Unbiased selective isolation of protein N-terminal peptides from complex proteome samples using phospho tagging (PTAG) and TiO2-based depletion

Molecular and Cellular Proteomics

Volumn 11, Issue 9, 2012, Pages 832-842

  Mommen, Geert P M ^a,b,c   Van De Waterbeemd, Bas ^a   Meiring, Hugo D ^a   Kersten, Gideon ^a   Heck, Albert J R ^b,c   De Jong, Ad P J M ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FORMALDEHYDE; INTERNAL PEPTIDE; LYSINE; MITOCHONDRIAL PROTEIN; PEPTIDE; PHOSPHOPEPTIDE; PROTEOME; TITANIUM DIOXIDE; UNCLASSIFIED DRUG;

ACETYLATION; AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DERIVATIZATION; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; NEISSERIA MENINGITIDIS; NONHUMAN; PHOSPHO TAGGING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN ISOLATION; PROTEOMICS; SACCHAROMYCES CEREVISIAE; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, LIQUID; FUNGAL PROTEINS; ISOTOPE LABELING; NEISSERIA MENINGITIDIS; PEPTIDE FRAGMENTS; PHOSPHATES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE; STAINING AND LABELING; TANDEM MASS SPECTROMETRY; TITANIUM;

NEISSERIA MENINGITIDIS;

EID: 84865727892     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.O112.018283     Document Type: Article

References (50)

1. Cox, J., and Mann, M. (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80, 273-299
2. McDonald, L., Robertson, D. H. Hurst, J. L., and Beynon, R. J. (2005) Positional proteomics: selective recovery and analysis of N-terminal proteolytic peptides. Nat. Methods 2, 955-957
3. McDonald, L., and Beynon, R. J. (2006) Positional proteomics: preparation of amino-terminal peptides as a strategy for proteome simplification and characterization. Nat. Protoc. 1, 1790-1798
4. Gevaert, K., Goethals, M., Martens, L., Van Damme, J., Staes, A., Thomas, G. R., and Vandekerckhove, J. (2003) Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat. Biotechnol. 21, 566-569
5. Doucet, A., Butler, G. S., Rodriguez, D., Prudova, A., and Overall, C. M. (2008) Metadegradomics: toward in vivo quantitative degradomics of proteolytic post-translational modifications of the cancer proteome. Mol. Cell. Proteomics 7, 1925-1951
6. Van Damme, P., Arnesen, T., and Gevaert, K. (2011) Protein alpha-Nacetylation studied by N-terminomics. FEBS J. 278, 3822-3834
7. Nakazawa, T., Yamaguchi, M., Okamura, T. A., Ando, E., Nishimura, O., and Tsunasawa, S. (2008) Terminal proteomics: N- and C-terminal analyses for high-fidelity identification of proteins using MS. Proteomics 8, 673-685
8. Huesgen, P. F., and Overall, C. M. (2011) N- and C-terminal degradomics: new approaches to reveal biological roles for plant proteases from substrate identification. Physiol Plant 145, 5-17
9. Schilling, O., Barré, O., Huesgen, P. F., and Overall, C. M. (2010) Proteomewide analysis of protein carboxy termini: C terminomics. Nat. Methods 7, 508-511
10. Van Damme, P., Staes, A., Bronsoms, S., Helsens, K., Colaert, N., Timmerma, E., Aviles, F. X., Vandekerckhove, J., and Gevaert, K. (2010) Complementary positional proteomics for screening substrates of endoand exoproteases. Nat. Methods 7, 512-515
11. Staes, A., Impens, F., Van Damme, P., Ruttens, B., Goethals, M., Demol, H., Timmerman, E.. Vandekerckhove, J., and Gevaert, K. (2011) Selecting protein N-terminal peptides by combined fractional diagonal chromatography. Nat. Protoc. 6, 1130-1141
12. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A., Schilling, O., Kainthan, R. K., Starr, A. E., Foster, L. J., Kizhakkedathu, J. N., and Overall, C. M. (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-288
13. Kleifeld, O., Doucet, A., Prudova, A., auf dem Keller, U., Gioia, M., Kizhakkedathu, J. N., and Overall, C. M. (2011) Identifying and quantifying proteolytic events and the natural N terminome by terminal amine isotopic labeling of substrates. Nat. Protoc. 6, 1578-1611
14. Beaudette, P., Rossi, N. A., Huesgen, P. F., Yu X., Shenoi, R. A., Doucet, A., Overall, C. M., and Kizhakkedathu. J. N. (2011) Development of soluble ester-linked aldehyde polymers for proteomics. Anal. Chem. 83, 6500-6510
15. Agard, N. J., and Wells, J. A. (2009) Methods for the proteomic identification of protease substrates. Curr. Opin. Chem. Biol. 13, 503-509
16. Timmer, J. C., Enoksson, M., Wildfang, E., Zhu, W., Igarashi, Y., Denault, J. B., Ma, Y., Dummitt, B., Chang, Y. H., Mast, A. E., Eroshkin, A., Smith, J. W., Tao, W. A., and Salvesen, G. S. (2007) Profiling constitutive proteolytic events in vivo. Biochem. J. 407, 41-48
17. Timmer, J. C., Zhu, W., Pop, C., Regan, T., Snipas, S. J., Eroshkin, A. M., Riedl, S. J., and Salvesen. G. S. (2009) Structural and kinetic determinants of protease substrates. Nat Struct Mol Biol. 16, 1101-1108
18. Mahrus, S., Trinidad, J. C., Barkan, D. T., Sali, A., Burlingame, A. L., and Wells. J. A. (2008) Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134, 866-876
19. Zhang, X., Ye, J., Engholm-Keller, K., and Hojrup, P. A proteome-scale study on in vivo protein Nalpha-acetylation using an optimized method. Proteomics 11, 81-93
20. Staes, A., Van Damme, P., Helsens, K., Demol, H., Vandekerckhove, J., and Gevaert, K. (2008) Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 8, 1362-1370
21. Dormeyer, W., Mohammed, S., Breukelen, B., Krijgsveld, J., and Heck, A. J. (2007) Targeted analysis of protein termini. J. Proteome Res. 6, 4634-4645
22. Helbig, A. O., Gauci, S., Raijmakers, R., van Breukelen, B., Slijper, M., Mohammed, S., and Heck, A. J. (2010) Profiling of N-acetylated protein termini provides in-depth insights into the N-terminal nature of the proteome. Mol. Cell. Proteomics 9, 928-939
23. Mohammed, S., and Heck, A. J. (2011) Strong cation exchange (SCX) based analytical methods for the targeted analysis of protein posttranslational modifications. Curr Opin Biotechnol. 22, 9-16
24. van de Waterbeemd, B., Streefland, M., van der Ley, P., Zomer, B., van Dijken, H., Martens, D., Wijffels, R., and van der Pol, L. (2010) Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine 28, 4810-6
25. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck. A. J., (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
26. Lemeer, S., Pinkse, M. W., Mohammed, S., van Breukelen, B., den Hertog, J., Slijper, M., and Heck, A. J. (2008) Online automated in vivo zebrafish phosphoproteomics: from large-scale analysis down to a single embryo. J. Proteome Res. 7, 1555-1564
27. Pinkse, M. W., Mohammed, S., Gouw, J. W., van Breukelen, B., Vos, H. R., and Heck. A. J. (2008) Highly robust, automated, and sensitive online TiO2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster. J. Proteome Res. 7, 687-697
28. Motoyama, A., Xu, T., Ruse, C. I., Wohlschlegel, J. A., and Yates, J. R., 3rd (2007) Anion and cation mixed-bed ion exchange for enhanced multidimensional separations of peptides and phosphopeptides. Anal. Chem. 79, 3623-3634
29. Meiring, H. D., van der Heeft, E., ten Hove, G. J., and de Jong, A. P. J. M. (2002) Nanoscale LC-MS(n) : technical design and applications to peptide and protein analysis. Sep. Sci. 25, 557-568
30. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971
31. Vogtle, F. N., Wortelkamp, S., Zahedi, R. P., Becker, D., Leidhold, C., Gevaert, K., Kellermann, J., Voos, W., Sickmann, A., Pfanner, N., and Meisinger, C. (2009) Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139, 428-439
32. Meiring, H. D., Soethout, E. C., de Jong, A. P., and van Els, C. A. (2007) Targeted identification of infection-related HLA class I-presented epitopes by stable isotope tagging of epitopes (SITE). Curr. Protoc. Immunol. 16, 16 3
33. Veenstra, T. D., Conrads, T. P., and Issaq, H. J. (2004) What to do with "one-hit wonders"? Electrophoresis 25, 1278-1279
34. Holst, J., Martin, D., Arnold, R., Huergo, C. C., Oster, P., O'Hallahan, J., and Rosenqvist, E. (2009) Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis. Vaccine 27, B3-12
35. Raijmakers, R., Kraiczek, K., de Jong, A. P., Mohammed, S., and Heck, A. J. (2010) Exploring the human leukocyte phosphoproteome using a microfluidic reversed-phase-TiO2-reversed-phase high-performance liquid chromatography phosphochip coupled to a quadrupole time-of-flight mass spectrometer. Anal. Chem. 82, 824-832
36. Boersema, P. J., Mohammed, S., and Heck, A. J. (2009) Phosphopeptide fragmentation and analysis by mass spectrometry. J. Mass Spectrom. 44, 861-878
37. Plasman, K., van Damme, P., Kaiserman, D., Impens, F., Demeyer, K., Helsens, K., Goethals, M., Bird, P. I., Vandekerckhove, J., and Gevaert, K. (2011) Probing the efficiency of proteolytic events by positional proteomics. Mol. Cell. Proteomics 10, 10.1074/mcp.M110 003301
38. Zhang, X., and Hojrup, P. (2010) Cyclization of the N-terminal X-Asn-Gly motif during sample preparation for bottom-up proteomics. Anal. Chem. 82, 8680-8685
39. Frottin, F., Martinez, A., Peynot, P., Mitra, S., Holz, R. C., Giglione, C., and Meinnel, T. (2006) The proteomics of N-terminal methionine cleavage. Mol. Cell. Proteomics 5, 2336-2349
40. Michalski, A., Cox, J., and Mann, M. (2011) More than 100,000 detectable peptide species elute in single shotgun proteomics runs but the majority is inaccessible to data-dependent LC-MS/MS. J. Proteome Res. 10, 1785-1793
41. Mischerikow, N., and Heck, A. J. (2011) Targeted large-scale analysis of protein acetylation. Proteomics 11, 571-589
42. Mogk, A., Schmidt, R., and Bukau, B. (2007) The N-end rule pathway for regulated proteolysis: prokaryotic and eukaryotic strategies. Trends Cell Biol. 17, 165-172
43. Arnesen, T., Van Damme, P., Polevoda, B., Helsens, K., Evjenth, R., Colaert, N., Varhaug, J. E., Vandekerckhove, J., Lillehaug, J. R., Sherman, F., and Gevaert, K. (2009) Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proc. Natl. Acad. Sci. U.S.A. 106, 8157-8162
44. Lange, P. F., and Overall, C. M. (2011) TopFIND, a knowledgebase linking protein termini with function. Nat Methods 8, 703-704
45. auf dem Keller, U., Prudova, A., Gioia, M., Butler, G. S., and Overall, C. M. (2010) A statistics-based platform for quantitative N-terminome analysis and identification of protease cleavage products. Mol. Cell. Proteomics 9 912-27
46. Frese, C. K., Altelaar, A. F., Hennrich, M. L., Nolting, D., Zeller, M., Griep-Raming, J., Heck, A. J., and Mohammed, S. (2011) Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap Velos. J. Proteome Res. 10, 2377-2388
47. Helsens, K., Van Damme, P., Degroeve, S., Martens, L., Arnesen, T., Vandekerckhove, J., and Gevaert, K. (2011) Bioinformatics analysis of a Saccharomyces cerevisiae N-terminal proteome provides evidence of alternative translation initiation and post-translational N-terminal acetylation. J. Proteome Res. 10, 3578-3589
48. Helbig, A. O., Rosati, S., Pijnappel, P. W., van Breukelen, B., Timmers, M. H., Mohammed, S., Slijper, M., and Heck, A. J. (2010) Perturbation of the yeast N-acetyltransferase NatB induces elevation of protein phosphorylation levels. BMC Genomics 11, 685
49. Miller Jenkins, L. M., Durell, S. R., Mazur, S. J., and Appella, E. (2012) p53 N-Terminal Phosphorylation: A Defining Layer of Complex Regulation. Carcinogenesis 10.1093/carcin/bgs145
50. Vener, A .V., Harms, A., Sussman, M. R., and Vierstra, R. D. (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J. Biol. Chem. 276, 6959-6966