Protease cleavage site fingerprinting by label-free in-gel degradomics reveals pH-dependent specificity switch of legumain

EMBO Journal

Volumn 36, Issue 16, 2017, Pages 2455-2465

  Vidmar, Robert ^a   Vizovišek, Matej ^a   Turk, Dušan ^a,b   Turk, Boris ^a,b,c   Fonović, Marko ^a,b  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

caspase; legumain; protease; proteomics; specificity profiling

Indexed keywords

CYSTEINE PROTEINASE; LEGUMAIN;

ELECTROPHORESIS; ENZYME SPECIFICITY; MASS SPECTROMETRY; METABOLISM; PH; PROCEDURES; PROTEOMICS; TEMPERATURE;

CYSTEINE ENDOPEPTIDASES; ELECTROPHORESIS; HYDROGEN-ION CONCENTRATION; MASS SPECTROMETRY; PROTEOMICS; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 85027545284     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201796750     Document Type: Article

References (49)

1. Agard NJ, Mahrus S, Trinidad JC, Lynn A, Burlingame AL, Wells JA (2012) Global kinetic analysis of proteolysis via quantitative targeted proteomics. Proc Natl Acad Sci USA 109: 1913–1918
2. Biniossek ML, Nagler DK, Becker-Pauly C, Schilling O (2011) Proteomic identification of protease cleavage sites characterizes prime and non-prime specificity of cysteine cathepsins B, L, and S. J Proteome Res 10: 5363–5373
3. Bromme D, Nallaseth FS, Turk B (2004) Production and activation of recombinant papain-like cysteine proteases. Methods 32: 199–206
4. Choe Y, Leonetti F, Greenbaum DC, Lecaille F, Bogyo M, Bromme D, Ellman JA, Craik CS (2006) Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J Biol Chem 281: 12824–12832
5. Coffey A, van den Burg B, Veltman R, Abee T (2000) Characteristics of the biologically active 35-kDa metalloprotease virulence factor from Listeria monocytogenes. J Appl Microbiol 88: 132–141
6. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K (2009) Improved visualization of protein consensus sequences by iceLogo. Nat Methods 6: 786–787
7. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367–1372
8. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794–1805
9. Crawford ED, Seaman JE, Agard N, Hsu GW, Julien O, Mahrus S, Nguyen H, Shimbo K, Yoshihara HA, Zhuang M, Chalkley RJ, Wells JA (2013) The DegraBase: a database of proteolysis in healthy and apoptotic human cells. Mol Cell Proteomics 12: 813–824
10. Dall E, Brandstetter H (2012) Activation of legumain involves proteolytic and conformational events, resulting in a context- and substrate-dependent activity profile. Acta Crystallogr Sect F Struct Biol Cryst Commun 68: 24–31
11. Doucet A, Kleifeld O, Kizhakkedathu JN, Overall CM (2011) Identification of proteolytic products and natural protein N-termini by Terminal Amine Isotopic Labeling of Substrates (TAILS). Methods Mol Biol 753: 273–287
12. Eckhard U, Huesgen PF, Schilling O, Bellac CL, Butler GS, Cox JH, Dufour A, Goebeler V, Kappelhoff R, Keller UA, Klein T, Lange PF, Marino G, Morrison CJ, Prudova A, Rodriguez D, Starr AE, Wang Y, Overall CM (2016) Active site specificity profiling of the matrix metalloproteinase family: proteomic identification of 4300 cleavage sites by nine MMPs explored with structural and synthetic peptide cleavage analyses. Matrix Biol 49: 37–60
13. Gevaert K, Goethals M, Martens L, Van Damme J, Staes A, Thomas GR, Vandekerckhove J (2003) Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nat Biotechnol 21: 566–569
14. Jakoby T, van den Berg BH, Tholey A (2012) Quantitative protease cleavage site profiling using tandem-mass-tag labeling and LC-MALDI-TOF/TOF MS/MS analysis. J Proteome Res 11: 1812–1820
15. Johnson GD, Jiang W (2005) Characterization of cathepsin L secreted by Sf21 insect cells. Arch Biochem Biophys 444: 7–14
16. Kasperkiewicz P, Gajda AD, Drag M (2012) Current and prospective applications of non-proteinogenic amino acids in profiling of proteases substrate specificity. Biol Chem 393: 843–851
17. Kleifeld O, Doucet A, Auf dem Keller U, Prudova A, Schilling O, Kainthan RK, Starr AE, Foster LJ, Kizhakkedathu JN, Overall CM (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat Biotechnol 28: 281–288
18. Lopez-Otin C, Bond JS (2008) Proteases: multifunctional enzymes in life and disease. J Biol Chem 283: 30433–30437
19. Mahrus S, Trinidad JC, Barkan DT, Sali A, Burlingame AL, Wells JA (2008) Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell 134: 866–876
20. Mihelic M, Dobersek A, Guncar G, Turk D (2008) Inhibitory fragment from the p41 form of invariant chain can regulate activity of cysteine cathepsins in antigen presentation. J Biol Chem 283: 14453–14460
21. O'Donoghue AJ, Eroy-Reveles AA, Knudsen GM, Ingram J, Zhou M, Statnekov JB, Greninger AL, Hostetter DR, Qu G, Maltby DA, Anderson MO, Derisi JL, McKerrow JH, Burlingame AL, Craik CS (2012) Global identification of peptidase specificity by multiplex substrate profiling. Nat Methods 9: 1095–1100
22. Olsen JV, Ong SE, Mann M (2004) Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol Cell Proteomics 3: 608–614
23. Poreba M, Szalek A, Kasperkiewicz P, Drag M (2014) Positional scanning substrate combinatorial library (PS-SCL) approach to define caspase substrate specificity. Methods Mol Biol 1133: 41–59
24. Poreba M, Solberg R, Rut W, Lunde NN, Kasperkiewicz P, Snipas SJ, Mihelic M, Turk D, Turk B, Salvesen GS, Drag M (2016) Counter selection substrate library strategy for developing specific protease substrates and probes. Cell Chem Biol 23: 1023–1035
25. Rawlings ND, Waller M, Barrett AJ, Bateman A (2014) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 42: D503–D509
26. Rawlings ND, Barrett AJ, Finn R (2016) Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 44: D343–D350
27. Rodriguez J, Gupta N, Smith RD, Pevzner PA (2008) Does trypsin cut before proline? J Proteome Res 7: 300–305
28. Sanman LE, Bogyo M (2014) Activity-based profiling of proteases. Annu Rev Biochem 83: 249–273
29. Schilling O, Overall CM (2008) Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat Biotechnol 26: 685–694
30. Seaman JE, Julien O, Lee PS, Rettenmaier TJ, Thomsen ND, Wells JA (2016) Cacidases: caspases can cleave after aspartate, glutamate and phosphoserine residues. Cell Death Differ 23: 1717–1726
31. Shahinian H, Tholen S, Schilling O (2013) Proteomic identification of protease cleavage sites: cell-biological and biomedical applications. Expert Rev Proteomics 10: 421–433
32. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850–858
33. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856–2860
34. Steen H, Mann M (2004) The ABC's (and XYZ's) of peptide sequencing. Nat Rev Mol Cell Biol 5: 699–711
35. Stennicke HR, Salvesen GS (1997) Biochemical characteristics of caspases-3, -6, -7, and -8. J Biol Chem 272: 25719–25723
36. Stennicke HR, Renatus M, Meldal M, Salvesen GS (2000) Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8. Biochem J 350(Pt 2): 563–568
37. Sukuru SC, Nigsch F, Quancard J, Renatus M, Chopra R, Brooijmans N, Mikhailov D, Deng Z, Cornett A, Jenkins JL, Hommel U, Davies JW, Glick M (2010) A lead discovery strategy driven by a comprehensive analysis of proteases in the peptide substrate space. Protein Sci 19: 2096–2109
38. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, Ghayur T, Brady KD, Wong WW (1997) Substrate specificities of caspase family proteases. J Biol Chem 272: 9677–9682
39. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW (1997) A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 272: 17907–17911
40. Timmer JC, Zhu W, Pop C, Regan T, Snipas SJ, Eroshkin AM, Riedl SJ, Salvesen GS (2009) Structural and kinetic determinants of protease substrates. Nat Struct Mol Biol 16: 1101–1108
41. Turk D, Guncar G, Podobnik M, Turk B (1998) Revised definition of substrate binding sites of papain-like cysteine proteases. Biol Chem 379: 137–147
42. Turk B (2006) Targeting proteases: successes, failures and future prospects. Nat Rev Drug Discovery 5: 785–799
43. Turk B, Turk D, Turk V (2012a) Protease signalling: the cutting edge. EMBO J 31: 1630–1643
44. Turk V, Stoka V, Vasiljeva O, Renko M, Sun T, Turk B, Turk D (2012b) Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochem Biophys Acta 1824: 68–88
45. Van Damme P, Van Damme J, Demol H, Staes A, Vandekerckhove J, Gevaert K (2009) A review of COFRADIC techniques targeting protein N-terminal acetylation. BMC Proc 3(Suppl 6): S6
46. Venne AS, Solari FA, Faden F, Paretti T, Dissmeyer N, Zahedi RP (2015) An improved workflow for quantitative N-terminal charge-based fractional diagonal chromatography (ChaFRADIC) to study proteolytic events in Arabidopsis thaliana. Proteomics 15: 2458–2469
47. Vizovisek M, Vidmar R, Van Quickelberghe E, Impens F, Andjelkovic U, Sobotic B, Stoka V, Gevaert K, Turk B, Fonovic M (2015) Fast profiling of protease specificity reveals similar substrate specificities for cathepsins K, L and S. Proteomics 15: 2479–2490
48. Vizovisek M, Vidmar R, Fonovic M, Turk B (2016) Current trends and challenges in proteomic identification of protease substrates. Biochimie 122: 77–87
49. Wejda M, Impens F, Takahashi N, Van Damme P, Gevaert K, Vandenabeele P (2012) Degradomics reveals that cleavage specificity profiles of caspase-2 and effector caspases are alike. J Biol Chem 287: 33983–33995