2005) Production of constitutively acetylated recombinant p53 from yeast and Escherichia coli by tethered catalysis. Protein Expression Purification 41, 417-425. (Pubitemid 40623229)
26. Sambrook, J., and Russell, D. W. (2001) Molecular cloning : A laboratory manual/Joseph Sambrook, David W. Russell Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Inoue, K., Mizuno, T., Wada, K., and Hagiwara, M. (2000) Novel RING Finger Proteins, Air1p and Air2p, Interact with Hmt1p and Inhibit the Arginine Methylation of Npl3p. J. Biol. Chem. 275, 32793-32799.
28. Tardiff, D. F., Abruzzi, K. C., and Rosbash, M. (2007) Protein characterization of Saccharomyces cerevisiae RNA polymerase II after in vivo crosslinking. Proc. Natl. Acad. Sci. U. S. A. 104, 19948-19953.
29. Hurt, E., Luo, M. J., Röther, S., Reed, R., and Strässer, K. (2004) Cotranscriptional recruitment of the serine-arginine-rich (SR)-like proteins Gbp2 and Hrb1 to nascent mRNA via the TREX complex. Proc. Natl. Acad. Sci. U. S. A. 101, 1858-1862. (Pubitemid 38228981)
30. Yu, M. C., Bachand, F., McBride, A. E., Komili, S., Casolari, J. M., and Silver, P. A. (2004) Arginine methyltransferase affects interactions and recruitment of mRNA processing and export factors. Genes Dev. 18, 2024-2035. (Pubitemid 39071583)
31. Linder, P., and Jankowsky, E. (2011) From unwinding to clamping - The DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 12, 505-516.
32. Windgassen, M., and Krebber, H. (2003) Identification of Gbp2 as a novel poly(A)- RNA-binding protein involved in the cytoplasmic delivery of messenger RNAs in yeast. EMBO Rep. 4, 278-283. (Pubitemid 36511724)
33. Kuhn, P., Xu, Q., Cline, E., Zhang, D., Ge, Y., and Xu, W. (2009) Delineating Anopheles gambiae coactivator associated arginine methyltransferase 1 automethylation using top-down high resolution tandem mass spectrometry. Protein Sci. 18, 1272-1280.
34. McBride, A. E., Weiss, V. H., Kim, H. K., Hogle, J. M., and Silver, P. A. (2000) Analysis of the yeast arginine methyltransferase Hmt1p/Rmt1p and its in vivo function. J. Biol. Chem. 275, 3128-3136.
35. Griffith, K. L., and Wolf Jr., R. E. (2002) Measuring β-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem. Biophys. Res. Commun. 290, 397-402. (Pubitemid 34694512)
36. Battesti, A., and Bouveret, E. (2008) Improvement of bacterial two-hybrid vectors for detection of fusion proteins and transfer to pBAD-tandem affinity purification, calmodulin binding peptide, or 6-histidine tag vectors. Proteomics 8, 4768-4771.
37. Ito, T., Tashiro, K., Muta, S., Ozawa, R., Chiba, T., Nishizawa, M., Yamamoto, K., Kuhara, S., and Sakaki, Y. (2000) Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc. Natl. Acad. Sci. U. S. A. 97, 1143-1147. (Pubitemid 30080826)
38. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. D., Moore, L., Adams, S. L., Millar, A., Taylor, P., Bennett, K., Boutilier, K., Yang, L., Wolting, C., Donaldson, I., Schandorff, S., Shewnarane, J., Vo, M., Taggart, J., Goudreault, M., Muskat, B., Alfarano, C., Dewar, D., Lin, Z., Michalickova, K., Willems, A. R., Sassi, H., Nielsen, P. A., Rasmussen, K. J., Andersen, J. R., Johansen, L. E., Hansen, L. H., Jespersen, H., Podtelejnikov, A., Nielsen, E., Crawford, J., Poulsen, V., Sorensen, B. D., Matthiesen, J., Hendrickson, R. C., Gleeson, F., Pawson, T., Moran, M. F., Durocher, D., Mann, M., Hogue, C. W. V., Figeys, D., and Tyers, M. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183. (Pubitemid 34059520)
39. Gavin, A. C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A.-M., Cruciat, C. M., Remor, M., Hofert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G., and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147. (Pubitemid 34059510)
40. Gavin, A. C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L. J., Bastuck, S., Dumpelfeld, B., Edelmann, A., Heurtier, M. A., Hoffman, V., Hoefert, C., Klein, K., Hudak, M., Michon, A. M., Schelder, M., Schirle, M., Remor, M., Rudi, T., Hooper, S., Bauer, A., Bouwmeester, T., Casari, G., Drewes, G., Neubauer, G., Rick, J. M., Kuster, B., Bork, P., Russell, R. B., and Superti-Furga, G. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636.
41. Yu, H., Braun, P., Yildirum, M. A., Lemmens, I., Venkatesan, K., Sahalie, J., Hirozane-Kishikawa, T., Gebreab, F., Li, N., Simonis, N., Hao, T., Rual, J. F., Dricot, A., Vazquez, A., Murray, R. R., Simon, C., Tardivo, L., Tam, S., Svrzikapa, N., Fan, C., de Smet, A. S., Motyl, A., Hudson, M. E., Park, J., Xin, X., Cusick, M. E., Moore, T., Boone, C., Snyder, M., Roth, F. P., Barabási, A. L., Tavernier, J., Hill, D. E., and Vidal, M. (2008) High-quality binary protein interaction map of the Yeast interactome network. Science 322, 104-110.
42. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrín-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G., St Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
43. Kwak, Y. T., Guo, J., Prajapati, S., Park, K. J., Surabhi, R. M., Miller, B., Gehrig, P., and Gaynor, R. B. (2003) Methylation of SPT5 Regulates Its Interaction with RNA Polymerase II and Transcriptional Elongation Properties. Mol. Cell 11, 1055-1066. (Pubitemid 36566326)
44. Fronz, K., Güttinger, S., Burkert, K., Kühn, U., Stöhr, N., Schierhorn, A., and Wahle, E. (2011) Arginine methylation of the nuclear poly(A) binding protein weakens the interaction with its nuclear import receptor, transportin. J. Biol. Chem. 286, 32986-32994.
45. Ostareck-Lederer, A., Ostareck, D. H., Rucknagel, K. P., Schierhorn, A., Moritz, B., Huttelmaier, S., Flach, N., Handoko, L., and Wahle, E. (2006) Asymmetric arginine dimethylation of heterogeneous nuclear ribonucleoprotein K by protein-arginine methyltransferase 1 inhibits its interaction with c-Src. J. Biol. Chem. 281, 11115-11125. (Pubitemid 43855536)
46. Bucheli, M. E., and Buratowski, S. (2005) Npl3 is an antagonist of mRNA 3' end formation by RNA polymerase II. EMBO J. 24, 2150-2160. (Pubitemid 40961799)
47. Bucheli, M. E., He, X., Kaplan, C. D., Moore, C. L., and Buratowski, S. (2007) Polyadenylation site choice in yeast is affected by competition between Npl3 and polyadenylation factor CFI. RNA 13, 1756-1764. (Pubitemid 47481683)
48. Dermody, J. L., Dreyfuss, J. M., Villén, J., Ogundipe, B., Gygi, S. P., Park, P. J., Ponticelli, A. S., Moore, C. L., Buratowski, S., and Bucheli, M. E. (2008) Unphosphorylated SR-Like protein Npl3 stimulates RNA Polymerase II elongation. PLoS ONE 3, e3273.
49. Kress, T. L., Krogan, N. J., and Guthrie, C. (2008) A Single SR-like Protein, Npl3, Promotes Pre-mRNA Splicing in Budding Yeast. Mol. Cell 32, 727-734.
50. Lee, M. S., Henry, M., and Silver, P. A. (1996) A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev. 10, 1233-1246. (Pubitemid 26171104)
51. Windgassen, M., Sturm, D., Cajigas, I. J., Gonzalez, C. I., Seedorf, M., Bastians, H., and Krebber, H. (2004) Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell. Biol. 24, 10479-10491. (Pubitemid 39507884)
52. Lukasiewicz, R., Nolen, B., Adams, J. A., and Ghosh, G. (2007) The RGG Domain of Npl3p Recruits Sky1p Through Docking Interactions. J. Mol. Biol. 367, 249-261. (Pubitemid 46274707)
53. Iost, I., Dreyfus, M., and Linder, P. (1999) Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J. Biol. Chem. 274, 17677-17683.
54. Xu, C., Henry, P. A., Setya, A., and Henry, M. F. (2003) In vivo analysis of nucleolar proteins modified by the yeast arginine methyltransferase Hmt1/Rmt1p. RNA 9, 746-759. (Pubitemid 36618202)
55. Gottschalk, A., Tang, J., Puig, O., Salgado, J., Neubauer, G., Colot, H. V., Mann, M., Seraphin, B., Rosbash, M., Luhrmann, R., and Fabrizio, P. (1998) A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA 4, 374-393. (Pubitemid 28160780)
56. Oeffinger, M., Wei, K. E., Rogers, R., DeGrasse, J. A., Chait, B. T., Aitchison, J. D., and Rout, M. P. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Meth. 4, 951-956. (Pubitemid 350042385)
57. Skrisovska, L., and Allain, F. H. T. (2008) Improved Segmental Isotope Labeling Methods for the NMR Study of Multidomain or Large Proteins: Application to the RRMs of Npl3p and hnRNP L. J. Mol. Biol. 375, 151-164. (Pubitemid 350160684)
58. Deka, P., Bucheli, M. E., Moore, C., Buratowski, S., and Varani, G. (2008) Structure of the yeast SR protein Npl3 and interaction with mRNA 3'-end processing signals. J. Mol. Biol. 375, 136-150. (Pubitemid 350160683)
59. Holub, P., Lalakova, J., Cerna, H., Pasulka, J., Sarazova, M., Hrazdilova, K., Arce, M. S., Hobor, F., Stefl, R., and Vanacova, S. (2012) Air2p is critical for the assembly and RNA-binding of the TRAMP complex and the KOW domain of Mtr4p is crucial for exosome activation. Nucleic Acids Res. 40, 5679-5693.
60. Hamill, S., Wolin, S. L., and Reinisch, K. M. (2010) Structure and function of the polymerase core of TRAMP, a RNA surveillance complex. Proc. Natl. Acad. Sci. U. S. A. 107, 15045-15050.
61. Kölbel, K., Ihling, C., Kühn, U., Neundorf, I., Otto, S., Stichel, J., Robaa, D., Beck-Sickinger, A. G., Sinz, A., and Wahle, E. (2012) Peptide backbone conformation affects the substrate preference of protein arginine methyltransferase I. Biochemistry 51, 5463-5475.
62. Singh, G. P., Ganapathi, M., and Dash, D. (2007) Role of intrinsic disorder in transient interactions of hub proteins. Proteins: Structure, Function, and Bioinformatics 66, 761-765.
63. Kzhyshkowska, J., Schü tt, H., Liss, M., Kremmer, E., Stauber, R., Wolf, H., and Dobner, T. (2001) Heterogeneous nuclear ribonucleoprotein E1BAP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1. Biochem. J. 358, 305-314. (Pubitemid 32826346)
64. Rajyaguru, P., and Parker, R. (2012) RGG motif proteins: Modulators of mRNA functional states. Cell Cycle 11, 2594-2599.
65. Thandapani, P., O'Connor, T. R., Bailey, T. L., and Richard, S. (2013) Defining the RGG/RG Motif. Mol. Cell 50, 613-623.
66. Gehrig, P. M., and Hunziker, P. E. (2004) Fragmentation pathways of NG-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS. J. Am. Soc. Mass Spectrom. 15, 142-149. (Pubitemid 38183202)
67. Romero, P., Obradovic, Z., and Dunker, K. (1997) Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Informatics 8, 110-124.
68. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., and Dunker, A. K. (2001) Sequence complexity of disordered protein. Proteins: Structure, Function, and Bioinformatics 42, 38-48.
69. Li, X., Romero, P., Rani, M., Dunker, A. K., and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Inform Ser Workshop Genome Inform 10, 30-40.