A proteogenomics approach integrating proteomics and ribosome profiling increases the efficiency of protein identification and enables the discovery of alternative translation start sites

Proteomics

Volumn 14, Issue 23-24, 2014, Pages 2688-2698

  Koch, Alexander ^a   Gawron, Daria ^a,b   Steyaert, Sandra ^a   Ndah, Elvis ^a,b   Crappé, Jeroen ^a   De Keulenaer, Sarah ^a   De Meester, Ellen ^a   Ma, Ming ^c   Shen, Ben ^c   Gevaert, Kris ^a,b   Van Criekinge, Wim ^a   Van Damme, Petra ^a,b   Menschaert, Gerben ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Department of Plant Systems Biology   (Belgium)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Bioinformatics; N terminomics; Proteogenomics; Ribosome profiling; Translation initiation

Indexed keywords

MESSENGER RNA; PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOMICS; HCT116 CELL LINE; HUMAN; HUMAN CELL; NEXT GENERATION SEQUENCING; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEOMICS; RIBOSOME PROFILING; RNA SEQUENCE; RNA TRANSLATION; TANDEM MASS SPECTROMETRY; TRANSLATION INITIATION; TRANSLATION START SITE; BIOLOGY; GENETICS; METABOLISM; PROCEDURES; RIBOSOME;

COMPUTATIONAL BIOLOGY; HCT116 CELLS; HUMANS; PROTEIN BIOSYNTHESIS; PROTEINS; PROTEOMICS; RIBOSOMES; TANDEM MASS SPECTROMETRY;

EID: 84914094148     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400180     Document Type: Article

References (57)

1. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
2. Craig, R., Beavis, R. C., TANDEM: matching proteins with tandem mass spectra. Bioinformatics 2004, 20, 1466-1467.
3. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L. et al., Open mass spectrometry search algorithm. J. Proteome Res. 2004, 3, 958-964.
4. Staes, A., Impens, F., Van Damme, P., Ruttens, B. et al., Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat. Protoc. 2011, 6, 1130-1141.
5. Nagaraj, N., Wisniewski, J. R., Geiger, T., Cox, J. et al., Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 2011, 7, 548.
6. Liu, S., Im, H., Bairoch, A., Cristofanilli, M. et al., A chromosome-centric human proteome project (C-HPP) to characterize the sets of proteins encoded in chromosome 17. J. Proteome Res. 2013, 12, 45-57.
7. Woo, S., Cha, S. W., Merrihew, G., He, Y. et al., Proteogenomic database construction driven from large scale RNA-seq data. J. Proteome Res. 2014, 13, 21-28.
8. Pinto, S. M., Manda, S. S., Kim, M. S., Taylor, K. et al., Functional annotation of proteome encoded by human chromosome 22. J. Proteome Res. 2014, 13, 2749-2760.
9. Wang, X., Slebos, R. J., Wang, D., Halvey, P. J. et al., Protein identification using customized protein sequence databases derived from RNA-Seq data. J. Proteome Res. 2012, 11, 1009-1017.
10. Ning, K., Nesvizhskii, A. I., The utility of mass spectrometry-based proteomic data for validation of novel alternative splice forms reconstructed from RNA-Seq data: a preliminary assessment. BMC Bioinformatics 2010, 11(Suppl 11) S14.
11. Ning, K., Fermin, D., Nesvizhskii, A. I., Comparative analysis of different label-free mass spectrometry based protein abundance estimates and their correlation with RNA-Seq gene expression data. J. Proteome Res. 2012, 11, 2261-2271.
12. Beck, M., Schmidt, A., Malmstroem, J., Claassen, M. et al., The quantitative proteome of a human cell line. Mol. Syst. Biol. 2011, 7, 549.
13. Djebali, S., Davis, C. A., Merkel, A., Dobin, A. et al., Landscape of transcription in human cells. Nature 2012, 489, 101-108.
14. Low, T. Y., van Heesch, S., van den Toorn, H., Giansanti, P. et al., Quantitative and qualitative proteome characteristics extracted from in-depth integrated genomics and proteomics analysis. Cell Rep. 2013, 5, 1469-1478.
15. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z. et al., Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455, 58-63.
16. Sonenberg, N., Hinnebusch, A. G., New modes of translational control in development, behavior, and disease. Mol. Cell 2007, 28, 721-729.
17. Baek, D., Villen, J., Shin, C., Camargo, F. D. et al., The impact of microRNAs on protein output. Nature 2008, 455, 64-71.
18. Touriol, C., Bornes, S., Bonnal, S., Audigier, S. et al., Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol. Cell 2003, 95, 169-178.
19. Michel, A. M., Choudhury, K. R., Firth, A. E., Ingolia, N. T. et al., Observation of dually decoded regions of the human genome using ribosome profiling data. Genome Res. 2012, 22, 2219-2229.
20. Namy, O., Rousset, J. P., Napthine, S., Brierley, I., Reprogrammed genetic decoding in cellular gene expression. Mol. Cell 2004, 13, 157-168.
21. Ingolia, N. T., Genome-wide translational profiling by ribosome footprinting. Methods Enzymol. 2010, 470, 119-142.
22. Ingolia, N. T., Lareau, L. F., Weissman, J. S., Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011, 147, 789-802.
23. Lee, S., Liu, B., Lee, S., Huang, S. X. et al., Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, E2424-E2432.
24. Menschaert, G., Van Criekinge, W., Notelaers, T., Koch, A. et al., Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol. Cell. Proteomics 2013, 12, 1780-1790.
25. Guttman, M., Rinn, J. L., Modular regulatory principles of large non-coding RNAs. Nature 2012, 482, 339-346.
26. Volders, P. J., Helsens, K., Wang, X., Menten, B. et al., LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic Acids Res. 2013, 41, D246-D251.
27. Bazzini, A. A., Johnstone, T. G., Christiano, R., Mackowiak, S. D. et al., Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation. EMBO J. 2014, 33, 981-993.
28. Van Damme, P., Gawron, D., Van Criekinge, W., Menschaert, G., N-terminal proteomics and ribosome profiling provide a comprehensive view of the alternative translation initiation landscape in mice and men. Mol. Cell. Proteomics 2014, 13, 1245-1261.
29. Boeckmann, B., Bairoch, A., Apweiler, R., Blatter, M. C. et al., The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003, 31, 365-370.
30. Ishihama, Y., Oda, Y., Tabata, T., Sato, T. et al., Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 2005, 4, 1265-1272.
31. Paoletti, A. C., Parmely, T. J., Tomomori-Sato, C., Sato, S. et al., Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 18928-18933.
32. 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.
33. Ju, J., Lim, S. K., Jiang, H., Seo, J. W. et al., Iso-migrastatin congeners from Streptomyces platensis and generation of a glutarimide polyketide library featuring the dorrigocin, lactimidomycin, migrastatin, and NK30424 scaffolds. J. Am. Chem. Soc. 2005, 127, 11930-11931.
34. Schneider-Poetsch, T., Ju, J., Eyler, D. E., Dang, Y. et al., Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 2010, 6, 209-217.
35. Guo, H., Ingolia, N. T., Weissman, J. S., Bartel, D. P., Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466, 835-840.
36. Barsnes, H., Vizcaino, J. A., Eidhammer, I., Martens, L., PRIDE Converter: making proteomics data-sharing easy. Nat. Biotechnol. 2009, 27, 598-599.
37. Martens, L., Hermjakob, H., Jones, P., Adamski, M. et al., PRIDE: the proteomics identifications database. Proteomics 2005, 5, 3537-3545.
38. Vaudel, M., Barsnes, H., Berven, F. S., Sickmann, A. et al. SearchGUI: an open-source graphical user interface for simultaneous OMSSA and X!Tandem searches. Proteomics 2011, 11, 996-999.
39. Hirosawa, M., Hoshida, M., Ishikawa, M., Toya, T., MASCOT: multiple alignment system for protein sequences based on three-way dynamic programming. Comp. Appl. Biosci. 1993, 9, 161-167.
40. Edgar, R., Domrachev, M., Lash, A. E., Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30, 207-210.
41. Doherty, M. K., Hammond, D. E., Clague, M. J., Gaskell, S. J., Beynon, R. J., Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J. Proteome Res. 2009, 8, 104-112.
42. Sandoval, P. C., Slentz, D. H., Pisitkun, T., Saeed, F. et al., Proteome-wide measurement of protein half-lives and translation rates in vasopressin-sensitive collecting duct cells. J. Am. Soc. Nephrol. 2013, 24, 1793-1805.
43. Huang da, W., Sherman, B. T., Lempicki, R. A., Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37, 1-13.
44. Ivanov, I. P., Firth, A. E., Michel, A. M., Atkins, J. F., Baranov, P. V., Identification of evolutionarily conserved non-AUG-initiated N-terminal extensions in human coding sequences. Nucleic Acids Res. 2011, 39, 4220-4234.
45. Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C. et al., Protein identification and analysis tools in the ExPASy server. Methods in Mol. Biol. 1999, 112, 531-552.
46. Searle, B. C., Turner, M., Nesvizhskii, A. I., Improving sensitivity by probabilistically combining results from multiple MS/MS search methodologies. J. Proteome Res. 2008, 7, 245-253.
47. Colaert, N., Vandekerckhove, J., Gevaert, K., Martens, L., A comparison of MS2-based label-free quantitative proteomic techniques with regards to accuracy and precision. Proteomics 2011, 11, 1110-1113.
48. McIlwain, S., Mathews, M., Bereman, M. S., Rubel, E. W. et al., Estimating relative abundances of proteins from shotgun proteomics data. BMC Bioinformatics 2012, 13, 308.
49. Schwanhausser, B., Busse, D., Li, N., Dittmar, G. et al., Global quantification of mammalian gene expression control. Nature 2011, 473, 337-342.
50. Stern-Ginossar, N., Weisburd, B., Michalski, A., Le, V. T. et al., Decoding human cytomegalovirus. Science 2012, 338, 1088-1093.
51. Slavoff, S. A., Mitchell, A. J., Schwaid, A. G., Cabili, M. N. et al., Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat. Chem. Biol. 2013, 9, 59-64.
52. Branca, R. M., Orre, L. M., Johansson, H. J., Granholm, V. et al., HiRIEF LC-MS enables deep proteome coverage and unbiased proteogenomics. Nat. Methods 2014, 11, 59-62.
53. Wethmar, K., Begay, V., Smink, J. J., Zaragoza, K. et al., C/EBPbetaDeltauORF mice-a genetic model for uORF-mediated translational control in mammals. Genes Dev. 2010, 24, 15-20.
54. Medenbach, J., Seiler, M., Hentze, M. W., Translational control via protein-regulated upstream open reading frames. Cell 2011, 145, 902-913.
55. Michel, A., O'Connor, P., Choudhury, R. K., Firth, A. et al., EMBO Conference Series: Protein Synthesis and Translational Control. Heidelberg, Germany 2013.
56. Vasquez, J. J., Hon, C. C., Vanselow, J. T., Schlosser, A., Siegel, T. N., Comparative ribosome profiling reveals extensive translational complexity in different Trypanosoma brucei life cycle stages. Nucleic Acids Res. 2014, 42, 3623-3637.
57. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M. et al., The human genome browser at UCSC. Genome Res. 2002, 12, 996-1006.