Lassomycin, a ribosomally synthesized cyclic peptide, kills mycobacterium tuberculosis by targeting the ATP-dependent protease ClpC1P1P2

Chemistry and Biology

Volumn 21, Issue 4, 2014, Pages 509-518

  Gavrish, Ekaterina ^a,d   Sit, Clarissa S ^b   Cao, Shugeng ^b   Kandror, Olga ^b   Spoering, Amy ^c   Peoples, Aaron ^c   Ling, Losee ^c   Fetterman, Ashley ^c   Hughes, Dallas ^c   Bissell, Anthony ^a,e   Torrey, Heather ^a   Akopian, Tatos ^b   Mueller, Andreas ^b   Epstein, Slava ^a   Goldberg, Alfred ^b   Clardy, Jon ^b   Lewis, Kim ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NovoBiotic Pharmaceuticals LLC   (United States)

^d Arietis Corp   (United States)

^e BOOZ ALLEN HAMILTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ANTIBIOTIC AGENT; CLPC1P1P2 PROTEASE; CYCLOPEPTIDE; LASSOMYCIN; RIFAMPICIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; PROTEINASE INHIBITOR;

3T3 CELL LINE; ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL VIABILITY; BACTERICIDAL ACTIVITY; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DRUG ISOLATION; DRUG MECHANISM; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME MECHANISM; HEPG2 CELL LINE; MAMMAL CELL; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; MYCOBACTERIUM PARATUBERCULOSIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; RIBOSOME; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; STRUCTURE ACTIVITY RELATION;

CORYNEBACTERINEAE; MAMMALIA; MYCOBACTERIUM TUBERCULOSIS; UNCULTURED BACTERIUM;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ATP-DEPENDENT PROTEASES; DOSE-RESPONSE RELATIONSHIP, DRUG; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PEPTIDES, CYCLIC; PROTEASE INHIBITORS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84899576523     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2014.01.014     Document Type: Article

References (39)

1. T. Akopian, O. Kandror, R.M. Raju, M. Unnikrishnan, E.J. Rubin, and A.L. Goldberg The active ClpP protease from M. tuberculosis is a complex composed of a heptameric ClpP1 and a ClpP2 ring EMBO J. 31 2012 1529 1541
2. P.G. Arnison, M.J. Bibb, G. Bierbaum, A.A. Bowers, T.S. Bugni, G. Bulaj, J.A. Camarero, D.J. Campopiano, G.L. Challis, and J. Clardy et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature Nat. Prod. Rep. 30 2013 108 160
3. G.C. Baker, J.J. Smith, and D.A. Cowan Review and re-analysis of domain-specific 16S primers J. Microbiol. Methods 55 2003 541 555
4. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucleic Acids Res. 28 2000 235 242
5. S. Buerger, A. Spoering, E. Gavrish, C. Leslin, L. Ling, and S.S. Epstein Microbial scout hypothesis and microbial discovery Appl. Environ. Microbiol. 78 2012 3229 3233
6. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
7. B.P. Conlon, E.S. Nakayasu, L.E. Fleck, M.D. LaFleur, V.M. Isabella, K. Coleman, S.N. Leonard, R.D. Smith, J.N. Adkins, and K. Lewis Activated ClpP kills persisters and eradicates a chronic biofilm infection Nature 503 2013 365 370
8. L. Dethlefsen, and D.A. Relman Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4554 4561
9. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA+ proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114
10. T.P. Geladopoulos, T.G. Sotiroudis, and A.E. Evangelopoulos A malachite green colorimetric assay for protein phosphatase activity Anal. Biochem. 192 1991 112 116
11. P. Güntert, C. Mumenthaler, and K. Wüthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
12. P.I. Hanson, and S.W. Whiteheart AAA+ proteins: have engine, will work Nat. Rev. Mol. Cell Biol. 6 2005 519 529
13. J. Inokoshi, M. Matsuhama, M. Miyake, H. Ikeda, and H. Tomoda Molecular cloning of the gene cluster for lariatin biosynthesis of Rhodococcus jostii K01-B0171 Appl. Microbiol. Biotechnol. 95 2012 451 460
14. M. Iwatsuki, H. Tomoda, R. Uchida, H. Gouda, S. Hirono, and S. Omura Lariatins, antimycobacterial peptides produced by Rhodococcus sp. K01-B0171, have a lasso structure J. Am. Chem. Soc. 128 2006 7486 7491
15. T. Kaeberlein, K. Lewis, and S.S. Epstein Isolating " uncultivable" microorganisms in pure culture in a simulated natural environment Science 296 2002 1127 1129
16. I. Keren, S. Minami, E. Rubin, and K. Lewis Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters MBio 2 2011 e00100 e00111
17. T. Kieser, M.J. Bibb, M.J. Buttner, K.F. Chater, and D.A. Hopwood Practical Streptomyces Genetics 2000 The John Innes Foundation Norwich
18. J. Kirstein, A. Hoffmann, H. Lilie, R. Schmidt, H. Rübsamen- Waigmann, H. Brötz-Oesterhelt, A. Mogk, and K. Turgay The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease EMBO Mol Med 1 2009 37 49
19. K. Lewis Antibiotics: recover the lost art of drug discovery Nature 485 2012 439 440
20. K. Lewis Platforms for antibiotic discovery Nat. Rev. Drug Discov. 12 2013 371 387
21. A. Lupas, J.M. Flanagan, T. Tamura, and W. Baumeister Self-compartmentalizing proteases Trends Biochem. Sci. 22 1997 399 404
22. G.M. Morris, R. Huey, W. Lindstrom, M.F. Sanner, R.K. Belew, D.S. Goodsell, and A.J. Olson Autodock4 and AutoDockTools4: automated docking with selective receptor flexiblity J. Comput. Chem. 30 2009 2785 2791
23. D.J. Payne, M.N. Gwynn, D.J. Holmes, and D.L. Pompliano Drugs for bad bugs: confronting the challenges of antibacterial discovery Nat. Rev. Drug Discov. 6 2007 29 40
24. R.M. Raju, M. Unnikrishnan, D.H. Rubin, V. Krishnamoorthy, O. Kandror, T.N. Akopian, A.L. Goldberg, and E.J. Rubin Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability in vitro and during infection PLoS Pathog. 8 2012 e1002511
25. M.C. Rea, C.S. Sit, E. Clayton, P.M. O'Connor, R.M. Whittal, J. Zheng, J.C. Vederas, R.P. Ross, and C. Hill Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile Proc. Natl. Acad. Sci. USA 107 2010 9352 9357
26. J.C. Sacchettini, E.J. Rubin, and J.S. Freundlich Drugs versus bugs: in pursuit of the persistent predator Mycobacterium tuberculosis Nat. Rev. Microbiol. 6 2008 41 52
27. V.K. Sambandamurthy, S.C. Derrick, K.V. Jalapathy, B. Chen, R.G. Russell, S.L. Morris, and W.R. Jacobs Jr. Long-term protection against tuberculosis following vaccination with a severely attenuated double lysine and pantothenate auxotroph of Mycobacterium tuberculosis Infect. Immun. 73 2005 1196 1203
28. E.K. Schmitt, M. Riwanto, V. Sambandamurthy, S. Roggo, C. Miault, C. Zwingelstein, P. Krastel, C. Noble, D. Beer, and S.P. Rao et al. The natural product cyclomarin kills Mycobacterium tuberculosis by targeting the ClpC1 subunit of the caseinolytic protease Angew. Chem. Int. Ed. Engl. 50 2011 5889 5891
29. N.C. Shaner, R.E. Campbell, P.A. Steinbach, B.N. Giepmans, A.E. Palmer, and R.Y. Tsien Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein Nat. Biotechnol. 22 2004 1567 1572
30. C.S. Sit, R.T. McKay, C. Hill, R.P. Ross, and J.C. Vederas The 3D structure of thuricin CD, a two-component bacteriocin with cysteine sulfur to α-carbon cross-links J. Am. Chem. Soc. 133 2011 7680 7683
31. D.F. Smee, A.C. Morrison, D.L. Barnard, and R.W. Sidwell Comparison of colorimetric, fluorometric, and visual methods for determining anti-influenza (H1N1 and H3N2) virus activities and toxicities of compounds J. Virol. Methods 106 2002 71 79
32. D.M. Smith, H. Fraga, C. Reis, G. Kafri, and A.L. Goldberg ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle Cell 144 2011 526 538
33. J.T. Staley, and A. Konopka Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats Annu. Rev. Microbiol. 39 1985 321 346
34. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461
35. D. Vasudevan, S.P. Rao, and C.G. Noble Structural basis of mycobacterial inhibition by cyclomarin A J. Biol. Chem. 288 2013 30883 30891
36. S.R. White, and B. Lauring AAA+ ATPases: achieving diversity of function with conserved machinery Traffic 8 2007 1657 1667
37. A.Y. Yu, and W.A. Houry ClpP: a distinctive family of cylindrical energy-dependent serine proteases FEBS Lett. 581 2007 3749 3757
38. J.H. Zhang, T.D. Chung, and K.R. Oldenburg A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73
39. A. Zumla, P. Nahid, and S.T. Cole Advances in the development of new tuberculosis drugs and treatment regimens Nat. Rev. Drug Discov. 12 2013 388 404