Global identification of peptidase specificity by multiplex substrate profiling

Nature Methods

Volumn 9, Issue 11, 2012, Pages 1095-1100

  O'Donoghue, Anthony J ^a   Alegra Eroy Reveles, A A ^a,b   Knudsen, Giselle M ^a   Ingram, Jessica ^a   Zhou, Min ^a   Statnekov, Jacob B ^a   Greninger, Alexander L ^a   Hostetter, Daniel R ^a   Qu, Gang ^c   Maltby, David A ^a   Anderson, Marc O ^b   Derisi, Joseph L ^a   McKerrow, James H ^a   Burlingame, Alma L ^a   Craik, Charles S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPEPTIDASE; GRANZYME B; KLASSEVIRUS 3C PROTEIN; PEPTIDASE; TETRADECAPEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MULTIPLEX SUBSTRATE PROFILING; NONHUMAN; PANCREAS CANCER; PEPTIDE LIBRARY; PHYSICAL CHEMISTRY; PLATYHELMINTH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; TURNOVER TIME;

ANIMALS; CARBOXYPEPTIDASES; CARCINOMA, PANCREATIC DUCTAL; CATHEPSIN E; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; CYSTEINE ENDOPEPTIDASES; EXOPEPTIDASES; GRANZYMES; HUMANS; MICE; PANCREATIC ELASTASE; PEPTIDE HYDROLASES; PEPTIDE LIBRARY; PEPTIDES; SCHISTOSOMA MANSONI; SUBSTRATE SPECIFICITY; TANDEM MASS SPECTROMETRY; VIRAL PROTEINS;

PLATYHELMINTHES; SCHISTOSOMA;

EID: 84869088814     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2182     Document Type: Article

References (39)

1. Puente, X.S., Gutiérrez-Fernández, A., Velasco, G. & López-Otín, C. A genomic view of the complexity of mammalian proteolytic systems. Biochem. Soc. Trans. 33, 331-334 (2005). (Pubitemid 40604365)
2. Van Damme, P., Vandekerckhove, J. & Gevaert, K. Disentanglement of protease substrate repertoires. Biol. Chem. 389, 371-381 (2008). (Pubitemid 351773913)
3. Matthews, D.J. & Wells, J.A. Substrate phage: selection of protease substrates by monovalent phage display. Science 260, 1113-1117 (1993). (Pubitemid 23186784)
4. Boulware, K.T. & Daugherty, P.S. Protease specificity determination by using cellular libraries of peptide substrates (CLiPS). Proc. Natl. Acad. Sci. USA 103, 7583-7588 (2006).
5. Turk, B.E., Huang, L.L., Piro, E.T. & Cantley, L.C. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat. Biotechnol. 19, 661-667 (2001). (Pubitemid 32625438)
6. Harris, J.L. et al. Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proc. Natl. Acad. Sci. USA 97, 7754-7759 (2000). (Pubitemid 30460720)
7. Choe, Y. et al. Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem. 281, 12824-12832 (2006). (Pubitemid 43855375)
8. auf dem Keller, U. & Schilling, O. Proteomic techniques and activity-based probes for the system-wide study of proteolysis. Biochimie 92, 1705-1714 (2010).
9. Mahrus, S. et al. Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134, 866-876 (2008).
10. Staes, A. et al. Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 8, 1362-1370 (2008). (Pubitemid 351518548)
11. Impens, F. et al. A quantitative proteomics design for systematic identification of protease cleavage events. Mol. Cell. Proteomics 9, 2327-2333 (2010).
12. Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J. & Gevaert, K. Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6, 786-787 (2009).
13. Chajkowski, S.M. et al. Highly selective hydrolysis of kinins by recombinant prolylcarboxypeptidase. Biochem. Biophys. Res. Commun. 405, 338-343 (2011).
14. Sun, J. et al. Importance of the P4′ residue in human granzyme B inhibitors and substrates revealed by scanning mutagenesis of the proteinase inhibitor 9 reactive center loop. J. Biol. Chem. 276, 15177-15184 (2001).
15. Cordingley, M.G., Callahan, P.L., Sardana, V.V., Garsky, V.M. & Colonno, R.J. Substrate requirements of human rhinovirus 3C protease for peptide cleavage in vitro. J. Biol. Chem. 265, 9062-9065 (1990).
16. Sojka, D. et al. Characterization of gut-associated cathepsin D hemoglobinase from tick Ixodes ricinus (IrCD1). J. Biol. Chem. 287, 21152-21163 (2012).
17. Ingram, J.R. et al. Investigation of the proteolytic functions of an expanded cercarial elastase gene family in Schistosoma mansoni. PLoS Negl. Trop. Dis. 6, e1589 (2012).
18. Knudsen, G.M., Medzihradszky, K.F., Lim, K.-C., Hansell, E. & McKerrow, J.H. Proteomic analysis of Schistosoma mansoni cercarial secretions. Mol. Cell. Proteomics 4, 1862-1875 (2005). (Pubitemid 41830181)
19. Curwen, R.S., Ashton, P.D., Sundaralingam, S. & Wilson, R.A. Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol. Cell. Proteomics 5, 835-844 (2006). (Pubitemid 43792793)
20. Nolan-Stevaux, O. et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev. 23, 24-36 (2009).
21. Fricker, L. Carboxypeptidase E. in Handbook of Proteolytic Enzymes 2nd edn. (eds. Barrett, A.J., Rawlings, N.D. & Woessner, J.F.) 840-844 (Academic, 2004).
22. Caglic, D. et al. Murine and human cathepsin B exhibit similar properties: possible implications for drug discovery. Biol. Chem. 390, 175-179 (2009).
23. Mason, R.W., Johnson, D.A., Barrett, A.J. & Chapman, H.A. Elastinolytic activity of human cathepsin L. Biochem. J. 233, 925-927 (1986). (Pubitemid 16116171)
24. Zaidi, N., Herrmann, T., Voelter, W. & Kalbacher, H. Recombinant cathepsin E has no proteolytic activity at neutral pH. Biochem. Biophys. Res. Commun. 360, 51-55 (2007). (Pubitemid 46990322)
25. Impens, F. et al. MS-driven protease substrate degradomics. Proteomics 10, 1284-1296 (2010).
26. Rawlings, N.D., Barrett, A.J. & Bateman, A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 40, D343-D350 (2012).
27. Ruggles, S.W., Fletterick, R.J. & Craik, C.S. Characterization of structural determinants of granzyme B reveals potent mediators of extended substrate specificity. J. Biol. Chem. 279, 30751-30759 (2004). (Pubitemid 38938008)
28. Prudova, A., Auf dem Keller, U., Butler, G.S. & Overall, C.M. Multiplex N-terminome analysis of MMP-2 and MMP-9 substrate degradomes by iTRAQ-TAILS quantitative proteomics. Mol. Cell. Proteomics 9, 894-911 (2010).
29. Zhou, C. et al. Design and synthesis of prolylcarboxypeptidase (PrCP) inhibitors to validate PrCP as a potential target for obesity. J. Med. Chem. 53, 7251-7263 (2010).
30. Cohen, F.E. et al. Arresting tissue invasion of a parasite by protease inhibitors chosen with the aid of computer modeling. Biochemistry 30, 11221-11229 (1991).
31. Cruz-Monserrate, Z. et al. Detection of pancreatic cancer tumours and precursor lesions by cathepsin E activity in mouse models. Gut 61, 1315-1322 (2012).
32. Barkan, D.T. et al. Prediction of protease substrates using sequence and structure features. Bioinformatics 26, 1714-1722 (2010).
33. Harris, J.L., Peterson, E.P., Hudig, D., Thornberry, N.A. & Craik, C.S. Definition and redesign of the extended substrate specificity of granzyme B. J. Biol. Chem. 273, 27364-27373 (1998). (Pubitemid 28500453)
34. Salter, J.P. et al. Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J. Biol. Chem. 277, 24618-24624 (2002). (Pubitemid 34951990)
35. Chalkley, R.J., Baker, P.R., Medzihradszky, K.F., Lynn, A.J. & Burlingame, A.L. In-depth analysis of tandem mass spectrometry data from disparate instrument types. Mol. Cell. Proteomics 7, 2386-2398 (2008).
36. Elias, J.E. & Gygi, S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214 (2007). (Pubitemid 46358868)
37. Liu, H., Sadygov, R.G. & Yates, J.R. III. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193-4201 (2004). (Pubitemid 38943698)
38. Choi, H., Fermin, D. & Nesvizhskii, A.I. Significance analysis of spectral count data in label-free shotgun proteomics. Mol. Cell. Proteomics 7, 2373-2385 (2008).
39. O'Donoghue, A.J. et al. Inhibition of a secreted glutamic peptidase prevents growth of the fungus Talaromyces emersonii. J. Biol. Chem. 283, 29186-29195 (2008).