Two steps forward-one step back: Advances in affinity purification mass spectrometry of macromolecular complexes

Proteomics

Volumn 12, Issue 10, 2012, Pages 1591-1608

  Oeffinger, Marlene ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Affinity purification; Cell lysis; Quantitative mass spectrometry; Ribonucleoprotein complexes (RNPs); Systems biology

Indexed keywords

EPITOPE; RNA;

AFFINITY PURIFICATION COUPLED TO MASS SPECTROMETRY; ANALYTIC METHOD; BACTERIAL CELL; CELL FUNCTION; CYTOLYSIS; HIGH THROUGHPUT SCREENING; MACROMOLECULE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW;

AFFINITY LABELS; CHROMATOGRAPHY, AFFINITY; MASS SPECTROMETRY; PROTEIN INTERACTION MAPPING; PROTEINS; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; SYSTEMS BIOLOGY;

EID: 84862638898     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100509     Document Type: Review

References (136)

1. Gavin, A. C., Bosche, M., Krause, R., Grandi, P. et al., Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415, 141-147.
2. Kuhner, S., van Noort, V., Betts, M. J., Leo-Macias, A. et al., Proteome organization in a genome-reduced bacterium. Science 2009, 326, 1235-1240.
3. Goh, K. I., Cusick, M. E., Valle, D., Childs, B. et al., The human disease network. Proc. Natl. Acad. Sci. USA 2007, 104, 8685-8690.
4. Taylor, I. W., Linding, R., Warde-Farley, D., Liu, Y. et al., Dynamic modularity in protein interaction networks predicts breast cancer outcome. Nat. Biotechnol. 2009, 27, 199-204.
5. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W. et al., Life with 6000 genes. Science 1996, 274, 546, 563-547.
6. Costanzo, M. C., Hogan, J. D., Cusick, M. E., Davis, B. P. et al., The yeast proteome database (YPD) and Caenorhabditis elegans proteome database (WormPD): comprehensive resources for the organization and comparison of model organism protein information. Nucleic Acids Res. 2000, 28, 73-76.
7. Grigoriev, A., On the number of protein-protein interactions in the yeast proteome. Nucleic Acids Res. 2003, 31, 4157-4161.
8. Albert, I., Albert, R., Conserved network motifs allow protein-protein interaction prediction. Bioinformatics 2004, 20, 3346-3352.
9. Johnson, M. E., Hummer, G., Nonspecific binding limits the number of proteins in a cell and shapes their interaction networks. Proc. Natl. Acad. Sci. USA 2011, 108, 603-608.
10. Gavin, A., Aloy, P., Grandi, P., Krause, R. et al., Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440, 631-636.
11. Krogan, N., Cagney, G., Yu, H., Zhong, G. et al., Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440, 637-643.
12. Collins, S. R., Kemmeren, P., Zhao, X.-C., Greenblatt, J. F. et al., Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol. Cell. Proteomics 2007, 6, 439-450.
13. Hunter, N., Borts, R. H., Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 1997, 11, 1573-1582.
14. Plowman, G. D., Sudarsanam, S., Bingham, J., Whyte, D. et al., The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. Proc. Natl. Acad. Sci. USA 1999, 96, 13603-13610.
15. Liao, Y., Kariya, K., Hu, C. D., Shibatohge, M. et al., RA-GEF, a novel Rap1A guanine nucleotide exchange factor containing a Ras/Rap1A-associating domain, is conserved between nematode and humans. J. Biol. Chem. 1999, 274, 37815-37820.
16. Ranganathan, R., Ross, E. M., PDZ domain proteins: scaffolds for signaling complexes. Curr. Biol. 1997, 7, R770-R773.
17. Picotti, P., Bodenmiller, B., Mueller, L. N., Domon, B. et al., Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138, 795-806.
18. Trinkle-Mulcahy, L., Boulon, S., Lam, Y. W., Urcia, R. et al., Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J. Cell Biol. 2008, 183, 223-239.
19. Cristea, I., Williams, R., Chait, B., Rout, M., Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 2005, 4, 1933-1941.
20. Oeffinger, M., Wei, K. E., Rogers, R., Degrasse, J. A. et al., Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 2007, 4, 951-956.
21. Abmayr, S. M. A. W., J. L., Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr. Protoc. Pharmacol. 2001, 12.3.1-12.3.13.
22. Schultz, M. C., Hockman, D. J., Harkness, T. A., Garinther, W. I. et al., Chromatin assembly in a yeast whole-cell extract. Proc. Natl. Acad. Sci. USA 1997, 94, 9034-9039.
23. Breitkreutz, A., Choi, H., Sharom, J. R., Boucher, L. et al., A global protein kinase and phosphatase interaction network in yeast. Science 2010, 328, 1043-1046.
24. Dilworth, D. J., Saleem, R. A., Rogers, R. S., Mirzaei, H. et al., QTIPS: a novel method of unsupervised determination of isotopic amino acid distribution in SILAC experiments. J. Am. Soc. Mass. Spectrom. 2010, 21, 1417-1422.
25. Schlosshauer, M., Baker, D., Realistic protein-protein association rates from a simple diffusional model neglecting long-range interactions, free energy barriers, and landscape ruggedness. Protein Sci. 2004, 13, 1660-1669.
26. Morokuma, K., Why do molecules interact? The origin of electron donor-acceptor complexes, hydrogen bonding and proton affinity. Acc. Chem. Res. 1977, 10, 294-300.
27. Roth, C. M., Neal, B. L., Lenhoff, A. M., Van der Waals interactions involving proteins. Biophys. J. 1996, 70, 977-987.
28. Kortemme, T., Morozov, A. V., Baker, D., An orientation-dependent hydrogen bonding potential improves prediction of specificity and structure for proteins and protein-protein complexes. J. Mol. Biol. 2003, 326, 1239-1259.
29. van Oss, C. J., Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. J. Mol. Recognit. 2003, 16, 177-190.
30. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M. et al., A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17, 1030-1032.
31. Archambault, V., Chang, E., Drapkin, B., Cross, F. et al., Targeted proteomic study of the cyclin-Cdk module. Mol. Cell 2004, 14, 699-711.
32. Alber, F., Dokudovskaya, S., Veenhoff, L. M., Zhang, W. et al., The molecular architecture of the nuclear pore complex. Nature 2007, 450, 695-701.
33. Lambert, J. P., Fillingham, J., Siahbazi, M., Greenblatt, J. et al., Defining the budding yeast chromatin-associated interactome. Mol. Syst. Biol. 2010, 6, 448-464.
34. Hubner, N. C., Bird, A. W., Cox, J., Splettstoesser, B. et al., Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 2010, 189, 739-754.
35. Barrios-Rodiles, M., Brown, K. R., Ozdamar, B., Bose, R. et al., High-throughput mapping of a dynamic signaling network in mammalian cells. Science 2005, 307, 1621-1625.
36. Schwenk, J., Harmel, N., Zolles, G., Bildl, W. et al., Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 2009, 323, 1313-1319.
37. Muller, C. S., Haupt, A., Bildl, W., Schindler, J. et al., Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc. Natl. Acad. Sci. USA 2010, 107, 14950-14957.
38. Rout, M., Aitchison, J., Suprapto, A., Hjertaas, K. et al., The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell. Biol. 2000, 148, 635-651.
39. Chang, I. F., Mass spectrometry-based proteomic analysis of the epitope-tag affinity purified protein complexes in eukaryotes. Proteomics 2006, 6, 6158-6166.
40. Cheeseman, I. M., Desai, A., A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci STKE. 2005, 266, pl1.
41. Trinkle-Mulcahy, L., Lamond, A. I., Toward a high-resolution view of nuclear dynamics. Science 2007, 318, 1402-1407.
42. Poser, I., Sarov, M., Hutchins, J. R., Heriche, J. K. et al., BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods 2008, 5, 409-415.
43. Hu, P., Janga, S. C., Babu, M., Diaz-Mejia, J. J. et al., Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol. 2009, 7, e96.
44. Glatter, T., Wepf, A., Aebersold, R., Gstaiger, M., An integrated workflow for charting the human interaction proteome: insights into the PP2A system. Mol. Syst. Biol. 2009, 5, 237-250.
45. Sowa, M. E., Bennett, E. J., Gygi, S. P., Harper, J. W., Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138, 389-403.
46. Behrends, C., Sowa, M. E., Gygi, S. P., Harper, J. W., Network organization of the human autophagy system. Nature 2010, 466, 68-76.
47. Hutchins, J. R., Toyoda, Y., Hegemann, B., Poser, I. et al., Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328, 593-599.
48. Bürckstümmer, T., Bennett, K. L., Preradovic, A., Schütze, G. et al., An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat. Methods 2006, 3, 1013-1019.
49. Ewing, R. M., Chu, P., Elisma, F., Li, H. et al., Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Syst. Biol. 2007, 3, 89-105.
50. Van Leene, J., Hollunder, J., Eeckhout, D., Persiau, G. et al., Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6, 397.
51. Rohila, J. S., Chen, M., Chen, S., Chen, J. et al., Protein-protein interactions of tandem affinity purified protein kinases from rice. PLoS One 2009, 4, e6685.
52. Veraksa, A., Bauer, A., Artavanis-Tsakonas, S., Analyzing protein complexes in Drosophila with tandem affinity purification-mass spectrometry. Dev. Dyn. 2005, 232, 827-834.
53. Agell, N., Bachs, O., Rocamora, N., Villalonga, P., Modulation of the Ras/Raf/MEK/ERK pathway by Ca(2+), and calmodulin. Cell Signal 2002, 14, 649-654.
54. Head, J. F., A better grip on calmodulin. Curr. Biol. 1992, 2, 609-611.
55. Knuesel, M., Wan, Y., Xiao, Z., Holinger, E. et al., Identification of novel protein-protein interactions using a versatile mammalian tandem affinity purification expression system. Mol. Cell. Proteomics 2003, 2, 1225-1233.
56. Gloeckner, C. J., Boldt, K., Schumacher, A., Roepman, R. et al., A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 2007, 7, 4228-4234.
57. Schimanski, B., Nguyen, T. N., Gunzl, A., Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination. Eukaryot. Cell 2005, 4, 1942-1950.
58. Drakas, R., Prisco, M., Baserga, R., A modified tandem affinity purification tag technique for the purification of protein complexes in mammalian cells. Proteomics 2005, 5, 132-137.
59. Forler, D., Kocher, T., Rode, M., Gentzel, M. et al., An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat. Biotechnol. 2003, 21, 89-92.
60. Selbach, M., Mann, M., Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK). Nat. Methods 2006, 3, 981-983.
61. Kittler, R., Pelletier, L., Ma, C., Poser, I. et al., RNA interference rescue by bacterial artificial chromosome transgenesis in mammalian tissue culture cells. Proc. Natl. Acad. Sci. USA 2005, 102, 2396-2401.
62. Kyriakakis, P., Tipping, M., Abed, L., Veraksa, A., Tandem affinity purification in Drosophila: the advantages of the GS-TAP system. Fly 2008, 2, 229-235.
63. Honey, S., Schneider, B. L., Schieltz, D. M., Yates, J. R. et al., A novel multiple affinity purification tag and its use in identification of proteins associated with a cyclin-CDK complex. Nucleic Acids Res. 2001, 29, E24.
64. Rubio, V., Shen, Y., Saijo, Y., Liu, Y. et al., An alternative tandem affinity purification strategy applied to Arabidopsis protein complex isolation. Plant J. 2005, 41, 767-778.
65. Libby, R. T., Cosman, D., Cooney, M. K., Merriam, J. E. et al., Human rhinovirus 3C protease: cloning and expression of an active form in Escherichia coli. Biochemistry 1988, 27, 6262-6268.
66. Rinner, O., Seebacher, J., Walzthoeni, T., Mueller, L. N. et al., Identification of cross-linked peptides from large sequence databases. Nat. Methods 2008, 5, 315-318.
67. Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F. et al., Probing native protein structures by chemical cross-linking, mass spectrometry and bioinformatics. Mol. Cell. Proteomics 2010, 9, 1634-1649.
68. Tagwerker, C., Flick, K., Cui, M., Guerrero, C. et al., A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivocross-linking. MCP 2006, 5, 737-748.
69. Petroski, M. D., Deshaies, R. J., Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 2005, 123, 1107-1120.
70. Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F. et al., Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol. Cell. Proteomics 2010, 9, 1634-1649.
71. Moorman, N. J., Sharon-Friling, R., Shenk, T., Cristea, I. M., A targeted spatial-temporal proteomics approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol. Cell. Proteomics 2010, 9, 851-860.
72. Chen, G. I., Gingras, A.-C., Affinity-purification mass spectrometry (AP-MS) of serine/threonine phosphatases. Methods 2007, 42, 298-305.
73. Tackett, A., DeGrasse, J., Sekedat, M., Oeffinger, M. et al., I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J. Proteome Res. 2005, 4, 1752-1756.
74. Ramisetty, S. R., Washburn, M. P., Unraveling the dynamics of protein interactions with quantitative mass spectrometry. Crit. Rev. Biochem. Mol. Biol. 2011, 46, 216-228.
75. Lundgren, D. H., Hwang, S. I., Wu, L., Han, D. K., Role of spectral counting in quantitative proteomics. Expert Rev. Proteomics 2010, 7, 39-53.
76. Gingras, A.-C., Gstaiger, M., Raught, B., Aebersold, R., Analysis of protein complexes using mass spectrometry. Nat. Rev. Mol. Cell Biol. 2007, 8, 645-654.
77. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. et al., Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415, 180-183.
78. Marelli, M., Smith, J. J., Jung, S., Yi, E. et al., Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. J. Cell Biol. 2004, 167, 1099-1112.
79. Strambio-de-Castillia, C., Blobel, G., Rout, M. P., Proteins connecting the nuclear pore complex with the nuclear interior. J. Cell Biol. 1999, 144, 839-855.
80. Devos, D., Dokudovskaya, S., Alber, F., Williams, R. et al., Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol. 2004, 2, e380.
81. Rothbauer, U., Zolghadr, K., Muyldermans, S., Schepers, A. et al., A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol. Cell. Proteomics 2008, 7, 282-289.
82. Einhauer, A., Jungbauer, A., The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J. Biochem. Biophys. Methods 2001, 49, 455-465.
83. Hartmuth, K., Vornlocher, H.-P., Luhrmann, R., Tobramycin affinity tag purification of spliceosomes. Method. Mol. Biol. 2004, 257, 47-64.
84. Lingner, J., Cech, T. R., Purification of telomerase from Euplotes aediculatus: requirement of a primer 3' overhang. Proc. Natl. Acad. Sci. USA 1996, 93, 10712-10717.
85. Carey, J., Uhlenbeck, O. C., Kinetic and thermodynamic characterization of the R17 coat protein-ribonucleic acid interaction. Biochemistry 1983, 22, 2610-2615.
86. Bachler, M., Schroeder, R., von Ahsen, U., StreptoTag: a novel method for the isolation of RNA-binding proteins. RNA 1999, 5, 1509-1516.
87. Srisawat, C., Engelke, D. R., Streptavidin aptamers: affinity tags for the study of RNAs and ribonucleoproteins. RNA (New York, NY) 2001, 7, 632-641.
88. Jurica, M. S., Moore, M. J., Capturing splicing complexes to study structure and mechanism. Methods 2002, 28, 336-345.
89. Hogg, J., Collins, K., RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA 2007, 13, 868-880.
90. Hogg, J. R., Goff, S. P., Upf1 senses 3′UTR length to potentiate mRNA decay. Cell 2010, 143, 379-389.
91. Holstege, F., Jennings, E., Wyrick, J., Lee, T. et al., Dissecting the regulatory circuitry of a eukaryotic genome. Cell 1998, 95, 717-728.
92. Zenklusen, D., Larson, D. R., Singer, R. H., Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 2008 15, 1263-1271.
93. Ghaemmaghami, S., Huh, W., Bower, K., Howson, R. et al., Global analysis of protein expression in yeast. Nature 2003, 425, 737-741.
94. Oeffinger, M., Wei, K., Rogers, R., DeGrasse, J. et al., Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 2007, 4, 951-956.
95. de Lichtenberg, U., Jensen, L. J., Brunak, S., Bork, P., Dynamic complex formation during the yeast cell cycle. Science 2005, 307, 724-727.
96. Perez-Fernandez, J., Roman, A., De Las Rivas, J., Bustelo, X. R. et al., The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 2007, 27, 5414-5429.
97. Lebreton, A., Rousselle, J.-C., Lenormand, P., Namane, A. et al., 60S ribosomal subunit assembly dynamics defined by semi-quantitative mass spectrometry of purified complexes. Nucleic Acids Res. 2008, 36, 4988-4999.
98. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
99. Schäfer, T., Maco, B., Petfalski, E., Tollervey, D. et al., Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 2006, 441, 651-655.
100. Bassler, J., Kallas, M., Pertschy, B., Ulbrich, C. et al., The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell 2010, 38, 712-721.
101. Rinner, O., Mueller, L. N., Hubálek, M., Müller, M. et al., An integrated mass spectrometric and computational framework for the analysis of protein interaction networks. Nat. Biotechnol. 2007, 25, 345-352.
102. Boulon, S., Ahmad, Y., Trinkle-Mulcahy, L., Verheggen, C. et al., Establishment of a protein frequency library and its application in the reliable identification of specific protein interaction partners. Mol. Cell. Proteomics 2010, 9, 861-879.
103. Gouw, J. W., Krijgsveld, J., Heck, A. J., Quantitative proteomics by metabolic labeling of model organisms. Mol. Cell. Proteomics 2010, 9, 11-24.
104. Choudhary, C., Mann, M., Decoding signalling networks by mass spectrometry-based proteomics. Nat. Rev. Mol. Cell Biol. 2010, 11, 427-439.
105. Asara, J. M., Christofk, H. R., Freimark, L. M., Cantley, L. C., A label-free quantification method by MS/MS TIC compared to SILACand spectral counting in a proteomics screen. Proteomics 2008, 8, 994-999.
106. Choi, H., Larsen, B., Lin, Z. Y., Breitkreutz, A. et al., SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat. Methods 2011, 8, 70-73.
107. Skarra, D. V., Goudreault, M., Choi, H., Mullin, M. et al., Label-free quantitative proteomics and SAINT analysis enable interactome mapping for the human Ser/Thr protein phosphatase 5. Proteomics 2011, 11, 1508-1516.
108. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
109. Brand, M., Ranish, J. A., Kummer, N. T., Hamilton, J. et al., Dynamic changes in transcription factor complexes during erythroid differentiation revealed by quantitative proteomics. Nat. Struct. Mol. Biol. 2004, 11, 73-80.
110. Andersen, J., Lam, Y., Leung, A., Ong, S. et al., Nucleolar proteome dynamics. Nature 2005, 433, 77-83.
111. Wang, X., Huang, L., Identifying dynamic interactors of protein complexes by quantitative mass spectrometry. Mol. Cell. Proteomics 2008, 7, 46-57.
112. Mousson, F., Kolkman, A., Pijnappel, W. W., Timmers, H. T. et al., Quantitative proteomics reveals regulation of dynamic components within TATA-binding protein (TBP) transcription complexes. Mol. Cell. Proteomics 2008, 7, 845-852.
113. Fang, L., Wang, X., Yamoah, K., Chen, P. L. et al., Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J. Proteome Res. 2008, 7, 4914-4925.
114. Mittler, G., Butter, F., Mann, M., A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res. 2009, 19, 284-293.
115. Jain, R., Devine, T., George, A. D., Chittur, S. V. et al., RIP-chip analysis: rna-binding protein immunoprecipitation-microarray (chip) profiling. Method. Mol. Biol. 2011, 703, 247-263.
116. Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M. et al., RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008, 18, 1509-1517.
117. Pan, Q., Shai, O., Lee, L. J., Frey, B. J. et al., Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 2008, 40, 1413-1415.
118. Sanford, J. R., Wang, X., Mort, M., Vanduyn, N. et al., Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 2009, 19, 381-394.
119. Ingolia, N. T., Ghaemmaghami, S., Newman, J. R., Weissman, J. S., Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324, 218-223.
120. Zhang, C., Darnell, R. B., Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 2011, 29, 607-614.
121. Taoka, M., Ikumi, M., Nakayama, H., Masaki, S. et al., In-gel digestion for mass spectrometric characterization of RNA from fluorescently stained polyacrylamide gels. Anal. Chem. 2010, 82, 7795-7803.
122. Yu, H., Braun, P., Yildirim, M. A., Lemmens, I. et al., High-quality binary protein interaction map of the yeast interactome network. Science 2008, 322, 104-110.
123. Picotti, P., Rinner, O., Stallmach, R., Dautel, F. et al., High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nat. Methods 2010, 7, 43-46.
124. Bisson, N., James, D. A., Ivosev, G., Tate, S. A. et al., Selected reaction monitoring mass spectrometry reveals the dynamics of signaling through the GRB2 adaptor. Nat. Biotechnol. 2011, 29, 653-658.
125. Puts, C. F., Lenoir, G., Krijgsveld, J., Williamson, P. et al., A P4-ATPase protein interaction network reveals a link between aminophospholipid transport and phosphoinositide metabolism. J. Proteome Res. 2010, 9, 833-842.
126. Zhang, H., Tang, X., Munske, G. R., Tolic, N. et al., Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry. Mol. Cell. Proteomics 2009, 8, 409-420.
127. Alvarez-Rueda, N., Behar, G., Ferre, V., Pugniere, M. et al., Generation of llama single-domain antibodies against methotrexate, a prototypical hapten. Mol. Immunol. 2007, 44, 1680-1690.
128. Kühner, S., van Noort, V., Betts, M. J., Leo-Macias, A. et al., Proteome organization in a genome-reduced bacterium. Science 2009, 326, 1235-1240.
129. Colwill, K., Gräslund, S., A roadmap to generate renewable protein binders to the human proteome. Nat. Methods 2011, 8, 551-558.
130. Lamond, A. I., Sproat, B., Ryder, U., Hamm, J. Probing the structure and function of U2 snRNP with antisense oligonucleotides made of 2'-OMe RNA. Cell 1989, 58, 383-390.
131. Kurth, I., Cristofari, G., Lingner, J. An affinity oligonucleotide displacement strategy to purify ribonucleoprotein complexes applied to human telomerase. Methods Mol. Biol. 2008, 488, 9-22.
132. Lejeune, F., Maquat, L. E. Immunopurification and analysis of protein and RNA components of mRNP in mammalian cells. Methods Mol. Biol. 2004, 257, 115-124.
133. Beach, D. L., Keene, J. D. Ribotrap: targeted purification of RNA-specific RNPs from cell lysates through immunoaffinity precipitation to identify regulatory proteins and RNAs. Methods Mol. Biol. 2008, 419, 69-91.
134. Di Tomasso, G., Lampron, P., Dagenais, P., Omichinski, J. G. et al. The ARiBo tag: a reliable tool for affinity purification of RNAs under native conditions. Nucleic Acids Res. 2011, 39(3), 18-28.
135. Butter F, Scheibe M, Mörl M, Mann M. Unbiased RNA-protein interaction screen by quantitative proteomics. Proc. Natl. Acad. Sci. USA 2009, 106, 10626-10631.
136. Slobodin, B., Gerst, J. E. A novel mRNA affinity purification technique for the identification of interacting proteins and transcripts in ribonucleoprotein complexes. RNA 2010, 16, 2277-2290.