Antibacterial activity of and resistance to small molecule inhibitors of the clpp peptidase

ACS Chemical Biology

Volumn 8, Issue 12, 2013, Pages 2669-2677

  Compton, Corey L ^a   Schmitz, Karl R ^b   Sauer, Robert T ^b   Sello, Jason K ^a  

^a BROWN UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BETA LACTONE; ENDOPEPTIDASE CLP; ETHAMBUTOL; ISONIAZID; KANAMYCIN; MOXIFLOXACIN; STREPTOMYCIN; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; DIASTEREOISOMER; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; GENE LOCUS; GROWTH INHIBITION; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; STREPTOMYCES COELICOLOR;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; DRUG RESISTANCE, BACTERIAL; GENETIC COMPLEMENTATION TEST; ISOENZYMES; KINETICS; LACTONES; MICROBIAL SENSITIVITY TESTS; MYCOBACTERIUM TUBERCULOSIS; PROTEOLYSIS; SERINE ENDOPEPTIDASES; STREPTOMYCES COELICOLOR; STRUCTURE-ACTIVITY RELATIONSHIP; TANDEM MASS SPECTROMETRY;

EID: 84890844579     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400577b     Document Type: Article

References (52)

1. Cox, G. and Wright, G. (2013) Intrinsic antibiotic resistance: Mechanisms, origins, challenges and solutions Int. J. Med. Microbiol. 303, 287-292
2. Christian, L., Philippe, G., Mukund, U., Knut, L., Haileyesus, G., and Raviglione, M. (2012) Global tuberculosis control: Lessons learnt and future prospects Nat. Rev. Microbiol. 10, 407-416
3. World Health Organization (2012) Global tuberculosis report. http://apps.who.int/iris/bitstream/10665/75938/1/9789241564502-eng.pdf
4. Dorman, S. and Chaisson, R. (2007) From magic bullets back to the magic mountain: the rise of extensively drug-resistant tuberculosis Nat. Med. 13, 295-298
5. Koul, A., Arnoult, E., Lounis, N., Guillemont, J., and Andries, K. (2011) The challenge of new drug discovery for tuberculosis Nature 469, 483-490
6. Boucher, H., Talbot, G., Bradley, J., Edwards, J., Gilbert, D., Rice, L., Scheld, M., Spellberg, B., and Bartlet, J. (2009) Bad bugs, no drugs: No ESKAPE! an update from the infectious diseases society of America Clin. Infect. Dis. 48, 1-12
7. Raju, R., Ennikrishnan, M., Rubin, D., Krishnamoorthy, V., Kandror, O., Akopian, T., Goldberg, A., and Rubin, E. (2012) Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability in vitro and during infection PLoS Pathog. 8 e1002511
8. Baker, T. and Sauer, R. (2012) ClpXP, an ATP-powered unfolding and protein-degradation machine Biochim. Biophys. Acta, Mol. Cell Res. 1, 15-28
9. Darwin, K., Ehrt, S., Gutierrez-Ramos, J., Weich, N., and Nathan, C. (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide Science 302, 1963-1966
10. Ollinger, J., O'Malley, T., Kesicki, E., Odingo, J., and Parish, T. (2012) Validation of the essential ClpP protease in Mycobacterium tuberculosis as a novel drug target J. Bacteriol. 194, 663-668
11. Sassetti, C. and Rubin, E. (2003) Genetic requirements for mycobacterial survival during infection Proc. Natl. Acad. Sci. U.S.A. 100, 12989-12994
12. Raju, R., Goldberg, A., and Rubin, E. (2012) Bacterial proteolytic complexes as therapeutic targets Nat. Rev. Drug Discovery 11, 777-789
13. Kenniston, J., Baker, T., and Sauer, R. (2005) Partitioning between unfolding and release of native domains during ClpXP degradation determines substrate selectivity and partial processing Proc. Natl. Acad. Sci. U.S.A. 102, 1390-1395
14. Wang, J., Hartling, J., and Flanagan, J. (1997) The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis Cell 91, 447-456
15. Gaillot, O., Pellegrini, E., Bregenholt, S., Nair, S., and Berche, P. (2000) The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes Mol. Microbiol. 35, 1286-1294
16. Robertson, G., Ng, W., Foley, J., Gilmour, R., and Winkler, M. (2002) Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence J. Bacteriol. 184, 3508-3520
17. Xie, F., Zhang, Y., Li, G., Zhou, L., Liu, S., and Wang, C. (2013) The ClpP protease is required for the stress tolerance and biofilm formation in Actinobacillus pleuropneumoniae PloS One 8 e53600
18. Akopian, T., Kandror, O., Raju, R., UnniKrishnan, M., Rubin, E., and Goldberg, A. (2012) The active ClpP protease from M. tuberculosis is a complex composed of a heptameric ClpP1 and a ClpP2 ring EMBO J. 31, 1529-1541
19. Socha, A., Tan, N., LaPlante, K., and Sello, J. (2010) Diversity-oriented synthesis of cyclic acyldepsipeptides leads to the discovery of a potent antibacterial agent Bioorg. Med. Chem. 18, 7193-7202
20. Zeiler, E., Vadim, S., Korotkov, Lorenz-Baath, K., Böttcher, T., and Sieber, S. (2012) Development and characterization of improved β-lactone-based anti-virulence drugs targeting ClpP Bioorg. Med. Chem. 20, 583-591
21. Bottcher, T. and Sieber, S. (2008) β-lactones as specific inhibitors of ClpP attenuate the production of extracellular virulence factors of Staphylococcus aureus J. Am. Chem. Soc. 130, 14400-14401
22. Böttcher, T. and Sieber, S. (2009) β-lactones decrease the intracellular virulence of Listeria monocytogenes in macrophages ChemMedChem 4, 1260-1263
23. Böttcher, T. and Sieber, S. (2009) Structurally refined B-lactones as potent inhibitors of devastating bacterial virulence factors ChemBioChem 10, 663-666
24. Brotz-Oesterhelt, H., Beyer, D., Kroll, H., Endermann, R., Ladel, C., Schroeder, W., Hinzin, B., Raddatz, S., Paulson, H., Henninger, K., Bandow, J., Sahl, H., and Labischinski, H. (2005) Dysregulation of bacterial proteolytic machinery by a new class of antibiotics Nat. Med. 11, 1082-1087
25. Gersch, M., Gut, F., Korotkov, V., Lehmann, J., Bottcher, T., Rusch, M., Hedberg, C., Waldmann, H., Klebe, G., and Sieber, S. (2013) The mechanism of caseinolytic protease (ClpP) inhibition Angew. Chem., Int. Ed. 52, 3009-3014
26. Kirstein, J., Hoffmann, A., Lille, H., Schmidt, R., Rubsamen-Walgmann, H., BrotzOesterhelt, H., Mogk, A., and Turgay, K. (2009) The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease EMBO Mol. Med. 1, 37-49
27. Schmitt, E., Riwanto, M., Sambandamurthy, V., Roggo, S., Miault, C., Zwingelstein, C., Krastel, P., Noble, C., Beer, D., Rao, S., Au, M., Niyomrattanakit, P., Lim, V., Zheng, J., Jeffery, D., Pethe, K., and Camacho, L. (2011) The natural product cyclomarin kills Mycobacterium tuberculosis by targeting the ClpC1 subunit of the caseinolytic protease Angew. Chem., Int. Ed. 123, 6011-6013
28. Cheng, L., Naumann, T., Horswill, A., Hong, S., Venters, B., Tomsho, J., Benkovic, S., and Keiler, K. (2007) Discovery of antibacterial cyclic peptides that inhibit the ClpXP protease Protein Sci. 16, 1535-1542
29. Roberts, D., Personne, Y., Ollinger, J., and Parish, T. (2013) Proteases in Mycobacterium tuberculosis pathogenesis: potential as drug targets Future Microbiol. 8, 621-631
30. Bentley, S., Chater, K., Cerdeno-Tarrage, A., Challis, G., Thomson, N., James, K., Harris, D., Quail, M., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorreck, A., Woodward, J., Barrell, B., Parhill, J., and Hopwood, D. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) Nature 417, 141-147
31. Liu, G., Shirley, M., and Romo, D. (2012) A diastereoselective, nucleophile promoted aldol-lactonization of ketoacids leading to bicyclic-beta-lactones J. Org. Chem. 77, 2496-2500
32. Danheiser, R. and Nowick, J. (1991) A practical and efficient method for the synthesis of β-lactones J. Org. Chem. 56, 1176-1185
33. Lee, M., Baker, T., and Sauer, R. (2010) Control of substrate gating and translocation into ClpP by channel residues and ClpX binding J. Mol. Biol. 399, 707-718
34. Gottesman, S., Roche, E., Zhou, Y., and Sauer, R. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system Genes Dev. 12, 1338-1347
35. Zeiller, E., List, A., Alte, F., Gersch, M., Wachtel, R., Poreba, M., Drag, M., Groll, M., and Sieber, S. (2013) Structural and functional insights into caseinolytic proteases reveal an unprecedented regulation principle of their catalytic triad Proc. Natl. Acad. Sci. U.S.A. 110, 11302-11307
36. Walsh, C. (2000) Molecular mechanisms that confer antibacterial drug resistance Nature 406, 775-781
37. Kieser, T, Bibb, M, Buttner, M, Chater, K, and Hopwood, D. (2000) Practical Streptomyces Genetics. The John Innes Foundation, Norwich, U.K.
38. Vecchione, J. and Sello, J. (2008) Characterization of an inducible, antibiotic-resistant aminoacyl-tRNA synthetase gene in Streptomyces coelicolor J. Bacteriol. 190, 6253-6257
39. Vecchione, J. and Sello, J. (2009) A novel tryptophanyl-tRNA synthetase gene confers high-level resistance to indolmycin Antimicrob. Agents Chemother. 53, 3972-3980
40. Gominet, M., Seghezzi, N., and Mazodier, P. (2011) Acyl depsipeptide (ADEP) resistance in Streptomyces. Microbiology 157, 2226-2234
41. Maurer, K., Pfeiffer, F., Zehender, H., and Mecke, D. (1983) Characterization of two glyceraldehyde-3-phosphate dehydrogenase isoenzymes from the pentalenolactone producer Streptomyces arenae J. Bacteriol. 153, 930-936
42. Thiara, S. and Cundliffe, E. (1988) Cloning and characterization of a DNA gyrase B gene from Streptomyces sphaeroides that confers resistance to novobiocin EMBO J. 7, 2255-2259
43. Viala, J. and Mazodier, P. (2002) ClpP-dependent degradation of PopR allows tightly regulated expression of the clpP3 clpP4 operon in Streptomyces lividans Mol. Microbiol. 44, 633-643
44. Viala, J., Rapoport, G., and Mazodier, P. (2000) The clpP multigenic family in Streptomyces lividans: Conditional expression of the clpP3 clpP4 operon is controlled by PopR, a novel transcriptional activator Mol. Microbiol. 38, 602-612
45. Personne, Y., Brown, A. C., Schuessler, D. L., and Parish, T. (2013) Mycobacterium tuberculosis ClpP proteases are co-transcribed but exhibit different substrate specificities PLoS One 8 e60228
46. Sello, J. (2012) Mining the antibiotic resistome Chem. Biol. 19 (10) 1220-1
47. D'Costa, V., McGrann, K., Hughes, D., and Wright, G. (2006) Sampling the antibiotic resistome Science. 311, 374-377
48. Spanogiannopoulos, P., Thaker, M., Koteva, K., Waglechner, N., and Wright, G. D. (2012) Characterization of a rifampin-inactivating glycosyltransferase from a screen of environmental atinomycetes Antimicrob. Agents Chemother. 56, 5061-5069
49. Forsberg, K., Reyes, A., Wang, B., Selleck, E., Sommer, M., and Dantas, G. (2012) The shared antibiotic resistome of soil bacteria and human pathogens Science 337, 1107-1111
50. Gust, B., Kieser, T., and Chater, K. (2002) REDIRECT technology: PCR-targeting system in Streptomyces coelicolor. http://streptomyces.org.uk/ redirect/protocol-V1-4.pdf
51. Franzblau, S., Witzig, R., McLaughlin, J., Torres, P., Madico, G., Hernandez, A., Degnan, M., Cook, M., Quenzer, V., Ferguson, R., and Gilman, R. (1998) Rapid, low-technology MIC determination with clinical Mycobacterium tuberculosis isolates by using the microplate Alamar Blue assay J. Clin. Microbiol. 36, 362-366
52. Pang, Y., Brown, B., Steingrube, V., Wallace, R., and Roberts, M. (1994) Tetracycline resistance determinants in Mycobacterium and Streptomyces species Antimicrob. Agents Chemother. 38, 1408-1412