Strategies for detection and quantification of cysteine cathepsins-evolution from bench to bedside

Biochimie

Volumn 122, Issue , 2016, Pages 48-61

  Hughes, Caroline S ^a   Burden, Roberta E ^a   Gilmore, Brendan F ^a   Scott, Christopher J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Activity based probe; Affinity binding probe; Cathepsin; Cysteine proteinase; Proteolysis; Quenched substrate

Indexed keywords

ACYLOXYMETHYL KETONE; CATHEPSIN; CATHEPSIN B; CATHEPSIN F; CATHEPSIN H; CATHEPSIN K; CATHEPSIN L; CATHEPSIN O; CATHEPSIN S; CATHEPSIN V; CATHEPSIN W; CATHEPSIN X; CHLOROMETHYL KETONE; CYSTEINE; DIAZOMETHYL KETONE; DIPEPTIDYL PEPTIDASE I; ENZYME INHIBITOR; EPOXIDE; FLUOROMETHYL KETONE; KETONE; NANOPARTICLE; PHOSPHONIC ACID DERIVATIVE; QUANTUM DOT; SULFONE; UNCLASSIFIED DRUG; VINYLSULPHONE; PROTEIN BINDING;

ENZYME ACTIVITY; ENZYME SUBSTRATE; PH; PROTEIN ANALYSIS; PROTEIN BINDING; REVIEW; ANIMAL; ENZYME ASSAY; ENZYME SPECIFICITY; ENZYMOLOGY; HUMAN; METABOLISM; NEOPLASMS; PROCEDURES; PROTEOMICS; TRANSLATIONAL RESEARCH;

ANIMALS; CATHEPSINS; CYSTEINE; ENZYME ASSAYS; HUMANS; NEOPLASMS; PROTEIN BINDING; PROTEOMICS; SUBSTRATE SPECIFICITY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84957851359     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.07.029     Document Type: Review

References (161)

1. I. Schechter, and A. Berger On the size of the active site in proteases. I. Papain Biochem. Biophys. Res. Commun. 27 2 1967 Apr 20 157 162
2. C. Lopez-Otin, and J.S. Bond Proteases: multifunctional enzymes in life and disease J. Biol. Chem. 283 45 2008 Nov 7 30433 30437
3. N.D. Rawlings, F.R. Morton, C.Y. Kok, J. Kong, and A.J. Barrett MEROPS: the peptidase database Nucleic Acids Res. 36 Database issue 2008 Jan D320 D325
4. B. Turk, V. Turk, and D. Turk Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors Biol. Chem. 378 3-4 1997 Mar-Apr 141 150
5. N.M. Hooper Proteases: a primer Essays Biochem. 38 2002 1 8
6. V. Turk, B. Turk, G. Guncar, D. Turk, and J. Kos Lysosomal cathepsins: structure, role in antigen processing and presentation, and cancer Adv. Enzyme Regul. 42 2002 285 303
7. T.Y. Nakagawa, and A.Y. Rudensky The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation Immunol. Rev. 172 1999 Dec 121 129
8. B.D. Gelb, G.P. Shi, H.A. Chapman, and R.J. Desnick Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency Science 273 5279 1996 Aug 30 1236 1238
9. V. Gocheva, W. Zeng, D. Ke, D. Klimstra, T. Reinheckel, C. Peters, and et al. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis Genes Dev. 20 5 2006 Mar 1 543 556
10. P.J. Wolters, and H.A. Chapman Importance of lysosomal cysteine proteases in lung disease Respir. Res. 1 3 2000 170 177
11. S. Guha, and H. Padh Cathepsins: fundamental effectors of endolysosomal proteolysis Indian J. Biochem. Biophys. 45 2 2008 Apr 75 90
12. E. Staun-Ram, and A. Miller Cathepsins (S and B) and their inhibitor cystatin C in immune cells: modulation by interferon-beta and role played in cell migration J. Neuroimmunol. 232 1-2 2011 Mar 200 206
13. R.R. Annand, J.R. Dahlen, C.A. Sprecher, P. De Dreu, D.C. Foster, J.A. Mankovich, and et al. Caspase-1 (interleukin-1beta-converting enzyme) is inhibited by the human serpin analogue proteinase inhibitor 9 Biochem. J. 342 Pt 3 1999 Sep 15 655 665
14. J. Rozman, J. Stojan, R. Kuhelj, V. Turk, and B. Turk Autocatalytic processing of recombinant human procathepsin B is a bimolecular process FEBS Lett. 459 3 1999 Oct 15 358 362
15. B. Turk, D. Turk, and G.S. Salvesen Regulating cysteine protease activity: essential role of protease inhibitors as guardians and regulators Curr. Pharm. Des. 8 18 2002 1623 1637
16. L.E. Edgington, M. Verdoes, and M. Bogyo Functional imaging of proteases: recent advances in the design and application of substrate-based and activity-based probes Curr. Opin. Chem. Biol. 15 6 2011 Dec 798 805
17. C.H. Chuang, K.H. Chuang, H.E. Wang, S.R. Roffler, J.T. Shiea, S.C. Tzou, and et al. In vivo positron emission tomography imaging of protease activity by generation of a hydrophobic product from a noninhibitory protease substrate Clin. Cancer Res. 18 1 2012 Jan 1 238 247
18. J. Neefjes, and N.P. Dantuma Fluorescent probes for proteolysis: tools for drug discovery Nat. Rev. Drug Discov. 3 1 2004 Jan 58 69
19. E.A. Jares-Erijman, and T.M. Jovin FRET imaging Nat. Biotechnol. 21 11 2003 Nov 1387 1395
20. M. Poreba, M. Mihelic, P. Krai, J. Rajkovic, A. Krezel, M. Pawelczak, and et al. Unnatural amino acids increase activity and specificity of synthetic substrates for human and malarial cathepsin C Amino Acids 46 4 2014 Apr 931 943
21. W. Rut, P. Kasperkiewicz, A. Byzia, M. Poreba, K. Groborz, and M. Drag Recent advances and concepts in substrate specificity determination of proteases using tailored libraries of fluorogenic substrates with unnatural amino acids Biol. Chem. 396 4 2015 Apr 329 337
22. N. Lutzner, and H. Kalbacher Quantifying cathepsin S activity in antigen presenting cells using a novel specific substrate J. Biol. Chem. 283 52 2008 Dec 26 36185 36194
23. M. Oliveira, R.J. Torquato, M.F. Alves, M.A. Juliano, D. Bromme, N.M. Barros, and et al. Improvement of cathepsin S detection using a designed FRET peptide based on putative natural substrates Peptides 31 4 2010 Apr 562 567
24. J.O. Link, and S. Zipfel Advances in cathepsin S inhibitor design Curr. Opin. Drug Discov. Dev. 9 4 2006 Jul 471 482
25. A. Watzke, G. Kosec, M. Kindermann, V. Jeske, H.P. Nestler, V. Turk, and et al. Selective activity-based probes for cysteine cathepsins Angew. Chem. Int. Ed. Engl. 47 2 2008 406 409
26. D. Caglic, A. Globisch, M. Kindermann, N.H. Lim, V. Jeske, H.P. Juretschke, and et al. Functional in vivo imaging of cysteine cathepsin activity in murine model of inflammation Bioorg. Med. Chem. 19 3 2011 Feb 1 1055 1061
27. M. Sameni, K. Moin, and B.F. Sloane Imaging proteolysis by living human breast cancer cells Neoplasia 2 6 2000 Nov-Dec 496 504
28. I. Podgorski, B.E. Linebaugh, M. Sameni, C. Jedeszko, S. Bhagat, M.L. Cher, and et al. Bone microenvironment modulates expression and activity of cathepsin B in prostate cancer Neoplasia 7 3 2005 Mar 207 223
29. R.E. Burden, J.A. Gormley, T.J. Jaquin, D.M. Small, D.J. Quinn, S.M. Hegarty, and et al. Antibody-mediated inhibition of cathepsin S blocks colorectal tumor invasion and angiogenesis Clin. Cancer Res. 15 19 2009 Oct 1 6042 6051
30. R.E. Burden, P. Snoddy, R.J. Buick, J.A. Johnston, B. Walker, and C.J. Scott Recombinant cathepsin S propeptide attenuates cell invasion by inhibition of cathepsin L-like proteases in tumor microenvironment Mol. Cancer Ther. 7 3 2008 Mar 538 547
31. M. Sameni, A. Anbalagan, M.B. Olive, K. Moin, R.R. Mattingly, and B.F. Sloane MAME models for 4D live-cell imaging of tumor: microenvironment interactions that impact malignant progression J. Vis. Exp. 60 2012 Feb 17 pii: 3661. doi(60):10.3791/3661
32. H.Y. Hu, S. Gehrig, G. Reither, D. Subramanian, M.A. Mall, O. Plettenburg, and et al. FRET-based and other fluorescent proteinase probes Biotechnol. J. 9 2 2014 Feb 266 281
33. C.H. Tung, U. Mahmood, S. Bredow, and R. Weissleder In vivo imaging of proteolytic enzyme activity using a novel molecular reporter Cancer Res. 60 17 2000 Sep 1 4953 4958
34. C. Bremer, C.H. Tung, and R. Weissleder In vivo molecular target assessment of matrix metalloproteinase inhibition Nat. Med. 7 6 2001 Jun 743 748
35. E. Gounaris, C.H. Tung, C. Restaino, R. Maehr, R. Kohler, J.A. Joyce, and et al. Live imaging of cysteine-cathepsin activity reveals dynamics of focal inflammation, angiogenesis, and polyp growth PLoS One 3 8 2008 Aug 13 e2916
36. K.M. Kozloff, L. Quinti, S. Patntirapong, P.V. Hauschka, C. Tung, R. Weissleder, and et al. Non-invasive optical detection of cathepsin K-mediated fluorescence reveals osteoclast activity in vitro and in vivo Bone 44 2 2009 190 198
37. S.A. Lin, M. Patel, D. Suresch, B. Connolly, B. Bao, K. Groves, and et al. Quantitative longitudinal imaging of vascular inflammation and treatment by ezetimibe in apoE Mice by FMT using new optical imaging biomarkers of cathepsin activity and alpha(v)beta(3) integrin Int. J. Mol. Imag. 2012 2012 189254
38. C. Bremer, C.H. Tung, A. Bogdanov Jr., and R. Weissleder Imaging of differential protease expression in breast cancers for detection of aggressive tumor phenotypes Radiology 222 3 2002 Mar 814 818
39. R. Weissleder, C.H. Tung, U. Mahmood, and A. Bogdanov Jr. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes Nat. Biotechnol. 17 4 1999 Apr 375 378
40. U. Mahmood, C.H. Tung, A. Bogdanov Jr., and R. Weissleder Near-infrared optical imaging of protease activity for tumor detection Radiology 213 3 1999 Dec 866 870
41. J.K. Mito, J.M. Ferrer, B.E. Brigman, C.L. Lee, R.D. Dodd, W.C. Eward, and et al. Intraoperative detection and removal of microscopic residual sarcoma using wide-field imaging Cancer 118 21 2012 Nov 1 5320 5330
42. K.C. Cuneo, J.K. Mito, M.P. Javid, J.M. Ferrer, Y. Kim, W.D. Lee, and et al. Imaging primary mouse sarcomas after radiation therapy using cathepsin-activatable fluorescent imaging agents Int. J. Radiat. Oncol. Biol. Phys. 86 2013 Feb 4 136 142
43. A. Cobos-Correa, J.B. Trojanek, S. Diemer, M.A. Mall, and C. Schultz Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation Nat. Chem. Biol. 5 9 2009 Sep 628 630
44. S. Gehrig, M.A. Mall, and C. Schultz Spatially resolved monitoring of neutrophil elastase activity with ratiometric fluorescent reporters Angew. Chem. Int. Ed. Engl. 51 25 2012 Jun 18 6258 6261
45. H.Y. Hu, D. Vats, M. Vizovisek, L. Kramer, C. Germanier, K.U. Wendt, and et al. In vivo imaging of mouse tumors by a lipidated cathepsin S substrate Angew. Chem. Int. Ed. Engl. 53 29 2014 Jul 14 7669 7673
46. R. Fischer, D. Bachle, M. Fotin-Mleczek, G. Jung, H. Kalbacher, and R. Brock A targeted protease substrate for a quantitative determination of protease activities in the endolysosomal pathway Chembiochem 7 9 2006 Sep 1428 1434
47. T. Jiang, E.S. Olson, Q.T. Nguyen, M. Roy, P.A. Jennings, and R.Y. Tsien Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc. Natl. Acad. Sci. U. S. A. 101 51 2004 Dec 21 17867 17872
48. T.A. Aguilera, E.S. Olson, M.M. Timmers, T. Jiang, and R.Y. Tsien Systemic in vivo distribution of activatable cell penetrating peptides is superior to that of cell penetrating peptides Integr. Biol. (Camb) 1 5-6 2009 Jun 371 381
49. Q.T. Nguyen, E.S. Olson, T.A. Aguilera, T. Jiang, M. Scadeng, L.G. Ellies, and et al. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival Proc. Natl. Acad. Sci. U. S. A. 107 9 2010 Mar 2 4317 4322
50. J.H. Ryu, S.A. Kim, H. Koo, J.Y. Yhee, A. Lee, J.H. Na, and et al. Cathepsin B-sensitive nanoprobe for in vivo tumor diagnosis J. Mater Chem. 21 44 2011 17631 17634
51. E. Petryayeva, W.R. Algar, and I.L. Medintz Quantum dots in bioanalysis: a review of applications across various platforms for fluorescence spectroscopy and imaging Appl. Spectrosc. 67 3 2013 Mar 215 252
52. D.J. Norris, and M.G. Bawendi Measurement and assignment of the size-dependent optical spectrum in CdSe quantum dots Phys. Rev. B Condens Matter 53 24 1996 Jun 15 16338 16346
53. B.R. Knudsen, M.L. Jepsen, and Y.P. Ho Quantum dot-based nanosensors for diagnosis via enzyme activity measurement Expert Rev. Mol. Diagn. 13 4 2013 May 367 375
54. I.L. Medintz, A.R. Clapp, F.M. Brunel, T. Tiefenbrunn, H.T. Uyeda, E.L. Chang, and et al. Proteolytic activity monitored by fluorescence resonance energy transfer through quantum-dot-peptide conjugates Nat. Mater. 5 7 2006 Jul 581 589
55. Y. Zhang, M.K. So, and J. Rao Protease-modulated cellular uptake of quantum dots Nano Lett. 6 9 2006 Sep 1988 1992
56. K. Yang, L. Zhu, L. Nie, X. Sun, L. Cheng, C. Wu, and et al. Visualization of protease activity in vivo using an activatable photo-acoustic imaging probe based on CuS nanoparticles Theranostics 4 2 2014 Jan 2 134 141
57. C. Kim, C. Favazza, and L.V. Wang In vivo photoacoustic tomography of chemicals: high-resolution functional and molecular optical imaging at new depths Chem. Rev. 110 5 2010 May 12 2756 2782
58. L. Li, R.J. Zemp, G. Lungu, G. Stoica, and L.V. Wang Photoacoustic imaging of lacZ gene expression in vivo J. Biomed. Opt. 12 2 2007 Mar-Apr 020504
59. E. Terreno, D.D. Castelli, A. Viale, and S. Aime Challenges for molecular magnetic resonance imaging Chem. Rev. 110 5 2010 May 12 3019 3042
60. M. Haris, A. Singh, I. Mohammed, R. Ittyerah, K. Nath, R.P. Nanga, and et al. In vivo magnetic resonance imaging of tumor protease activity Sci. Rep. 4 2014 Aug 15 6081
61. K. Cai, M. Haris, A. Singh, F. Kogan, J.H. Greenberg, H. Hariharan, and et al. Magnetic resonance imaging of glutamate Nat. Med. 18 2 2012 Jan 22 302 306
62. G. Lalmanach, R. Mayer, C. Serveau, J. Scharfstein, and F. Gauthier Biotin-labelled peptidyl diazomethane inhibitors derived from the substrate-like sequence of cystatin: targeting of the active site of cruzipain, the major cysteine proteinase of Trypanosoma cruzi Biochem. J. 318 Pt 2 1996 Sep 1 395 399
63. G. Blum, G. von Degenfeld, M.J. Merchant, H.M. Blau, and M. Bogyo Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes Nat. Chem. Biol. 3 10 2007 Oct 668 677
64. M. Verdoes, L.E. Edgington, F.A. Scheeren, M. Leyva, G. Blum, K. Weiskopf, and et al. A nonpeptidic cathepsin S activity-based probe for noninvasive optical imaging of tumor-associated macrophages Chem. Biol. 19 5 2012 May 25 619 628
65. G. Blum, S.R. Mullins, K. Keren, M. Fonovic, C. Jedeszko, M.J. Rice, and et al. Dynamic imaging of protease activity with fluorescently quenched activity-based probes Nat. Chem. Biol. 1 4 2005 Sep 203 209
66. E. Schellenberger, F. Rudloff, C. Warmuth, M. Taupitz, B. Hamm, and J. Schnorr Protease-specific nanosensors for magnetic resonance imaging Bioconjug. Chem. 19 12 2008 Dec 2440 2445
67. Q.H. Zheng, X. Fei, T.R. DeGrado, J.Q. Wang, K.L. Stone, T.D. Martinez, and et al. Synthesis, biodistribution and micro-PET imaging of a potential cancer biomarker carbon-11 labeled MMP inhibitor (2R)-2-[[4-(6-fluorohex-1-ynyl)phenyl]sulfonylamino]-3-methylbutyric acid [11C]methyl ester Nucl. Med. Biol. 30 7 2003 Oct 753 760
68. J.C. Powers, J.L. Asgian, O.D. Ekici, and K.E. James Irreversible inhibitors of serine, cysteine, and threonine proteases Chem. Rev. 102 12 2002 Dec 4639 4750
69. M. Fonovic, and M. Bogyo Activity-based probes as a tool for functional proteomic analysis of proteases Expert Rev. Proteom. 5 5 2008 Oct 721 730
70. A.M. Sadaghiani, S.H. Verhelst, and M. Bogyo Tagging and detection strategies for activity-based proteomics Curr. Opin. Chem. Biol. 11 1 2007 Feb 20 28
71. K. Docherty, R.J. Carroll, and D.F. Steiner Conversion of proinsulin to insulin: involvement of a 31,500 molecular weight thiol protease Proc. Natl. Acad. Sci. U. S. A. 79 15 1982 Aug 4613 4617
72. K. Docherty, J.C. Hutton, and D.F. Steiner Cathepsin B-related proteases in the insulin secretory granule J. Biol. Chem. 259 10 1984 May 25 6041 6044
73. K. Docherty, R. Carroll, and D.F. Steiner Identification of a 31,500 molecular weight islet cell protease as cathepsin B Proc. Natl. Acad. Sci. U. S. A. 80 11 1983 Jun 3245 3249
74. J.I. Gordon, H.F. Sims, C. Edelstein, A.M. Scanu, and A.W. Strauss Extracellular processing of proapolipoprotein A-II in Hep G2 cell cultures is mediated by a 54-kDa protease immunologically related to cathepsin B J. Biol. Chem. 260 27 1985 Nov 25 14824 14831
75. A.B. Berger, M.D. Witte, J.B. Denault, A.M. Sadaghiani, K.M. Sexton, G.S. Salvesen, and et al. Identification of early intermediates of caspase activation using selective inhibitors and activity-based probes Mol. Cell 23 4 2006 Aug 509 521
76. F. Uhlmann, D. Wernic, M.A. Poupart, E.V. Koonin, and K. Nasmyth Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast Cell 103 3 2000 Oct 27 375 386
77. H.H. Otto, and T. Schirmeister Cysteine proteases and their inhibitors Chem. Rev. 97 1 1997 Feb 5 133 172
78. C.J. Scott, A. McDowell, S.L. Martin, J.F. Lynas, K. Vandenbroeck, and B. Walker Irreversible inhibition of the bacterial cysteine protease-transpeptidase sortase (SrtA) by substrate-derived affinity labels Biochem. J. 366 Pt 3 2002 Sep 15 953 958
79. B. Walker, B.M. Cullen, G. Kay, I.M. Halliday, A. McGinty, and J. Nelson The synthesis, kinetic characterization and application of a novel biotinylated affinity label for cathepsin B Biochem. J. 283 Pt 2 1992 Apr 15 449 453
80. G.D. Green, and E. Shaw Peptidyl diazomethyl ketones are specific inactivators of thiol proteinases J. Biol. Chem. 256 4 1981 Feb 25 1923 1928
81. B.M. Cullen, I.M. Halliday, G. Kay, J. Nelson, and B. Walker The application of a novel biotinylated affinity label for the detection of a cathepsin B-like precursor produced by breast-tumour cells in culture Biochem. J. 283 Pt 2 1992 Apr 15 461 465
82. A. McGinty, M. Moore, D.W. Halton, and B. Walker Characterization of the cysteine proteinases of the common liver fluke Fasciola hepatica using novel, active-site directed affinity labels Parasitology 106 05 1993 487 493
83. C. Perdereau, E. Godat, M.C. Maurel, E. Hazouard, E. Diot, and G. Lalmanach Cysteine cathepsins in human silicotic bronchoalveolar lavage fluids Biochim. Biophys. Acta 1762 3 2006 Mar 351 356
84. T. Brown Silica exposure, smoking, silicosis and lung cancer - complex interactions Occup. Med. 59 2 2009 March 01 89 95
85. C. Naudin, A. Joulin-Giet, G. Couetdic, P. Plesiat, A. Szymanska, E. Gorna, and et al. Human cysteine cathepsins are not reliable markers of infection by Pseudomonas aeruginosa in cystic fibrosis PLoS One 6 9 2011 e25577
86. M. Kasabova, A. Joulin-Giet, F. Lecaille, B.F. Gilmore, S. Marchand-Adam, A. Saidi, and et al. Regulation of TGF-beta1-driven differentiation of human lung fibroblasts: emerging roles of cathepsin B and cystatin C J. Biol. Chem. 289 23 2014 Jun 6 16239 16251
87. T. Garenne, A. Saidi, B.F. Gilmore, E. Niemiec, V. Roy, L.A. Agrofoglio, and et al. Active site labeling of cysteine cathepsins by a straightforward diazomethylketone probe derived from the N-terminus of human cystatin C Biochem. Biophys. Res. Commun. 460 2 2015 May 1 250 254
88. J.P. Falgueyret, W.C. Black, W. Cromlish, S. Desmarais, S. Lamontagne, C. Mellon, and et al. An activity-based probe for the determination of cysteine cathepsin protease activities in whole cells Anal. Biochem. 335 2 2004 Dec 15 218 227
89. A. Veilleux, W.C. Black, J.Y. Gauthier, C. Mellon, M.D. Percival, P. Tawa, and et al. Probing cathepsin S activity in whole blood by the activity-based probe BIL-DMK: cellular distribution in human leukocyte populations and evidence of diurnal modulation Anal. Biochem. 411 1 2011 Apr 1 43 49
90. A. Borodovsky, B.M. Kessler, R. Casagrande, H.S. Overkleeft, K.D. Wilkinson, and H.L. Ploegh A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14 EMBO J. 20 18 2001 Sep 17 5187 5196
91. H. Ovaa, B.M. Kessler, U. Rolen, P.J. Galardy, H.L. Ploegh, and M.G. Masucci Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells Proc. Natl. Acad. Sci. U. S. A. 101 8 2004 Feb 24 2253 2258
92. M. Bogyo, J.S. McMaster, M. Gaczynska, D. Tortorella, A.L. Goldberg, and H. Ploegh Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors Proc. Natl. Acad. Sci. U. S. A. 94 13 1997 Jun 24 6629 6634
93. M. Bogyo, S. Shin, J.S. McMaster, and H.L. Ploegh Substrate binding and sequence preference of the proteasome revealed by active-site-directed affinity probes Chem. Biol. 5 6 1998 Jun 307 320
94. M.D. Mertens, J. Schmitz, M. Horn, N. Furtmann, J. Bajorath, M. Mares, and et al. A coumarin-labeled vinyl sulfone as tripeptidomimetic activity-based probe for cysteine cathepsins Chembiochem 15 7 2014 May 5 955 959
95. A. Baruch, D. Greenbaum, E.T. Levy, P.A. Nielsen, N.B. Gilula, N.M. Kumar, and et al. Defining a link between gap junction communication, proteolysis, and cataract formation J. Biol. Chem. 276 31 2001 Aug 3 28999 29006
96. D. Greenbaum, K.F. Medzihradszky, A. Burlingame, and M. Bogyo Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools Chem. Biol. 7 8 2000 Aug 569 581
97. M. Bogyo, S. Verhelst, V. Bellingard-Dubouchaud, S. Toba, and D. Greenbaum Selective targeting of lysosomal cysteine proteases with radiolabeled electrophilic substrate analogs Chem. Biol. 7 1 2000 Jan 27 38
98. D. Greenbaum, K.F. Medzihradszky, A. Burlingame, and M. Bogyo Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools Chem. Biol. 7 8 2000 569 581
99. D. Greenbaum, A. Baruch, L. Hayrapetian, Z. Darula, A. Burlingame, K.F. Medzihradszky, and et al. Chemical approaches for functionally probing the proteome Mol. Cell. Proteom. 1 1 2002 Jan 60 68
100. M. Reich, P.F. van Swieten, V. Sommandas, M. Kraus, R. Fischer, E. Weber, and et al. Endocytosis targets exogenous material selectively to cathepsin S in live human dendritic cells, while cell-penetrating peptides mediate nonselective transport to cysteine cathepsins J. Leukoc. Biol. 81 4 2007 Apr 990 1001
101. S. Jordans, S. Jenko-Kokalj, N.M. Kuhl, S. Tedelind, W. Sendt, D. Bromme, and et al. Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiological pH and redox conditions BMC Biochem. 10 2009 Sep 22 23-2091-10-23
102. R.F. Wang, and H.Y. Wang Enhancement of antitumor immunity by prolonging antigen presentation on dendritic cells Nat. Biotechnol. 20 2 2002 Feb 149 154
103. J.A. Joyce, A. Baruch, K. Chehade, N. Meyer-Morse, E. Giraudo, F.Y. Tsai, and et al. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis Cancer Cell 5 5 2004 May 443 453
104. F. Cattaruzza, V. Lyo, E. Jones, D. Pham, J. Hawkins, K. Kirkwood, and et al. Cathepsin S is activated during colitis and causes visceral hyperalgesia by a PAR2-dependent mechanism in mice Gastroenterology 141 5 2011 Nov 1864-74.e1-3
105. G. Blum, G. von Degenfeld, M.J. Merchant, H.M. Blau, and M. Bogyo Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes Nat. Chem. Biol. 3 10 2007 Oct 668 677
106. J.L. Cutter, N.T. Cohen, J. Wang, A.E. Sloan, A.R. Cohen, A. Panneerselvam, and et al. Topical application of activity-based probes for visualization of brain tumor tissue PLoS One 7 3 2012 e33060
107. F. Cattaruzza, V. Lyo, E. Jones, D. Pham, J. Hawkins, K. Kirkwood, and et al. Cathepsin S is activated during colitis and causes visceral hyperalgesia by a PAR2-dependent mechanism in mice Gastroenterology 141 5 2011 Nov 1864-74.e1-3
108. L. Ben-Aderet, E. Merquiol, D. Fahham, A. Kumar, E. Reich, Y. Ben-Nun, and et al. Detecting cathepsin activity in human osteoarthritis via activity-based probes Arthritis Res. Ther. 17 1 2015 Mar 20 69-015-0586-5
109. G.P. Shi, A.C. Webb, K.E. Foster, J.H. Knoll, C.A. Lemere, J.S. Munger, and et al. Human cathepsin S: chromosomal localization, gene structure, and tissue distribution J. Biol. Chem. 269 15 1994 Apr 15 11530 11536
110. S. Conus, and H.U. Simon Cathepsins and their involvement in immune responses Swiss Med. Wkly. 140 2010 Jul 20 w13042
111. T. Flannery, R.S. McConnell, S. McQuaid, G. McGregor, M. Mirakhur, L. Martin, and et al. Detection of cathepsin S cysteine protease in human brain tumour microdialysates in vivo Br. J. Neurosurg. 21 2 2007 Apr 204 209
112. R.A. Mukhtar, O. Nseyo, M.J. Campbell, and L.J. Esserman Tumor-associated macrophages in breast cancer as potential biomarkers for new treatments and diagnostics Expert Rev. Mol. Diagn. 11 1 2011 Jan 91 100
113. K. Oresic Bender, L. Ofori, W.A. van der Linden, E.D. Mock, G.K. Datta, S. Chowdhury, and et al. Design of a highly selective quenched activity-based probe and its application in dual color imaging studies of cathepsin s activity localization J. Am. Chem. Soc. 137 14 2015 Apr 15 4771 4777
114. G. Ren, G. Blum, M. Verdoes, H. Liu, S. Syed, L.E. Edgington, and et al. Non-invasive imaging of cysteine cathepsin activity in solid tumors using a 64Cu-labeled activity-based probe PLoS One 6 11 2011 e28029
115. A.E. Speers, and B.F. Cravatt Profiling enzyme activities in vivo using click chemistry methods Chem. Biol. 11 4 2004 Apr 535 546
116. M.R. Pratt, M.D. Sekedat, K.P. Chiang, and T.W. Muir Direct measurement of cathepsin B activity in the cytosol of apoptotic cells by an activity-based probe Chem. Biol. 16 9 2009 Sep 25 1001 1012
117. H.C. Kolb, M.G. Finn, and K.B. Sharpless Click chemistry: diverse chemical function from a few good reactions Angew. Chem. Int. Ed. Engl. 40 11 2001 Jun 1 2004 2021
118. R. Breinbauer, and M. Kohn Azide-alkyne coupling: a powerful reaction for bioconjugate chemistry Chembiochem 4 11 2003 Nov 7 1147 1149
119. C.D. Hein, X.M. Liu, and D. Wang Click chemistry, a powerful tool for pharmaceutical sciences Pharm. Res. 25 10 2008 Oct 2216 2230
120. A.E. Speers, G.C. Adam, and B.F. Cravatt Activity-based protein profiling in vivo using a copper(i)-catalyzed azide-alkyne [3 + 2] cycloaddition J. Am. Chem. Soc. 125 16 2003 Apr 23 4686 4687
121. M.R. Pratt, M.D. Sekedat, K.P. Chiang, and T.W. Muir Direct measurement of cathepsin B activity in the cytosol of apoptotic cells by an activity-based probe Chem. Biol. 16 9 2009 Sep 25 1001 1012
122. E. Saxon, and C.R. Bertozzi Cell surface engineering by a modified Staudinger reaction Science 287 5460 2000 March 17 2007 2010
123. G. Blum, R.M. Weimer, L.E. Edgington, W. Adams, and M. Bogyo Comparative assessment of substrates and activity based probes as tools for non-invasive optical imaging of cysteine protease activity PLoS One 4 7 2009 Jul 28 e6374
124. R.P. Chen, A. Ren, and S.D. Ye Correlation between serum cathepsin S and insulin resistance in type 2 diabetes Exp. Ther. Med. 6 5 2013 Nov 1237 1242
125. E. Jobs, U. Riserus, E. Ingelsson, J. Sundstrom, M. Jobs, E. Nerpin, and et al. Serum cathepsin S is associated with decreased insulin sensitivity and the development of type 2 diabetes in a community-based cohort of elderly men Diabet. Care 36 1 2013 Jan 163 165
126. J. Liu, L. Ma, J. Yang, A. Ren, Z. Sun, G. Yan, and et al. Increased serum cathepsin S in patients with atherosclerosis and diabetes Atherosclerosis 186 2 2006 Jun 411 419
127. R.D. Wilkinson, R. Williams, C.J. Scott, and R.E. Burden Cathepsin S: therapeutic, diagnostic and prognostic potential Biol. Chem. 396 2015 Apr 15 867 882
128. Y. Qin, Y. Yang, R. Liu, X. Cao, O. Liu, J. Liu, and et al. Combined cathepsin S and hs-CRP predicting inflammation of abdominal aortic aneurysm Clin. Biochem. 46 12 2013 Aug 1026 1029
129. S. Dufort, L. Sancey, C. Wenk, V. Josserand, and J.L. Coll Optical small animal imaging in the drug discovery process Biochim. Biophys. Acta 1798 12 2010 Dec 2266 2273
130. S. Wagner, H.J. Breyholz, C. Holtke, A. Faust, O. Schober, M. Schafers, and et al. A new 18F-labelled derivative of the MMP inhibitor CGS 27023A for PET: radiosynthesis and initial small-animal PET studies Appl. Radiat. Isot. 67 4 2009 Apr 606 610
131. S. Wagner, H.J. Breyholz, M.P. Law, A. Faust, C. Holtke, S. Schroer, and et al. Novel fluorinated derivatives of the broad-spectrum MMP inhibitors N-hydroxy-2(R)-[[(4-methoxyphenyl)sulfonyl](benzyl)- and (3-picolyl)-amino]-3-methyl-butanamide as potential tools for the molecular imaging of activated MMPs with PET J. Med. Chem. 50 23 2007 Nov 15 5752 5764
132. P.E. Huber, J.W. Jenne, R. Rastert, I. Simiantonakis, H.P. Sinn, H.J. Strittmatter, and et al. A new noninvasive approach in breast cancer therapy using magnetic resonance imaging-guided focused ultrasound surgery Cancer Res. 61 23 2001 Dec 1 8441 8447
133. M. Ahmed, L. Solbiati, C.L. Brace, D.J. Breen, M.R. Callstrom, J.W. Charboneau, and et al. Image-guided tumor ablation: standardization of terminology and reporting criteria-a 10-year update Radiology 273 1 2014 Oct 241 260
134. E.S. Olson, T. Jiang, T.A. Aguilera, Q.T. Nguyen, L.G. Ellies, M. Scadeng, and et al. Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and MR imaging of proteases Proc. Natl. Acad. Sci. U. S. A. 107 9 2010 Mar 2 4311 4316
135. R. Ta, M. Suchy, J.H. Tam, A.X. Li, F.S. Martinez-Santiesteban, T.J. Scholl, and et al. A dual magnetic resonance imaging/fluorescent contrast agent for cathepsin-D detection Contrast Media Mol. Imag. 8 2 2013 Mar-Apr 127 139
136. Y. Ikeda, T. Ikata, T. Mishiro, S. Nakano, M. Ikebe, and S. Yasuoka Cathepsins B and L in synovial fluids from patients with rheumatoid arthritis and the effect of cathepsin B on the activation of pro-urokinase J. Med. Invest. 47 1-2 2000 Feb 61 75
137. C.S. Gondi, and J.S. Rao Cathepsin B as a cancer target Expert Opin. Ther. Targets 17 3 2013 Mar 281 291
138. M. Niedergethmann, B. Wostbrock, J.W. Sturm, F. Willeke, S. Post, and R. Hildenbrand Prognostic impact of cysteine proteases cathepsin B and cathepsin L in pancreatic adenocarcinoma Pancreas 29 3 2004 Oct 204 211
139. T.C. Hart, P.S. Hart, M.D. Michalec, Y. Zhang, E. Firatli, T.E. Van Dyke, and et al. Haim-Munk syndrome and Papillon-Lefevre syndrome are allelic mutations in cathepsin C J. Med. Genet. 37 2 2000 Feb 88 94
140. C. Hewitt, D. McCormick, G. Linden, D. Turk, I. Stern, I. Wallace, and et al. The role of cathepsin C in Papillon-Lefevre syndrome, prepubertal periodontitis, and aggressive periodontitis Hum. Mutat. 23 3 2004 Mar 222 228
141. K.R. Smith, H.H. Dahl, L. Canafoglia, E. Andermann, J. Damiano, M. Morbin, and et al. Cathepsin F mutations cause type B Kufs disease, an adult-onset neuronal ceroid lipofuscinosis Hum. Mol. Genet. 22 7 2013 Apr 1 1417 1423
142. I. Santamaria, G. Velasco, A.M. Pendas, A. Paz, and C. Lopez-Otin Molecular cloning and structural and functional characterization of human cathepsin F, a new cysteine proteinase of the papain family with a long propeptide domain J. Biol. Chem. 274 20 1999 May 14 13800 13809
143. V. Gocheva, X. Chen, C. Peters, T. Reinheckel, and J.A. Joyce Deletion of cathepsin H perturbs angiogenic switching, vascularization and growth of tumors in a mouse model of pancreatic islet cell cancer Biol. Chem. 391 8 2010 Aug 937 945
144. M.A. Aldahmesh, A.O. Khan, H. Alkuraya, N. Adly, S. Anazi, A.A. Al-Saleh, and et al. Mutations in LRPAP1 are associated with severe myopia in humans Am. J. Hum. Genet. 93 2 2013 Aug 8 313 320
145. F. Buhling, M. Kouadio, C.E. Chwieralski, U. Kern, J.M. Hohlfeld, N. Klemm, and et al. Gene targeting of the cysteine peptidase cathepsin H impairs lung surfactant in mice PLoS One 6 10 2011 e26247
146. S. Boonen, E. Rosenberg, F. Claessens, D. Vanderschueren, and S. Papapoulos Inhibition of cathepsin K for treatment of osteoporosis Curr. Osteoporos. Rep. 10 1 2012 Mar 73 79
147. M. Skoumal, G. Haberhauer, G. Kolarz, G. Hawa, W. Woloszczuk, and A. Klingler Serum cathepsin K levels of patients with longstanding rheumatoid arthritis: correlation with radiological destruction Arthritis Res. Ther. 7 1 2005 R65 R70
148. J. Liu, G.K. Sukhova, J.T. Yang, J. Sun, L. Ma, A. Ren, and et al. Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells Atherosclerosis 184 2 2006 Feb 302 311
149. J.M. Lankelma, D.M. Voorend, T. Barwari, J. Koetsveld, A.H. Van der Spek, A.P. De Porto, and et al. Cathepsin L, target in cancer treatment? Life Sci. 86 7-8 2010 Feb 13 225 233
150. O. Vasiljeva, T. Reinheckel, C. Peters, D. Turk, V. Turk, and B. Turk Emerging roles of cysteine cathepsins in disease and their potential as drug targets Curr. Pharm. Des. 13 4 2007 387 403
151. I. Santamaria, A.M. Pendas, G. Velasco, and C. Lopez-Otin Genomic structure and chromosomal localization of the human cathepsin O gene (CTSO) Genomics 53 2 1998 Oct 15 231 234
152. A.O. Samokhin, P.A. Lythgo, J.Y. Gauthier, M.D. Percival, and D. Bromme Pharmacological inhibition of cathepsin S decreases atherosclerotic lesions in Apoe-/-mice J. Cardiovasc. Pharmacol. 56 1 2010 Jul 98 105
153. D.M. Small, R.E. Burden, J. Jaworski, S.M. Hegarty, S. Spence, J.F. Burrows, and et al. Cathepsin S from both tumor and tumor-associated cells promote cancer growth and neovascularization Int. J. Cancer 133 9 2013 Nov 2102 2112
154. D. Small, R. Burden, and C. Scott The emerging relevance of the cysteine protease cathepsin S in disease Clin. Rev. Bone Miner. Metab. 9 2 2011 06/01 122 132
155. S. Taleb, and K. Clement Emerging role of cathepsin S in obesity and its associated diseases Clin. Chem. Lab. Med. 45 3 2007 328 332
156. T. Zheng, M.J. Kang, K. Crothers, Z. Zhu, W. Liu, C.G. Lee, and et al. Role of cathepsin S-dependent epithelial cell apoptosis in IFN-gamma-induced alveolar remodeling and pulmonary emphysema J. Immunol. 174 12 2005 Jun 15 8106 8115
157. E. Tolosa, W. Li, Y. Yasuda, W. Wienhold, L.K. Denzin, A. Lautwein, and et al. Cathepsin V is involved in the degradation of invariant chain in human thymus and is overexpressed in myasthenia gravis J. Clin. Invest. 112 4 2003 Aug 517 526
158. Y. Niwa, T. Suzuki, N. Dohmae, K. Umezawa, and S. Simizu Determination of cathepsin V activity and intracellular trafficking by N-glycosylation FEBS Lett. 586 20 2012 Oct 19 3601 3607
159. D. Kuester, M. Vieth, U. Peitz, S. Kahl, M. Stolte, A. Roessner, and et al. Upregulation of cathepsin W-expressing T cells is specific for autoimmune atrophic gastritis compared to other types of chronic gastritis World J. Gastroenterol. 11 38 2005 Oct 14 5951 5957
160. D. Jechorek, J. Votapek, F. Meyer, A. Kandulski, A. Roessner, and S. Franke Characterization of cathepsin X in colorectal cancer development and progression Pathol. Res. Pract. 210 12 2014 Dec 822 829
161. A.S. Abuelyaman, D. Hudig, S.L. Woodard, and J.C. Powers Fluorescent derivatives of diphenyl [1-(N-peptidylamino)alkyl]phosphonate esters: synthesis and use in the inhibition and cellular localization of serine proteases Bioconjug. Chem. 5 5 1994 Sep-Oct 400 405