An improved workflow for quantitative N-terminal charge-based fractional diagonal chromatography (ChaFRADIC) to study proteolytic events in Arabidopsis thaliana

Proteomics

Volumn 15, Issue 14, 2015, Pages 2458-2469

  Venne, A Saskia ^a   Solari, Fiorella A ^a   Faden, Frederik ^b,c   Paretti, Tomasso ^a,d   Dissmeyer, Nico ^b,c   Zahedi, René P ^a  

^a LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c ScienceCampus Halle Plant based Bioeconomy   (Germany)

^d UNIVERSITY OF PAVIA   (Italy)

Author keywords

N End rule pathway; N Terminal methionine excision; NERD; Protein degradation; Technology; Two dimensional chromatography

Indexed keywords

AMINO ACID; PLANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; CELLULAR DISTRIBUTION; CHARGE BASED FRACTIONAL DIAGONAL CHROMATOGRAPHY; CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; SENSITIVITY ANALYSIS; WILD TYPE; WORKFLOW;

EID: 85006467151     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201500014     Document Type: Article

References (76)

1. Harbauer, A. B., Zahedi, R. P., Sickmann, A., Pfanner, N., Meisinger, C., The protein import machinery of mitochondria-a regulatory hub in metabolism, stress, and disease. Cell Metab. 2014, 19, 357–374.
2. López-Otín, C., Bond, J. S., Proteases: multifunctional enzymes in life and disease. J. Biol. Chem. 2008, 283, 30433–30437.
3. Rogers, L. D., Overall, C. M., Proteolytic post-translational modification of proteins: proteomic tools and methodology. Mol. Cell. Proteomics 2013, 12, 3532–3542.
4. Mossmann, D., Meisinger, C., Vögtle, F., Processing of mitochondrial presequences. Biochim. Biophys. Acta (BBA)-Gene Regul. Mech. 2012, 1819, 1098–1106.
5. Reinders, J., Zahedi, R. P., Pfanner, N., Meisinger, C., Sickmann, A., Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J. Proteome Res. 2006, 5, 1543–1554.
6. Sickmann, A., Reinders, J., Wagner, Y., Joppich, C. et al., The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. U S A 2003, 100, 13207–13212.
7. Vögtle, F., Wortelkamp, S., Zahedi, R. P., Becker, D. et al., Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 2009, 139, 428–439.
8. Majovsky, P., Naumann, C., Lee, C.-W., Lassowskat, I. et al., Targeted proteomics analysis of protein degradation in plant signaling on an LTQ-Orbitrap mass spectrometer. J. Proteome Res. 2014, 13, 4246–4258.
9. Tasaki, T., Sriram, S. M., Park, K. S., Kwon, Y. T., The N-end rule pathway. Annu. Rev. Biochem. 2012, 81, 261–289.
10. Varshavsky, A., The N-end rule pathway and regulation by proteolysis. Protein Sci. 2011, 20, 1298–1345.
11. Bachmair, A., Finley, D., Varshavsky, A., In vivo half-life of a protein is a function of its amino-terminal residue. Science 1986, 234, 179–186.
12. Gibbs, D. J., Bacardit, J., Bachmair, A., Holdsworth, M. J., The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends Cell Biol. 2014, 24, 603–611
13. O'Brien, R. J., Wong, P. C., Amyloid precursor protein processing and Alzheimer's disease. Annu. Rev. Neurosci. 2011, 34, 185–204.
14. Lange, P. F., Overall, C. M., Protein TAILS: when termini tell tales of proteolysis and function. Curr. Opin. Chem. Biol. 2013, 17, 73–82.
15. De Strooper, B., Annaert, W., Novel research horizons for presenilins and γ-secretases in cell biology and disease. Annu. Rev. Cell Dev. Biol.2010, 26, 235–260.
16. Mossmann, D., Vogtle, F. N., Taskin, A. A., Teixeira, P. F. et al., Amyloid-beta peptide induces mitochondrial dysfunction by inhibition of preprotein maturation. Cell Metab. 2014, 20, 662–669.
17. Duffy, M. J., The role of proteolytic enzymes in cancer invasion and metastasis. Clin. Exp. Metastasis 1992, 10, 145–155.
18. Westley, B., May, F., Prognostic value of cathepsin D in breast cancer. Br. J. Cancer 1999, 79, 189–190.
19. Rakash, S., Rana, F., Rafiq, S., Masood, A., Amin, S., Role of proteases in cancer: a review. Biotechnol. Mol. Biol. Rev. 2012, 7, 90–101.
20. Stacker, S. A., Achen, M. G., Jussila, L., Baldwin, M. E., Alitalo, K., Metastasis: lymphangiogenesis and cancer metastasis. Nat. Rev. Cancer 2002, 2, 573–583.
21. van der Hoorn, R. A., Plant proteases: from phenotypes to molecular mechanisms. Annu. Rev. Plant Biol. 2008, 59, 191–223.
22. Feller, U., Proteolysis. In: Plant Cell Death Processes (ed. Noodén, L.D.). Elsevier Academic Press, Amsterdam, 2004, 107–123.
23. Rawlings, N. D., Waller, M., Barrett, A. J., Bateman, A., MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2014, 42 (Database issue), D503–D509.
24. Bonissone, S., Gupta, N., Romine, M., Bradshaw, R. A., Pevzner, P. A., N-terminal protein processing: a comparative proteogenomic analysis. Mol. Cell. Proteomics 2013, 12, 14–28.
25. Giglione, C., Boularot, A., Meinnel, T., Protein N-terminal methionine excision. Cell. Mol. Life Sci. 2004, 61, 1455–1474.
26. Bienvenut, W. V., Sumpton, D., Martinez, A., Lilla, S. et al., Comparative large scale characterization of plant versus mammal proteins reveals similar and idiosyncratic N-alpha-acetylation features. Mol. Cell. Proteomics 2012, 11, M111.015131.
27. Kim, H.-K., Kim, R.-R., Oh, J.-H., Cho, H. et al., The N-terminal methionine of cellular proteins as a degradation signal. Cell 2014, 156, 158–169.
28. Hwang, C.-S., Shemorry, A., Varshavsky, A., N-terminal acetylation of cellular proteins creates specific degradation signals. Science 2010, 327, 973–977.
29. Wang, H., Piatkov, K. I., Brower, C. S., Varshavsky, A., Glutamine-specific N-terminal amidase, a component of the N-end rule pathway. Mol. Cell. 2009, 34, 686–695.
30. Kwon, Y. T., Balogh, S. A., Davydov, I. V., Kashina, A. S. et al., Altered activity, social behavior, and spatial memory in mice lacking the NTAN1p amidase and the asparagine branch of the N-end rule pathway. Mol. Cell. Biol. 2000, 20, 4135–4148.
31. Grigoryev, S., Stewart, A. E., Kwon, Y. T., Arfin, S. M.et al., A mouse amidase specific for N-terminal asparagine the gene, the enzyme, and their function in the N-end rule pathway. J. Biol. Chem. 1996, 271, 28521–28532.
32. Baker, R. T., Varshavsky, A., Yeast N-terminal amidase a new enzyme and component of the N-end rule pathway. J. Biol. Chem. 1995, 270, 12065–12074.
33. Kwon, Y. T., Kashina, A. S., Davydov, I. V., Hu, R.-G. et al., An essential role of N-terminal arginylation in cardiovascular development. Science 2002, 297, 96–99.
34. Balzi, E., Choder, M., Chen, W., Varshavsky, A., Goffeau, A., Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J. Biol. Chem. 1990, 265, 7464–7471.
35. Hu, R.-G., Sheng, J., Qi, X., Xu, Z. et al., The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 2005, 437, 981–986.
36. Lee, M. J., Tasaki, T., Moroi, K., An, J. Y. et al., RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl. Acad. Sci. U S A 2005, 102, 15030–15035.
37. Weits, D. A., Giuntoli, B., Kosmacz, M., Parlanti, S. et al., Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat. Commun. 2014, 5, 3425.
38. Hu, R.-G., Wang, H., Xia, Z., Varshavsky, A., The N-end rule pathway is a sensor of heme. Proc. Natl. Acad. Sci. U S A 2008, 105, 76–81.
39. Ditzel, M., Wilson, R., Tenev, T., Zachariou, A. et al., Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat. Cell Biol. 2003, 5, 467–473.
40. Huesgen, P. F., Overall, C. M., N-and C-terminal degradomics: new approaches to reveal biological roles for plant proteases from substrate identification. Physiol. Plant. 2012, 145, 5–17.
41. Xu, G., Shin, S. B. Y., Jaffrey, S. R., Global profiling of protease cleavage sites by chemoselective labeling of protein N-termini. Proc. Natil. Acad. Sci. 2009, 106, 19310–19315.
42. Timmer, J., Enoksson, M., Wildfang, E., Zhu, W. et al., Profiling constitutive proteolytic events in vivo. Biochem. J. 2007, 407, 41–48.
43. Mahrus, S., Trinidad, J. C., Barkan, D. T., Sali, A. et al., Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 2008, 134, 866–876.
44. Gevaert, K., Goethals, M., Martens, L., Van Damme, J. et al., Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat. Biotechnol. 2003, 21, 566–569.
45. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A. et al., Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 2010, 28, 281–288.
46. Bland, C., Bellanger, L., Armengaud, J., Magnetic immunoaffinity enrichment for selective capture and MS/MS analysis of N-terminal-TMPP-labeled peptides. J. Proteome Res. 2013, 13, 668–680.
47. Mommen, G. P., van de Waterbeemd, B., Meiring, H. D., Kersten, G. et al., Unbiased selective isolation of protein N-terminal peptides from complex proteome samples using phospho tagging (PTAG) and TiO2-based depletion. Mol. Cell. Proteomics 2012, 11, 832–842.
48. Venne, A. S., Vögtle, F.-N., Meisinger, C., Sickmann, A., Zahedi, R. P., Novel highly sensitive, specific, and straightforward strategy for comprehensive N-terminal proteomics reveals unknown substrates of the mitochondrial peptidase Icp55. J. Proteome Res. 2013, 12, 3823–3830.
49. Staes, A., Van Damme, P., Helsens, K., Demol, H. et al., Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 2008, 8, 1362–1370.
50. Gevaert, K., Vandekerckhove, J., Reverse-Phase Diagonal Chromatography for Phosphoproteome Research. Methods Mol. Biol. 2009, 527, 219–227.
51. Gevaert, K., Ghesquière, B., Staes, A., Martens, L. et al., Reversible labeling of cysteine-containing peptides allows their specific chromatographic isolation for non-gel proteome studies. Proteomics 2004, 4, 897–908.
52. Ghesquière, B., Buyl, L., Demol, H., Van Damme, J. et al., A new approach for mapping sialylated N-glycosites in serum proteomes. J. Proteome Res. 2007, 6, 4304–4312.
53. Ghesquière, B., Colaert, N., Helsens, K., Dejager, L. et al., In vitro and in vivo protein-bound tyrosine nitration characterized by diagonal chromatography. Mol. Cell. Proteomics 2009, 8, 2642–2652.
54. Hennrich, M. L., van den Toorn, H. W., Groenewold, V., Heck, A. J., Mohammed, S., Ultra acidic strong cation exchange enabling the efficient enrichment of basic phosphopeptides. Anal. Chem. 2012, 84, 1804–1808.
55. Carrie, C., Venne, A. S., Zahedi, R. P., Soll, J., Identification of cleavage sites and substrate proteins for two mitochondrial intermediate peptidases in Arabidopsis thaliana. J. Exp. Bot. 2015, 66, 2691–2708.
56. Venne, A. S., Zahedi, R. P., The potential of fractional diagonal chromatography strategies for the enrichment of post-translational modifications. EuPA Open Proteomics 2014, 4, 165–170.
57. Hsu, J.-L., Huang, S.-Y., Chow, N.-H., Chen, S.-H., Stable-isotope dimethyl labeling for quantitative proteomics. Anal. Chem. 2003, 75, 6843–6852.
58. Gonczarowska-Jorge, H., Dell'Aica, M., Dickhut, C., Zahedi, R. P., Variable digestion strategies for phosphoproteomics analysis. Methods Mol. Biol. 2015, 1027, 123–129.
59. Burkhart, J. M., Schumbrutzki, C., Wortelkamp, S., Sickmann, A., Zahedi, R. P., Systematic and quantitative comparison of digest efficiency and specificity reveals the impact of trypsin quality on MS-based proteomics. J. Proteomics 2012, 75, 1454–1462.
60. Larsen, M. R., Graham, M. E., Robinson, P. J., Roepstorff, P., Improved detection of hydrophilic phosphopeptides using graphite powder microcolumns and mass spectrometry evidence for in vivo doubly phosphorylated dynamin I and dynamin III. Mol. Cell. Proteomics 2004, 3, 456–465.
61. 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.
62. Thingholm, T. E., Palmisano, G., Kjeldsen, F., Larsen, M. R., Undesirable charge-enhancement of isobaric tagged phosphopeptides leads to reduced identification efficiency. J. Proteome Res. 2010, 9, 4045–4052.
63. Vögtle, F. N., Wortelkamp, S., Zahedi, R. P., Becker, D. et al., Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 2009, 139, 428–439.
64. Karp, N. A., Huber, W., Sadowski, P. G., Charles, P. D. et al., Addressing accuracy and precision issues in iTRAQ quantitation. Mol. Cell. Proteomics 2010, 9, 1885–1897.
65. Vaudel, M., Burkhart, J. M., Radau, S., Zahedi, R. P. et al., Integral quantification accuracy estimation for reporter ion-based quantitative proteomics (iQuARI). J. Proteome Res. 2012, 11, 5074–5080.
66. Ting, L., Rad, R., Gygi, S. P., Haas, W., MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat. Methods 2011, 8, 937–940.
67. Wuhr, M., Haas, W., McAlister, G. C., Peshkin, L. et al., Accurate multiplexed proteomics at the MS2 level using the complement reporter ion cluster. Anal. Chem. 2012, 84, 9214–9221.
68. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J., Gevaert, K., Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 2009, 6, 786–787.
69. Berger, A., Schechter, I., Mapping the active site of papain with the aid of peptide substrates and inhibitors. Philos. Trans. R Soc. Lond. 1970, 257, 249–264.
70. Schmidt, O., Pfanner, N., Meisinger, C., Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mole. Cell Biol. 2010, 11, 655–667.
71. Vögtle, F.-N., Prinz, C., Kellermann, J., Lottspeich, F. et al., Mitochondrial protein turnover: role of the precursor intermediate peptidase Oct1 in protein stabilization. Mol. Biol. Cell 2011, 22, 2135–2143.
72. Apel, W., Schulze, W. X., Bock, R., Identification of protein stability determinants in chloroplasts. Plant J. 2010, 63, 636–650.
73. Tsiatsiani, L., Timmerman, E., De Bock, P. J., Vercammen, D. et al., The Arabidopsis metacaspase9 degradome. Plant Cell 2013, 25, 2831–2847.
74. Tanz, S. K., Castleden, I., Hooper, C. M., Vacher, M. et al., SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res. 2013, 41 (Database issue), D1185–D1191.
75. Dougan, D. A., Truscott, K. N., Zeth, K., The bacterial N-end rule pathway: expect the unexpected. Mol. Microbiol. 2010, 76, 545–558.
76. Vizcaíno, J. A., Côté, R. G., Csordas, A., Dianes, J. A. et al., The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 2013, 41, D1063–D1069.