LC-MS based cleavage site profiling of the proteases ADAM10 and ADAM17 using proteome-derived peptide libraries

Journal of Proteome Research

Volumn 13, Issue 4, 2014, Pages 2205-2214

  Tucher, Joanna ^a   Linke, Dennis ^a   Koudelka, Tomas ^a   Cassidy, Liam ^a   Tredup, Claudia ^a   Wichert, Rielana ^a   Pietrzik, Claus ^b   Becker Pauly, Christoph ^a   Tholey, Andreas ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

ADAM10; ADAM17; cleavage site specificity; ESI MS; MALDI MS; peptide library; PICS; Q PICS; TMT

Indexed keywords

ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; ADAM17 PROTEIN; AROMATIC AMINO ACID; UNCLASSIFIED DRUG; ADAM10 PROTEIN, MOUSE; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PEPTIDE LIBRARY; PROTEOME; SECRETASE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY MASS SPECTROMETRY; MASS SPECTROMETRY; NONHUMAN; PEPTIDE LIBRARY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PROTEOMICS; SACCHAROMYCES CEREVISIAE; ANIMAL; CHEMISTRY; HUMAN; LIQUID CHROMATOGRAPHY; METABOLISM; MOUSE; PROCEDURES;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CHROMATOGRAPHY, LIQUID; HUMANS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; PEPTIDE FRAGMENTS; PEPTIDE LIBRARY; PROTEOME; PROTEOMICS;

EID: 84898715213     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401135u     Document Type: Article

References (36)

1. Brou, C.; Logeat, F.; Gupta, N.; Bessia, C.; LeBail, O.; Doedens, J. R.; Cumano, A.; Roux, P.; Black, R. A.; Israel, A. A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE Mol. Cell 2000, 5, 207-216
2. Hartmann, D.; de Strooper, B.; Serneels, L.; Craessaerts, K.; Herreman, A.; Annaert, W.; Umans, L.; Lubke, T.; Lena Illert, A.; von Figura, K.; Saftig, P. The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts Hum. Mol. Genet. 2002, 11, 2615-2624
3. Sahin, U.; Weskamp, G.; Kelly, K.; Zhou, H. M.; Higashiyama, S.; Peschon, J.; Hartmann, D.; Saftig, P.; Blobel, C. P. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands J. Cell Biol. 2004, 164, 769-779
4. Pruessmeyer, J.; Ludwig, A. The good, the bad and the ugly substrates for ADAM10 and ADAM17 in brain pathology, inflammation and cancer Semin. Cell Dev. Biol. 2009, 20, 164-174
5. Saftig, P.; Reiss, K. The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: novel drug targets with therapeutic potential? Eur. J. Cell Biol. 2011, 90, 527-535
6. Becker-Pauly, C.; Rose-John, S. TNFalpha cleavage beyond TACE/ADAM17: matrix metalloproteinase 13 is a potential therapeutic target in sepsis and colitis EMBO Mol. Med. 2013, 5, 902-904
7. Rawlings, N. D.; Barrett, A. J.; Bateman, A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors Nucleic Acids Res. 2012, 40, D343-D350
8. Lambert, M. H.; Blackburn, R. K.; Seaton, T. D.; Kassel, D. B.; Kinder, D. S.; Leesnitzer, M. A.; Bickett, D. M.; Warner, J. R.; Andersen, M. W.; Badiang, J. G.; Cowan, D. J.; Gaul, M. D.; Petrov, K. G.; Rabinowitz, M. H.; Wiethe, R. W.; Becherer, J. D.; McDougald, D. L.; Musso, D. L.; Andrews, R. C.; Moss, M. L. Substrate specificity and novel selective inhibitors of TNF-alpha converting enzyme (TACE) from two-dimensional substrate mapping Comb. Chem. High Throughput Screening 2005, 8, 327-339
9. Mohan, M. J.; Seaton, T.; Mitchell, J.; Howe, A.; Blackburn, K.; Burkhart, W.; Moyer, M.; Patel, I.; Waitt, G. M.; Becherer, J. D.; Moss, M. L.; Milla, M. E. The tumor necrosis factor-alpha converting enzyme (TACE): a unique metalloproteinase with highly defined substrate selectivity Biochemistry 2002, 41, 9462-9469
10. Jin, G.; Huang, X.; Black, R.; Wolfson, M.; Rauch, C.; McGregor, H.; Ellestad, G.; Cowling, R. A continuous fluorimetric assay for tumor necrosis factor-alpha converting enzyme Anal. Biochem. 2002, 302, 269-275
11. Caescu, C. I.; Jeschke, G. R.; Turk, B. E. Active-site determinants of substrate recognition by the metalloproteinases TACE and ADAM10 Biochem. J. 2009, 424, 79-88
12. Jakoby, T.; van den Berg, B. H.; Tholey, A. Quantitative protease cleavage site profiling using tandem-mass-tag labeling and LC-MALDI-TOF/TOF MS/MS analysis J. Proteome Res. 2012, 11, 1812-1820
13. Schilling, O.; Overall, C. M. Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites Nat. Biotechnol. 2008, 26, 685-694
14. Jefferson, T.; Auf dem Keller, U.; Bellac, C.; Metz, V. V.; Broder, C.; Hedrich, J.; Ohler, A.; Maier, W.; Magdolen, V.; Sterchi, E.; Bond, J. S.; Jayakumar, A.; Traupe, H.; Chalaris, A.; Rose-John, S.; Pietrzik, C. U.; Postina, R.; Overall, C. M.; Becker-Pauly, C. The substrate degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin beta and ADAM10 Cell. Mol. Life Sci. 2013, 70, 309-333
15. Becker, C.; Kruse, M. N.; Slotty, K. A.; Kohler, D.; Harris, J. R.; Rosmann, S.; Sterchi, E. E.; Stocker, W. Differences in the activation mechanism between the alpha and beta subunits of human meprin Biol. Chem. 2003, 384, 825-831
16. Colaert, N.; Helsens, K.; Martens, L.; Vandekerckhove, J.; Gevaert, K. Improved visualization of protein consensus sequences by iceLogo Nat. Methods 2009, 6, 786-787
17. Tan, H. T.; Tan, S.; Lin, Q.; Lim, T. K.; Hew, C. L.; Chung, M. C. Quantitative and temporal proteome analysis of butyrate-treated colorectal cancer cells Mol. Cell. Proteomics 2008, 7, 1174-1185
18. Schechter, I.; Berger, A. On the size of the active site in proteases. I. Papain Biochem. Biophys. Res. Commun. 1967, 27, 157-162
19. Schilling, O.; Huesgen, P. F.; Barre, O.; Auf dem Keller, U.; Overall, C. M. Characterization of the prime and non-prime active site specificities of proteases by proteome-derived peptide libraries and tandem mass spectrometry Nat. Protoc. 2011, 6, 111-120
20. Becker-Pauly, C.; Barre, O.; Schilling, O.; Auf dem Keller, U.; Ohler, A.; Broder, C.; Schutte, A.; Kappelhoff, R.; Stocker, W.; Overall, C. M. Proteomic analyses reveal an acidic prime side specificity for the astacin metalloprotease family reflected by physiological substrates Mol. Cell. Proteomics 2011, 10, M111 009233
21. Jekel, P. A.; Weijer, W. J.; Beintema, J. J. Use of endoproteinase Lys-C from Lysobacter enzymogenes in protein sequence analysis Anal. Biochem. 1983, 134, 347-354
22. Sorensen, S. B.; Sorensen, T. L.; Breddam, K. Fragmentation of proteins by S. aureus strain V8 protease. Ammonium bicarbonate strongly inhibits the enzyme but does not improve the selectivity for glutamic acid FEBS Lett. 1991, 294, 195-197
23. Leonard, J. D.; Lin, F.; Milla, M. E. Chaperone-like properties of the prodomain of TNFalpha-converting enzyme (TACE) and the functional role of its cysteine switch Biochem. J. 2005, 387, 797-805
24. Suh, J.; Choi, S. H.; Romano, D. M.; Gannon, M. A.; Lesinski, A. N.; Kim, D. Y.; Tanzi, R. E. ADAM10 missense mutations potentiate beta-amyloid accumulation by impairing prodomain chaperone function Neuron 2013, 80, 385-401
25. Schwarz, J.; Broder, C.; Helmstetter, A.; Schmidt, S.; Yan, I.; Müller, M.; Schmidt-Arras, D.; Becker-Pauly, C.; Koch-Nolte, F.; Mittrücker, H.; Rabe, B.; Rose-John, S.; Chalaris, A. Short-term TNFα shedding is independent of cytoplasmic phosphorylation or furin cleavage of ADAM17 Biochim. Biophys. Acta 2013, 1833, 3355-3367
26. Lammich, S.; Kojro, E.; Postina, R.; Gilbert, S.; Pfeiffer, R.; Jasionowski, M.; Haass, C.; Fahrenholz, F. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3922-3977
27. Hikita, A.; Yana, I.; Wakeyama, H.; Nakamura, M.; Kadono, Y.; Oshima, Y.; Nakamura, K.; Seiki, M.; Tanaka, S. Negative regulation of osteoclastogenesis by ectodomain shedding of receptor activator of NF-kappaB ligand J. Biol. Chem. 2006, 281, 36846-36855
28. Mullberg, J.; Oberthur, W.; Lottspeich, F.; Mehl, E.; Dittrich, E.; Graeve, L.; Heinrich, P. C.; Rose-John, S. The soluble human IL-6 receptor. Mutational characterization of the proteolytic cleavage site J. Immunol. 1994, 152, 4958-4968
29. Rafiq, S.; Frayling, T. M.; Murray, A.; Hurst, A.; Stevens, K.; Weedon, M. N.; Henley, W.; Ferrucci, L.; Bandinelli, S.; Corsi, A. M.; Guralnik, J. M.; Melzer, D. A common variant of the interleukin 6 receptor (IL-6r) gene increases IL-6r and IL-6 levels, without other inflammatory effects Genes Immun. 2007, 8, 552-559
30. Dolnik, O.; Volchkova, V.; Garten, W.; Carbonnelle, C.; Becker, S.; Kahnt, J.; Stroher, U.; Klenk, H. D.; Volchkov, V. Ectodomain shedding of the glycoprotein GP of Ebola virus EMBO J. 2004, 23, 2175-2184
31. Marino, G.; Huesgen, P. F.; Eckhard, U.; Overall, C. M.; Schroder, W. P.; Funk, C. Family-wide characterization of Matrix Metallo-proteinases from Arabidopsis thaliana reveals their distinct proteolytic activity and cleavage site specificity Biochem. J. 2013, 457, 335-346
32. Nesatyy, V. J.; Groh, K.; Nestler, H.; Suter, M. J. On the acquisition of +1 charge states during high-throughput proteomics: Implications on reproducibility, number and confidence of protein identifications J Proteomics 2009, 72, 761-770
33. Biniossek, M. L.; Schilling, O. Enhanced identification of peptides lacking basic residues by LC-ESI-MS/MS analysis of singly charged peptides Proteomics 2012, 12, 1303-1309
34. Lasaosa, M.; Delmotte, N.; Huber, C. G.; Melchior, K.; Heinzle, E.; Tholey, A. A 2D reversed-phase x ion-pair reversed-phase HPLC-MALDI TOF/TOF-MS approach for shotgun proteome analysis Anal. Bioanal. Chem. 2009, 393, 1245-1256
35. Rietschel, B.; Baeumlisberger, D.; Arrey, T. N.; Bornemann, S.; Rohmer, M.; Schuerken, M.; Karas, M.; Meyer, B. The benefit of combining nLC-MALDI-Orbitrap MS data with nLC-MALDI-TOF/TOF data for proteomic analyses employing elastase J. Proteome Res. 2009, 8, 5317-5324
36. Maretzky, T.; Reiss, K.; Ludwig, A.; Buchholz, J.; Scholz, F.; Proksch, E.; de Strooper, B.; Hartmann, D.; Saftig, P. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 9182-9187