Inhibitor Fingerprinting of Rhomboid Proteases by Activity-Based Protein Profiling Reveals Inhibitor Selectivity and Rhomboid Autoprocessing

ACS Chemical Biology

Volumn 10, Issue 10, 2015, Pages 2325-2333

  Wolf, Eliane V ^a   Zeissler, Annett ^a   Verhelst, Steven H L ^a,b,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

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

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; RHOMBOID PROTEASE; RHOMBOID PROTEASE INHIBITOR; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; 3,4-DICHLOROISOCOUMARIN; BACTERIAL PROTEIN; COUMARIN DERIVATIVE; ESCHERICHIA COLI PROTEIN; MOLECULAR LIBRARY; PROTEINASE INHIBITOR;

ACTIVITY BASED PROTEIN PROFILING; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG SCREENING; DRUG SELECTIVITY; ENZYME INHIBITION; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN PROCESSING; SEQUENCE HOMOLOGY; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ENZYME SPECIFICITY; IC50; METABOLISM; MOLECULAR LIBRARY; PROTEIN MICROARRAY;

BACTERIAL PROTEINS; COUMARINS; ESCHERICHIA COLI PROTEINS; INHIBITORY CONCENTRATION 50; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEASE INHIBITORS; PROTEIN ARRAY ANALYSIS; SMALL MOLECULE LIBRARIES; SUBSTRATE SPECIFICITY;

EID: 84944744599     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00514     Document Type: Article

References (45)

1. Wolfe, M. S. (2009) Intramembrane proteolysis Chem. Rev. 109, 1599-1612 10.1021/cr8004197
2. Lemberg, M. K. and Freeman, M. (2007) Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Genome Res. 17, 1634-1646 10.1101/gr.6425307
3. Wang, Y., Zhang, Y., and Ha, Y. (2006) Crystal structure of a rhomboid family intramembrane protease Nature 444, 179-180 10.1038/nature05255
4. Wu, Z., Yan, N., Feng, L., Oberstein, A., Yan, H., Baker, R. P., Gu, L., Jeffrey, P. D., Urban, S., and Shi, Y. (2006) Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry Nat. Struct. Mol. Biol. 13, 1084-1091 10.1038/nsmb1179
5. Ben-Shem, A., Fass, D., and Bibi, E. (2007) Structural basis for intramembrane proteolysis by rhomboid serine proteases Proc. Natl. Acad. Sci. U. S. A. 104, 462-466 10.1073/pnas.0609773104
6. Lemieux, M. J., Fischer, S. J., Cherney, M. M., Bateman, K. S., and James, M. N. (2007) The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis Proc. Natl. Acad. Sci. U. S. A. 104, 750-754 10.1073/pnas.0609981104
7. Urban, S., Lee, J. R., and Freeman, M. (2001) Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107, 173-182 10.1016/S0092-8674(01)00525-6
8. Urban, S. and Wolfe, M. S. (2005) Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity Proc. Natl. Acad. Sci. U. S. A. 102, 1883-1888 10.1073/pnas.0408306102
9. Lemberg, M. K., Menendez, J., Misik, A., Garcia, M., Koth, C. M., and Freeman, M. (2005) Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases EMBO J. 24, 464-472 10.1038/sj.emboj.7600537
10. Brossier, F., Jewett, T. J., Sibley, L. D., and Urban, S. (2005) A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma Proc. Natl. Acad. Sci. U. S. A. 102, 4146-4151 10.1073/pnas.0407918102
11. Jeyaraju, D. V., McBride, H. M., Hill, R. B., and Pellegrini, L. (2011) Structural and mechanistic basis of Parl activity and regulation Cell Death Differ. 18, 1531-1539 10.1038/cdd.2011.22
12. Cheng, T. L., Wu, Y. T., Lin, H. Y., Hsu, F. C., Liu, S. K., Chang, B. I., Chen, W. S., Lai, C. H., Shi, G. Y., and Wu, H. L. (2011) Functions of rhomboid family protease RHBDL2 and thrombomodulin in wound healing J. Invest. Dermatol. 131, 2486-2494 10.1038/jid.2011.230
13. Xue, Y. and Ha, Y. (2012) Catalytic mechanism of rhomboid protease GlpG probed by 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate J. Biol. Chem. 287, 3099-3107 10.1074/jbc.M111.310482
14. Vinothkumar, K. R., Strisovsky, K., Andreeva, A., Christova, Y., Verhelst, S., and Freeman, M. (2010) The structural basis for catalysis and substrate specificity of a rhomboid protease EMBO J. 29, 3797-3809 10.1038/emboj.2010.243
15. Vosyka, O., Vinothkumar, K. R., Wolf, E. V., Brouwer, A. J., Liskamp, R. M., and Verhelst, S. H. L. (2013) Activity-based probes for rhomboid proteases discovered in a mass spectrometry-based assay Proc. Natl. Acad. Sci. U. S. A. 110, 2472-2477 10.1073/pnas.1215076110
16. Xue, Y., Chowdhury, S., Liu, X., Akiyama, Y., Ellman, J., and Ha, Y. (2012) Conformational change in rhomboid protease GlpG induced by inhibitor binding to its S′ subsites Biochemistry 51, 3723-3731 10.1021/bi300368b
17. Sherratt, A. R., Blais, D. R., Ghasriani, H., Pezacki, J. P., and Goto, N. K. (2012) Activity-Based Protein Profiling of the Escherichia coli GlpG Rhomboid Protein Delineates the Catalytic Core Biochemistry 51, 7794-7803 10.1021/bi301087c
18. Pierrat, O. A., Strisovsky, K., Christova, Y., Large, J., Ansell, K., Bouloc, N., Smiljanic, E., and Freeman, M. (2011) Monocyclic beta-lactams are selective, mechanism-based inhibitors of rhomboid intramembrane proteases ACS Chem. Biol. 6, 325-335 10.1021/cb100314y
19. Vinothkumar, K. R., Pierrat, O. A., Large, J. M., and Freeman, M. (2013) Structure of rhomboid protease in complex with beta-lactam inhibitors defines the S2′ cavity Structure 21, 1051-1058 10.1016/j.str.2013.03.013
20. Wolf, E. V., Zeissler, A., Vosyka, O., Zeiler, E., Sieber, S., and Verhelst, S. H. (2013) A new class of rhomboid protease inhibitors discovered by activity-based fluorescence polarization PLoS One 8, e72307 10.1371/journal.pone.0072307
21. Zoll, S., Stanchev, S., Began, J., Skerle, J., Lepsik, M., Peclinovska, L., Majer, P., and Strisovsky, K. (2014) Substrate binding and specificity of rhomboid intramembrane protease revealed by substrate-peptide complex structures EMBO J. 33, 2408-2421 10.15252/embj.201489367
22. Dickey, S. W., Baker, R. P., Cho, S., and Urban, S. (2013) Proteolysis inside the membrane is a rate-governed reaction not driven by substrate affinity Cell 155, 1270-1281 10.1016/j.cell.2013.10.053
23. Cravatt, B. F., Wright, A. T., and Kozarich, J. W. (2008) Activity-based protein profiling: from enzyme chemistry to proteomic chemistry Annu. Rev. Biochem. 77, 383-414 10.1146/annurev.biochem.75.101304.124125
24. Heal, W. P., Dang, T. H. T., and Tate, E. W. (2011) Activity-based probes: discovering new biology and new drug targets Chem. Soc. Rev. 40, 246-257 10.1039/C0CS00004C
25. Serim, S., Haedke, U., and Verhelst, S. H. L. (2012) Activity-based probes for the study of proteases: recent advances and developments ChemMedChem 7, 1146-1159 10.1002/cmdc.201200057
26. Sanman, L. E. and Bogyo, M. (2014) Activity-based profiling of proteases Annu. Rev. Biochem. 83, 249-273 10.1146/annurev-biochem-060713-035352
27. Jessani, N., Liu, Y. S., Humphrey, M., and Cravatt, B. F. (2002) Enzyme activity profiles of the secreted and membrane proteome that depict cancer cell invasiveness Proc. Natl. Acad. Sci. U. S. A. 99, 10335-10340 10.1073/pnas.162187599
28. Wolf, E. V., Seybold, M., Hadravova, R., Strisovsky, K., and Verhelst, S. H. L. (2015) Activity-based protein profiling of rhomboid proteases in liposomes ChemBioChem 16, 1616 10.1002/cbic.201500213
29. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns Proc. Natl. Acad. Sci. U. S. A. 95, 14863-14868 10.1073/pnas.95.25.14863
30. de Hoon, M. J., Imoto, S., Nolan, J., and Miyano, S. (2004) Open source clustering software Bioinformatics 20, 1453-1454 10.1093/bioinformatics/bth078
31. Haedke, U., Gotz, M., Baer, P., and Verhelst, S. H. L. (2012) Alkyne derivatives of isocoumarins as clickable activity-based probes for serine proteases Bioorg. Med. Chem. 20, 633-640 10.1016/j.bmc.2011.03.014
32. Bottcher, T. and Sieber, S. A. (2008) beta-lactones as privileged structures for the active-site labeling of versatile bacterial enzyme classes Angew. Chem., Int. Ed. 47, 4600-4603 10.1002/anie.200705768
33. Jessani, N., Niessen, S., Wei, B. Q. Q., Nicolau, M., Humphrey, M., Ji, Y. R., Han, W. S., Noh, D. Y., Yates, J. R., Jeffrey, S. S., and Cravatt, B. F. (2005) A streamlined platform for high-content functional proteomics of primary human specimens Nat. Methods 2, 691-697 10.1038/nmeth778
34. Chen, G. Y., Uttamchandani, M., Zhu, Q., Wang, G., and Yao, S. Q. (2003) Developing a strategy for activity-based detection of enzymes in a protein microarray ChemBioChem 4, 336-339 10.1002/cbic.200390054
35. Funeriu, D. P., Eppinger, J., Denizot, L., Miyake, M., and Miyake, J. (2005) Enzyme family-specific and activity-based screening of chemical libraries using enzyme microarrays Nat. Biotechnol. 23, 622-627 10.1038/nbt1090
36. Sieber, S. A., Mondala, T. S., Head, S. R., and Cravatt, B. F. (2004) Microarray platform for profiling enzyme activities in complex proteomes J. Am. Chem. Soc. 126, 15640-15641 10.1021/ja044286+
37. Eitelhuber, A. C., Vosyka, O., Nagel, D., Bognar, M., Lenze, D., Lammens, K., Schlauderer, F., Hlahla, D., Hopfner, K. P., Lenz, G., Hummel, M., Verhelst, S. H., and Krappmann, D. (2015) Activity-Based Probes for Detection of Active MALT1 Paracaspase in Immune Cells and Lymphomas Chem. Biol. 22, 129-138 10.1016/j.chembiol.2014.10.021
38. Sik, A., Passer, B. J., Koonin, E. V., and Pellegrini, L. (2004) Self-regulated cleavage of the mitochondrial intramembrane-cleaving protease PARL yields Pbeta, a nuclear-targeted peptide J. Biol. Chem. 279, 15323-15329 10.1074/jbc.M313756200
39. Lazareno-Saez, C., Arutyunova, E., Coquelle, N., and Lemieux, M. J. (2013) Domain swapping in the cytoplasmic domain of the Escherichia coli rhomboid protease J. Mol. Biol. 425, 1127-1142 10.1016/j.jmb.2013.01.019
40. Arutyunova, E., Panwar, P., Skiba, P. M., Gale, N., Mak, M. W., and Lemieux, M. J. (2014) Allosteric regulation of rhomboid intramembrane proteolysis EMBO J. 33, 1869-1881 10.15252/embj.201488149
41. Brouwer, A. J., Ceylan, T., van der Linden, T., and Liskamp, R. M. J. (2009) Synthesis of b-aminoethanesulfonyl fluorides or 2-substituted taurine sulfonyl fluorides as potential protease inhibitors Tetrahedron Lett. 50, 3391-3393 10.1016/j.tetlet.2009.02.130
42. Liu, Y. S., Patricelli, M. P., and Cravatt, B. F. (1999) Activity-based protein profiling: The serine hydrolases Proc. Natl. Acad. Sci. U. S. A. 96, 14694-14699 10.1073/pnas.96.26.14694
43. Kall, L., Krogh, A., and Sonnhammer, E. L. (2004) A combined transmembrane topology and signal peptide prediction method J. Mol. Biol. 338, 1027-1036 10.1016/j.jmb.2004.03.016
44. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9, 671-675 10.1038/nmeth.2089
45. Oakley, B. R., Kirsch, D. R., and Morris, N. R. (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels Anal. Biochem. 105, 361-363 10.1016/0003-2697(80)90470-4