A New Class of Rhomboid Protease Inhibitors Discovered by Activity-Based Fluorescence Polarization

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Wolf, Eliane V ^a   Zeißler, Annett ^a   Vosyka, Oliver ^a   Zeiler, Evelyn ^b   Sieber, Stephan ^b   Verhelst, Steven H L ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYNE; BETA LACTONE DERIVATIVE; ESCHERICHIA COLI PROTEIN; PROTEINASE INHIBITOR; RHOMBOID; RHOMBOID GLPG; RHOMBOID INHIBITOR; SERINE; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; COVALENT BOND; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; ESCHERICHIA COLI; FLUORESCENCE POLARIZATION;

DNA-BINDING PROTEINS; DRUG DISCOVERY; ENDOPEPTIDASES; ESCHERICHIA COLI PROTEINS; FLUORESCENCE POLARIZATION; INHIBITORY CONCENTRATION 50; MEMBRANE PROTEINS; MOLECULAR PROBES; PROTEASE INHIBITORS; SUBSTRATE SPECIFICITY;

EID: 84882749003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072307     Document Type: Article

References (41)

1. Wolfe MS, (2009) Intramembrane proteolysis. Chem Rev 109: 1599-1612.
2. Lemberg MK, (2011) Intramembrane proteolysis in regulated protein trafficking. Traffic 12: 1109-1118.
3. Weihofen A, Martoglio B, (2003) Intramembrane-cleaving proteases: controlled liberation of proteins and bioactive peptides. Trends Cell Biol 13: 71-78.
4. Koonin EV, Makarova KS, Rogozin IB, Davidovic L, Letellier MC, et al. (2003) The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol 4: R19.
5. Lemberg MK, Freeman M, (2007) Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases. Genome Res 17: 1634-1646.
6. Urban S, Lee JR, Freeman M, (2001) Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107: 173-182.
7. Stevenson LG, Strisovsky K, Clemmer KM, Bhatt S, Freeman M, et al. (2007) Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc Natl Acad Sci USA 104: 1003-1008.
8. Baker RP, Wijetilaka R, Urban S, (2006) Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog 2: e113.
9. Brossier F, Jewett TJ, Sibley LD, Urban S, (2005) A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc Natl Acad Sci USA 102: 4146-4151.
10. O'Donnell RA, Hackett F, Howell SA, Treeck M, Struck N, et al. (2006) Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 174: 1023-1033.
11. Wang Y, Zhang Y, Ha Y, (2006) Crystal structure of a rhomboid family intramembrane protease. Nature 444: 179-180.
12. Ben-Shem A, Fass D, Bibi E, (2007) Structural basis for intramembrane proteolysis by rhomboid serine proteases. Proc Natl Acad Sci USA 104: 462-466.
13. Wu Z, Yan N, Feng L, Oberstein A, Yan H, et al. (2006) Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry. Nat Struct Mol Biol 13: 1084-1091.
14. Wang Y, Maegawa S, Akiyama Y, Ha Y, (2007) The role of L1 loop in the mechanism of rhomboid intramembrane protease GlpG. J Mol Biol 374: 1104-1113.
15. Vinothkumar KR, Strisovsky K, Andreeva A, Christova Y, Verhelst S, et al. (2010) The structural basis for catalysis and substrate specificity of a rhomboid protease. EMBO J 29: 3797-3809.
16. Xue Y, Ha Y, (2012) Catalytic mechanism of rhomboid protease GlpG probed by 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate. J Biol Chem 287: 3099-3107.
17. Xue Y, Chowdhury S, Liu X, Akiyama Y, Ellman J, et al. (2012) Conformational change in rhomboid protease GlpG induced by inhibitor binding to its S' subsites. Biochemistry 51: 3723-3731.
18. Vosyka O, Vinothkumar KR, Wolf EV, Brouwer AJ, Liskamp RM, et al. (2013) Activity-based probes for rhomboid proteases discovered in a mass spectrometry-based assay. Proc Natl Acad Sci USA 110: 2472-2477.
19. Vinothkumar KR, Pierrat OA, Large JM, Freeman M, (2013) Structure of Rhomboid Protease in Complex with beta-Lactam Inhibitors Defines the S2' Cavity. Structure 21: 1051-1058.
20. Sherratt AR, Blais DR, Ghasriani H, Pezacki JP, Goto NK, (2012) Activity-Based Protein Profiling of the Escherichia coli GlpG Rhomboid Protein Delineates the Catalytic Core. Biochemistry 51: 7794-7803.
21. Pierrat OA, Strisovsky K, Christova Y, Large J, Ansell K, et al. (2011) Monocyclic beta-lactams are selective, mechanism-based inhibitors of rhomboid intramembrane proteases. ACS Chem Biol 6: 325-335.
22. Lemberg MK, Menendez J, Misik A, Garcia M, Koth CM, et al. (2005) Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases. EMBO J 24: 464-472.
23. Urban S, Wolfe MS, (2005) Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity. Proc Natl Acad Sci USA 102: 1883-1888.
24. Maegawa S, Ito K, Akiyama Y, (2005) Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane. Biochemistry 44: 13543-13552.
25. Bachovchin DA, Brown SJ, Rosen H, Cravatt BF, (2009) Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes. Nat Biotechnol 27: 387-394.
26. Cravatt BF, Wright AT, Kozarich JW, (2008) Activity-based protein profiling: from enzyme chemistry to proteomic chemistry. Annu Rev Biochem 77: 383-414.
27. Heal WP, Dang THT, Tate EW, (2011) Activity-based probes: discovering new biology and new drug targets. Chem Soc Rev 40: 246-257.
28. Sadaghiani AM, Verhelst SH, Bogyo M, (2007) Tagging and detection strategies for activity-based proteomics. Curr Opin Chem Biol 11: 20-28.
29. Bachovchin DA, Wolfe MR, Masuda K, Brown SJ, Spicer TP, et al. (2010) Oxime esters as selective, covalent inhibitors of the serine hydrolase retinoblastoma-binding protein 9 (RBBP9). Bioorg Med Chem Lett 20: 2254-2258.
30. Lone AM, Bachovchin DA, Westwood DB, Speers AE, Spicer TP, et al. (2011) A substrate-free activity-based protein profiling screen for the discovery of selective PREPL inhibitors. J Am Chem Soc 133: 11665-11674.
31. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73.
32. Antos JM, Chew GL, Guimaraes CP, Yoder NC, Grotenbreg GM, et al. (2009) Site-specific N- and C-terminal labeling of a single polypeptide using sortases of different specificity. J Am Chem Soc 131: 10800-10801.
33. Haedke U, Gotz M, Baer P, Verhelst SHL, (2012) Alkyne derivatives of isocoumarins as clickable activity-based probes for serine proteases. Bioorg Med Chem 20: 633-640.
34. Bottcher T, Sieber SA, (2008) beta-lactones as privileged structures for the active-site labeling of versatile bacterial. Angew Chem Int Ed Engl 47: 4600-4603.
35. Zeiler E, Braun N, Bottcher T, Kastenmuller A, Weinkauf S, et al. (2011) Vibralactone as a tool to study the activity and structure of the ClpP1P2 complex from Listeria monocytogenes. Angew Chem Int Ed Engl 50: 11001-11004.
36. Pitscheider M, Maeusbacher N, Sieber SA, (2012) Antibiotic activity and target discovery of three-membered natural product-derived heterocycles in pathogenic bacteria. Chem Sci 3: 2035-2041.
37. Powers JC, Asgian JL, Ekici OD, James KE, (2002) Irreversible inhibitors of serine, cysteine, and threonine proteases. Chem Rev 102: 4639-4750.
38. Serim S, Haedke U, Verhelst SH, (2012) Activity-based probes for the study of proteases: recent advances and developments. ChemMedChem 7: 1146-1159.
39. Bachovchin DA, Ji T, Li W, Simon GM, Blankman JL, et al. (2010) Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening. Proc Natl Acad Sci USA 107: 20941-20946.
40. Bottcher T, Sieber SA, (2008) beta-Lactones as Specific Inhibitors of CIpP Attenuate the Production of Extracellular Virulence Factors of Staphylococcus aureus. J Am Chem Soc 130: 14400-14401.
41. Bottcher T, Sieber SA, (2009) beta-Lactones Decrease the Intracellular Virulence of Listeria monocytogenes in Macrophages. ChemMedChem 4: 1260-1263.